HORTICULTURAL REVIEWS VOLUME 2
HORTICULTURAL REVIEWS VOLUME 2
edited by
JulesJanick Purdue University
avi
AVI PUBLISHING COMPANY, INC. W estport, Connecticut
0 Copyright 1980 by THE AVI PUBLISHING COMPANY, INC. Westport, Connecticut
All rights reserved. No part of this work covered by the copyright hereon may be reproduced or used in any form or by any means-graphic, electronic, or mechanical, including photocopying, recording, taping, or information storage and retrieval systems-without written permission of the publisher.
ISSN-0163-7851 ISBN-0-87055-352-6
Printed in the United States of America by Eastern Graphics, Inc., Old Saybrook, Connecticut
Horticultural Reviews is co-sponsored by the American Society for Horticultural Science and The AVI Publishing Company
Editorial Board, Volume 2 Frank G. Dennis, Jr. Donald N. Maynard Marlin N. Rogers
John Robert Magness
Dedication
This book is dedicated to Dr. John Robert Magness, premier pomologist, whose outstanding contributions to fruit research covered nearly 50 years. Dr. Magness has been a leader in fruit research for most of this century. He talks about his many accomplishments in his characteristically shy manner. In preparing a recent review on the evolution of fruit nutrition during the lifetime of our professional society, I asked Dr. Magness to relate his first-hand experiences in fruit nutrition during this period. “I cannot do t h a t . . . , ” he replied, “ . . . the society started in 1903 and the earliest I can remember professionally is 1910.” Since 1910, Dr. Magness’ accomplishments have marked every phase of fruit research and production. In the early 1920’s he was the leader in postharvest fruit physiology. His desire to quantify changes during the maturation of fruit resulted in the development of the Magness-Taylor pressure tester that is still in wide use today. Dr. Magness was the leading innovator in nutritional research in the 1930’s and by introducing leaf analysis into commercial orchards, he revolutionized fruit nutrition. He was in the forefront in studying noninfectious physiological disorders-most notably, internal cork of apples. Under his guidance the first applications of growth regulators, stop drop sprays, and fruit thinners were made in the 1940’s. These chemical treatments not only had a great impact on fruit production, but started an important trend toward the use of growth regulators for agriculture in general. He recognized and encouraged breeding for disease resistance 30 years before this became a general concern. Dr. Magness was an outstanding research administrator. He had an unusual ability to stimulate research and to appreciate the accomplishments of others. His love of research and dedication to improvement of fruit production remained with him throughout his career as a research administrator for USDA’s Bureau of Plant Industry. vii
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H e was uncomfortable when he was not doing research himself. When . . . personnel thought th at administrators should not do research . . . ” he retired and dedicated his services to horticulture as the Editor of 15 volumes of the Proceedings of the American Society for Horticultural Science. Dr. Magness’ success may be attributed to his excellent knowledge of tree physiology and fruit production; his unparalleled ability to observe various phenomena in the orchards; his unusual ability to evaluate his own work and that of others in an unbiased manner; his willingness to cooperate with others and to encourage them to seek the new; and his optimism and enthusiasm th at has been an inspiration to all his peers. John Magness, a t the age of 86, is still active and interested in new developments. Th e dedication of this book to him is but a small tribute to his greatness. “
Miklos Faust Fruit Laboratory Horticultural Research Institute Science and Education Administration U S . Department of Agriculture Beltsville, Maryland
Contributors
ATKINSON, DAVID, Department of Pomology, East Malling Research Station, Maidstone, Kent, United Kingdom BARKER, ALLEN V., Department of Plant and Soil Sciences, University of Massachusetts, Amherst, Massachusetts BASS, L.N., United States Department of Agriculture, Science and Education Administration, Agricultural Research, National Seed Storage Laboratory, Fort Collins, Colorado CALDAS, L.S., Departmento de Botanica, Universidade de Brasilia, Brasilia, DF, Brazil CAMPBELL, LOWELL E., United States Department of Agriculture, Beltsville, Maryland CATHEY, HENRY M., United States Department of Agriculture, Beltsville, Maryland DOUD, S.L., Division of Agriculture, Fort Valley State College, Fort Valley, Georgia FAUST, M., Fruit Laboratory, Horticultural Research Institute, Science and Education Administration, United States Department of Agriculture, Beltsville, Maryland FERY, RICHARD L., United States Vegetable Laboratory, Agricultural Research, Science and Education Administration, United States Department of Agriculture, Charleston, South Carolina JACKSON, JOHN E., Department of Pomology, East Malling Research Station, Maidstone, Kent, United Kingdom MARAFFA, S.B., Department of Horticulture, Ohio State University, Columbus, Ohio MILLS, HARRY A., Department of Horticulture, University of Georgia, Athens, Georgia RYDER, EDWARD J . , United States Agricultural Research Station, ix
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1636 East Alisal Street, P.O. Box 5098, Salinas, California SHARP, W.R., Pioneer Research Laboratory, Campbell Institute for Agricultural Research, 261 1 Branch Pike, Cinnaminson, New Jersey SHEAR, C.B., Fruit Laboratory, Horticultural Research Institute, Science and Education Administration, United States Department of Agriculture, Beltsville, Maryland SONDAHL, M.R., Departmento de Genetica, Instituto Agronomica, Caxia Postal 28, 13.100 Campinas, S.P., Brazil WHITAKER, THOMAS W., United States Department of Agriculture, P.O. Box 150, La Jolla, California YADAVA, U.L., Division of Agriculture, Fort Valley State College, Fort Valley, Georgia
Contents
DEDICATION vii 1 The Short Life and Replant Problems of Deciduous Fruit Trees 1 U.L. Yadava and S.L. Doud 2 Seed Viability During Long-Term Storage 117 L.N. Bass 3 Nutritional Ranges in Deciduous Tree Fruits and Nuts 142 C.B. Shear and M. Faust 4 The Lettuce Industry in California: A Quarter 164 Century Edward J. Ryder and Thomas W. Whitaker 5 Light Interception and Utilization by Orchard 208 Systems John E. Jackson 6 The Physiology of Asexual Embryogenesis 268 M.R. Sondahl, L.S. Caldas, S.B. Maraffa and W.R. Sharp 7 Geneticsof Vigna 311 Richard L. Fery 8 Ammonium and Nitrate Nutrition of Horticultural Crops 395 Allen V. Barker and Harry A. Mills 9 The Distribution and Effectiveness of the Roots of 424 Tree Crops David Atkinson 10 Light and Lighting Systems for Horticultural Plants 491 Henry M. Cathey and Lowell E. Campbell 539 INDEX (VOLUME 2) CUMULATIVE INDEX (VOLUMES 1-2) 541 xi
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
1 The Short Life and Replant Problems of Deciduous Fruit Trees1 U.L. Yadava and S.L. Doud2
Fort Valley State College, Fort Valley, Georgia 31030 I. TheProblem 3 A. Introduction 3 B. Economic Impact. 4 C. Distribution 5 D. Symptomology 10 15 11. Methods to Study the Problem A. Electrophysiological 15 B. Chemical and Biochemical 17 18 C. Isolation, Culture, and Bioassay D. Inoculation 19 23 E. Discoloration and Tissue Integrity F. Regrowth 23 G. Other Methods 24 111. Causal Factors 26 A. Environmental Factors 26 1.Macroclimatic (Natural) 26 a. Cold (Winter, Freeze or Frost) Injury i. Dormancy 27 ii. Extent of Injury 30 iii. Type of Injury 30 iv. Mechanism of Injury 31 32 v. Effect on Tree Life vi. Cold Hardiness 33
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'The survey of literature pertaining to this review was completed in May 1978. The authors wish to thank Drs. C.N. Clayton, M. Faust, A. Jones, R.E.C. Layne, E.L. Proebsting, Jr. and M.N. Westwood for helpful suggestions regarding the outline of this manuscript, and Mrs. Cynthia J. Andrews and Miss Donna M. Bird for assistance in preparation. 2Research Scientists, SEA/CR Agricultural Research, Division of Agriculture.
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b. Other Stresses 34 i. Water (Drought, Desiccation) 34 ii. Oxygen Deficiency (Wet-feet) 36 iii. Temperature Extremes 36 37 iv. Combination of Above Factors 2. Microclimatic (Cultural) 37 a. Cultural Practices 37 i. Crop Rotation 37 ii. Pruning and Training 38 39 iii. Cover Crops, Mulch, and Weed Control 40 iv. Irrigation and Tillage Operations b. Nutritional 41 41 i. Soil pH and Liming 42 ii. Type and Amount of Fertilizers iii. Time of Fertilization 43 44 iv. Nutritional Deficiencies and Interactions B. Pathogenic Factors 46 1.Bacteria 46 2.Fungi 41 3. Nematodes 49 50 4. Viruses and Mycoplasma-Like Organisms (MLO) 5. Insects 52 6. Pathogenic Interaction 52 C. Physio-Biochemical Factors 53 1.Phytotoxins 53 a. Microbial Phytotoxins 53 b. Plant Residues 54 c. Spray Residues 55 d. Other Phytotoxins 56 2. Biochemicals 57 a. Carbohydrates (CHO) 57 58 b. Proteins and Other Nitrogenous Compounds 58 c. Fatty and Organic Acids d. Phenolics 59 e. Other Biochemicals 59 60 3. Phytohormones and Growth Regulators a. Promoters 61 i.Auxins 61 ii. Gibberellins (GA) 62 iii. Cytokinins (CYK) 62 b. Inhibitors 63 i. Abscisic Acid (ABA) 64 ii. Other Inhibitors 64 c. Phytohormonal Interaction 65 IV. Control Measures 66 66 A. Plant Improvement Through Breeding for Resistance 70 B. Rootstocks
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C. Cultural Practices 75 D. Control of Pathogens 79 E. Miscellaneous Controls 81 1.Fumigation 82 2. Steam Sterilization 83 3. Other Methods 84 V. Conclusion 84 VI. Literaturecited 85
I. THE PROBLEM A. Introduction There are numerous causal factors that can devitalize, weaken or even kill the trees in a fruit orchard. The “short life” or “replant” problem is only one of many such problems which face the growers. The situation is widespread throughout the world (Shannon and Christ 19541, but the same problem as such does not necessarily occur in different growing areas or in all orchards within a specific region. The so-called fruit tree short life or replant problem, as recognized in different forms in various parts of the world, has been reported for more than two centuries (Gilmore 1959; Savory 1966). Other problems causing premature death of young trees are more recent. Some of these problems, such as pear decline and stem pitting, are detrimental for all ages of trees, but they could be a major cause for failure to establish an orchard a t a given site. For this reason, these problems are included in this review. The terms “replant” and “replanting” indicate, by definition, the second or following plantings of the same or a closely related species a t a given site (Savory 1966). The problem was named specific apple replant disease (SARD) by preference over “specific problem” or “specific sickness.” Discussing specific replant diseases of apple and cherry, Savory (1967) gave the following characteristic features of these types of disorders: (a) they are specific to a certain degree-occurring when a species is planted following its own type; (b) they inhibit root growth-affected plants have weak, necrotic, and sparsely branched roots and the top/root ratio of such trees is reduced; (c) there are no leaf symptoms-characteristically, however, in the first year shoot growth on affected trees ceases earlier than that on healthy trees, while in the second year of growth retarded replants have considerably fewer growing shoots than healthy trees; (d) replant diseases directly affect trees only in the first year after planting whereafter replants and healthy trees have very similar relative growth rates, though affected replants do not catch up with healthy trees soon; (e) replant diseases persist in the soil for very
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long periods-just how long is not known. Donoho e t al. (1967) used the term “apple tree decline” (ATD) for the condition of loss of tree vigor and productivity th at occurred for no apparent reason with no improvement due to management practices. Proebsting (1950), Gilmore (1949,1959), and Clayton (1968) pointed out the basic characteristic of the replant problem, by indicating the high degree of specificity as evident from peach failure following peach but not when following apple, and the reverse also being true where other fruits do well after peach. According to Clayton (1975a), the problem might be considered to be of two overlapping types: (a) stunting or retardation of growth, an d (b) death of trees. T h e latter is now called peach tree short life (PTSL), a term coined a few years ago to denote the disease syndrome consisting of bacterial canker, blast, decline, sour-sap, die-back, sudden death, gummosis, apoplexy, winter injury, cold injury, etc., as applied to the death of peach trees in late winter or early spring which for all appearances were healthy in the preceding fall (Clayton 1977). From the conflicting observations it appears th a t the short life and replant problem is a complex one, for which no single factor is responsible. Since there are so many problems by name and nature, obviously there will be no total agreement on one single nomenclature or classification for each problem or complex thereof. However, we will attempt to limit our discussion to those well documented problems which contribute to shortened tree life expectancy or failure in the establishment of the replants, usually through soil or site factors in conjunction with environmental and/or other stresses. This generally would exclude the disorders which are purely pathological in nature.
B. Economic Impact Hickey (1962) found in New York state th a t Cytospora canker severely reduced the production life of peach trees which earlier were weakened by cold injury. In Poland, bacterial canker of sweet cherry, incited by Pseudomonas mors-prunorum Wormald, recently has become a devastating disorder resulting in an acute shortage of sweet cherry trees in nurseries (Lyskanowska 1976). Gardan (1975) reported 300,000 tree deaths in the principal peach-growing area of France as a result of the cold injury-bacterial canker complex. McGlohon and Ferree (1976) reported t ha t the peach tree population in Georgia dropped from 1 6 million trees in 1930 to less than 3 million trees in 1960, and th a t the primary causal factor for this decrease in tree number was peach tree decline, now called peach tree short life (PTSL). According to Sharpe (1974), a n estimated half million trees, mostly under six years of age, succumbed to
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PTSL in 1972-1973 in the peach areas of southeastern United States. In central Georgia alone, for example, the recent average life-span of peach trees was cited as eight years and in the whole Southeast, as only about ten years (Fogle 1975; Hendrix and Powell 1969). This contrasts with a nearly 20-year life expectancy only a few decades ago. In fact, trees begin dying before the orchard reaches full productivity and this tremendous tree loss soon leaves the orchard operations unprofitable, making another replanting absolutely necessary. Many replanted orchards never reach production stage, i.e., the replants fail to establish, especially when replanted immediately following peaches on old (short-life) sites (Hendrix and Powell 1969).
C. Distribution The purpose of this review is not to deal individually with each of the problems affecting the different deciduous fruit trees, nor even all of the problems of the same tree fruit. Instead, it will focus on the distribution of only those problems which are recognized a s contributing towards the shortening of the tree vitality, as well a s those having a significant economic impact on cultivation of pome and stone fruits in the major production areas. Some of the well documented problems of these pomaceous fruit trees are enumerated as follows. Parker et al. (1966) reported from New York state th a t in some sites where root damage was especially severe new trees of apple, cherry, peach, plum, and pear could not be established after old orchards of the same crops were removed. Referring to the apple replant problem in quartz sand in Germany, Bunemann and Jensen (1970) mentioned th a t thoroughly washed quartz sand used previously in culture experiments inhibited seed germination and growth of apple seedlings, a s well as grafts. Banta (1960), Beattie (1962), Beattie et al. (1963), and Donoho et al. (1967) described a serious disorder of old apple orchards (usually 20 to 25 years or older) in the eastern United States a s apple tree decline. Ross and Crowe (1973, 1976) have reported incidences of a n apple replant disease in Nova Scotia, Canada. Refatti (1970a,b) has reported from the Valtellina area of Italy, where apple decline, affecting only ‘Delicious’ trees of ages from 5 to 19 years, has reached epidemic levels. However, a sharp increase in incidence was observed in the first two years of growth after the initial outbreak. This specific decline phenomenon, therefore, appeared to be different from usual decline experienced in Italy and also from certain other syndromes specific to ‘Delicious’ trees in other parts of the world. Stouffer et al. (1977) reported a n apple union necrosis and decline disorder which also affects the bud union integrity and scion growth of young trees in the Pennsylvania area. Occurrence of stem
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pitting and necrosis in some bodystocks for apple trees has been observed in New Hampshire by Smith (1954). Welsh and Spangelo (1971) reported that necrotic stem pitting and decline, two bud-transmissible diseases of apple, affected M a l u s robusta No. 5 apple rootstock severely in British Columbia but not in eastern Canadian provinces. Kaminska (1973a,b), Kaminska e t al. (1971), Kaminska and Zawadzka (1973), and Kunze (1972) provided a detailed discussion of the apple proliferation disorder in Poland which was more acute on 1- to 5- than on 12-year-old trees. Paulechova and Rakus (1971) found apple proliferation problem severely damaging to ‘Golden Delicious’ and other native cultivars in Czechoslovakia. Benson (1974a,b) mentioned an apple replant problem on old apple sites (apple following apple on the same site) in Washington state, and associated it with soil arsenic toxicity, non-specific disease organisms, and SARD. The latter problem has been emphasized in recent years (Benson and Covey 1976; Benson e t al. 1978). Apple replant disease also has been reported from England (Jackson 1973; Pitcher e t al. 1966) and New Zealand (Ryan 1975a,b). This disorder specifically affects apples on old apple sites without an apparent involvement of nematodes. Hoestra (1967, 1968) reported an apple replant problem in the Netherlands, with two main distinguishable characteristics: damage by Pratylenchus penetrans (Cobb) nematode on light soils, and SARD, not caused by nematodes, on heavy soils with near-neutral soil pH. A similar decline problem has been reported from Australia by Sitepu and Wallace (19741, who correlated P y t h i u m species, nematodes, and soil p H with the inhibition of growth (in terms of trunk circumference) of apple trees. Colbran (1953), also from Australia, reported poor and unthrifty growth of apple trees when used as replants in old apple orchards. Researchers from Germany (Borner 1959; Otto 1972a,b,c,d; Winkler and Otto 1972) reported a similar problem, occurring mainly as a result of soil sickness, which the nurserymen encountered after a cultivation of apples for one to two years on old apple sites. Apple decline, as related to canker and die-back diseases caused by Stereum p u r p u r e u m (Pers.) Fr., has been reported recently in two separate studies in Wisconsin (Setlife and Wade 1973) and in Himachal Pradesh, India (Shandilya 1974). Phytophthora collar rot, which produces cankers below the ground line and mostly on clonal rootstocks, has been reported in Michigan (Jones 1971b) as well as in the Rio Negro and the Nequen Valleys in Argentina (Sarasola and de Bustamante 1970). A thorough review on decline, replant, and other short life problems of pear has been published by the Pear Research Task Group of the University of California (Anon. 1971). Researchers from various regions have reported “Pear Blast,” which affected all commercial cultivars of pear in Connecticut (Sands and Kollas 1974), is widespread in the USSR
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(Dorozhkin and Griogortsevich 1976), and had existed for a t least a de cade in Chile (Cancino et al. 1974). The problem typically occurs in wet weather near bloom time. In the Pacific Coast states of the United States, pear decline, which was first recognized in 1956 (Westwood and Lombard 1977), develops with a gradual loss of tree vigor and reaches the advanced stage upon the attainment of severe or complete suppression of terminal growth (Batzer and Schneider 1960; Woodbridge and Lasheen 1960). In recent years, increases in the occurrence of pear decline have been reported from other parts of the world also (Agrios 1972; Blattny and Vana 1974; Luisetti and Paulin 1972; Luisetti et al. 1973; Rallo 1973; Sarasola and de Bustamante 1970; Schmid 1974; Seemuller and Kunze 1972; Soma and Schneider 1971). Spivey and McGlohon (1973) noted that decline and eventual death of young peach trees has been a world-wide problem for more than a century. Of the peach replants which die, most are those planted in locations from which an old tree recently has been removed (Upshall and Ruhnke 1935). Chandler et al. (1962) used the term “sudden decline” for a disorder of peach trees in Georgia which, in the early spring of 1962, resulted in the sudden death of about 200,000 trees a t or shortly after bloom. Chitwood (1949) associated the decline and replant problems in Maryland peach orchards with ring nematodes of the genus Criconemoides (now called Macroposthonia (Raski) Loof de Grisse). PTSL in North Carolina has been linked with the cold injury-Cytospora cankerbacterial canker complex (Clayton 1968, 1972, 1975a,b, 1977). Often trees from four to seven years old are most affected, and tops are killed to the soil line while roots are still alive. Daniel1 and Crosby (1970, 1971) preferred the terminology “quick” and “slow” decline for the PTSL syndrome, depending on its rate of advance towards killing or devitalizing trees. In Pennsylvania, the peach replanting problem on old sites has been associated with the failure to give replants a rapid early start with readily available source of nitrogen to overcome inhibition caused by previous crops (Hewetson 1957). Hung and Jenkins (1969) have recognized the peach replant syndrome in New Jersey to be a complex of nematodes and one or more cultural or other factors. The disorder also has been well documented in the western United States; however, the “peach replant problem” is the terminology preferred (Gilmore 1949, 1959, 1963; Proebsting 1950; Proebsting and Gilmore 1941). T h e reduction of tree growth in old peach soil, both in containers and in the field, has been associated with various soil-borne factors (Proebsting and Gilmore 1941). Another report from California by De Vay et al. (1967) stated that the decline of peach trees is a chronic root problem affecting 2- to 16-year-old trees, particularly in light soils. In Ontario, serious difficulties are frequent in the establishment of replants on old
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orchard sites (Koch 1955; Mountain and Boyce 1957, 1958a,b; Mountain and Patrick 1959; Patrick 1955; Ward and Durkee 1956; Wensley 1956). Agrios (1971) reported from Greece that peach and apricot trees die within three to four years of first tree decline symptoms. Mizutani et al. (1977) reported that the peach replant problem in Japan associated with root cyanogenesis under anaerobic conditions. The microbial aspect of peach replant disease, as related to rhizosphere effects, has been reported from Italy by Lepidi et al. (1974). Scotto La Massese et al. (1973) and Vigouroux et al. (1972) have presented a complete analysisof peach decline in France. A bark gummosis of peach trees caused by Botryosphaeria dothidea (Moug. ex Fr.) Ces. and de Not. reportedly has seriously affected thousands of trees in central Georgia (Weaver 1974b). Chirilei et al. (1970) showed that gummosis was responsible for premature decline of apricot trees in Romania. Heimann (1968) described an apricot gummosis in Germany which caused incidences of die-back over a period of six years. Gummosis has been reported also to be a result of Pseudomonas syringae (van Hall) infection in Hungary (Babos et al. 1976) and of Vulsa canker in Czechoslovakia (Rosik et al. 1971). Peach rosette and decline have been reported from Australia (Smith and Neales 1977; Smith et al. 1977a,b; Stubbs and Smith 1971) a s an important problem but not as a short life or replant problem. A decline condition of plum, closely resembling that affecting prune trees in New York state, probably caused by a strain of Prunus necrotic ringspot virus, has been reported in England (Posnette and Cropley 1970). Preliminary reports on cherry decline (Fos 1976) and apricot decline (Gardan et al. 1973) in France have been published. Cherry decline also has been reported from East Germany (Kegler et al. 1973). The apoplexy disorder of apricots has been reported from Hungary (Babos et al. 1976; Klement et al. 1972, 1974; Rozsnyay and Barna 1974; Rozsnyay and Klement 1973), Greece (Kouyeas 1971), Poland (Paclt 1972), Bulgaria (Iliev 1968), and other countries (Frenyo and Buban 1976). Perennial canker, caused by two related fungi, Cytospora cincta Sacc. and C. leucostoma Sacc., has been associated with killing young trees of peach, apricot, prune, plum, and sweet cherry plantings in many parts of the world; C. cincta is more common on apricots while C. leucostoma is predominant on peach (Clayton 1971; Hampson and Sinclair 1973; Hickey 1962; Jones 1971b; Stanova 1977; Weaver 1963). Bacterial canker, incited by Pseudomonas syringae van Hall and Ps.mors-prunorum Wormald, is another serious cankerous disorder prevalent on many stone fruits around the world (Davis 1968; Davis and English 1965, 1969a,b; Dorozhkin and Griogortsevich 1976; English 1961;
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Jones 1971a,b; Klement et al. 1974; Lyskanowska 1976; Prunier, Gardan and Luisetti 1970; Prunier, Luisetti and Gardan l970,1973a,b; Psallidas and Panagopoulos 1975; Weaver et al. 1974). Pseudomonas syringae canker problem has been closely associated with PTSL or decline disease of peaches (Cameron 1971b; Clayton 1968; Dowler and Petersen 1966; French and Miller 1974; Gardan et al. 1975; Lyskanowska 1976; Savage and Cowart 1942a; Zehr et al. 1976; Petersen 1975; Petersen and Dowler 1965). X-disease, so named because of its mysterious nature, still causes large losses in peach (Cochran 1975), and cherries (Granett and Gilmer 1971; Jensen 1971) on the West Coast of the United States though reported to be under control in the eastern United States (Sands and Walton 1975). In the eastern United States and Ontario, X-disease attacks peach, nectarine, sweet cherry, and tart cherry (Dhanvantari and Kappell978; Jones 1971b; Lukens et al. 1971; McKee et al. 1972; Rosenberger and Jones 1977; Sands and Walton 1975). In mid-Atlantic states of the United States, a new disorder called “stem pitting” was found to be responsible for the girdling, decline, and death of peach trees of various ages in 1967 (Jones 1971b). This disorder causes a sizeable problem in almost all stone fruits. A survey of declining stone fruit orchards in California (Mircetich et al. 1977) revealed widespread incidences of P r u n u s stem pitting (PSP),which is graft-transmissible (Smith and Stouffer 1975). Hutchins (1933) related phony virus peach disorder as one of the several major factors reducing productive life of peach trees in Georgia. Savage and Cowart (1942a) and Rhoads (1954) reported similar findings about the impact of phony on PTSL. Armillaria root rot, caused by fungus Armillaria mellea (Vahl) Quel, is another disorder which often eliminates otherwise good orchard sites from production (Jones 197l b ; Wilbur et al. 1972), and appears as one of the important factors responsible for affecting peach tree longevity in Georgia (Savage and Cowart 1942a). Other fungal disorders associated with the short life and decline of fruit trees have been cited as Clitocybe tabescens (Scop. ex Fr.) Bres. (Chandler 1969; Cohen 1963; Petersen 1961; Savage and Cowart 1942a, 1954; Savage et al. 1953; Weaver 1974a), Cylindrocladium species (Sobers and Seymour 1967;Weaver 1971), Pythium species (Hendrix and Powell 1970b; Hine 1961b; Mircetich and Keil 1970; Powell et al. 1965; Taylor et al. 1970), Phytophthora species (Hendrix and Powell 1970b; Jones 1971b; Mircetich and Matheron 1976; Powell et al. 1965), Thielauiopsis basicola (Berk. and Br.) (Hoestra 1965; Pepin et al. 1975; Sewell and Wilson 1975), Physalospora persicae Abik. and Kit. (Abiko and Kitajima 1970), and species of Fusarium and Rhizoctonia (Hine 1961b).
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D. Symptomology The short life and replant problem has a wide variety of symptoms. The general problem may be the result of injury to the root system, the top (shoots and leaves), or both. However, it is not uncommon for affected plants to manifest as part of their physio-pathological syndrome some type of exaggerated growth disorder, leaf malformation, adventitious root formation, thickening or elongation of plant parts, lack of or excessive branching, bending of stems, stunting, and disorganized growth characteristic of tumors and galls (Viglierchio 1971).In this discussion, we largely emphasize those symptoms characteristic of devitalization of tree growth and vigor as well as production span. Banta (1960) and Beattie (1962) observed the reduction and cessation of apple tree growth in a relatively short time with ultimate tree death within three to five years.Donoho et al. (1967) described ATD symptoms as a general loss of tree vigor resulting in short terminals, small leaves, and reduced productivity. Benson and his co-workers (1974a,b, 1976, 1978) have reported impaired or poor growth of apple replants in Washington state, as did Bollard (1956) in New Zealand. T o characterize SARD, Hoestra (1968) stated that SARD attack is confined to the feeder roots, is specific to apple, and is non-lethal; the causal factor stays in soil for several years and trees recover quickly upon transplanting to fresh soil. Apple trees affected with proliferation disease were shorter with thinner trunks and smaller crowns than healthy trees and had more chlorophyll in the leaves (Kaminska 1973a,b; Kaminska et al. 1971; Kaminska and Zawadzka 1973). Savory (1966) gave the following account of replant disease of apple and cherry in England. The root systems of affected trees were weak and small with discolored and necrotic fine roots, and no presence of pathogens. Aboveground symptoms included reduction in tree vigor and size. The condition of poor growth became obvious in the first year of replanting, normal vigor being restored on transfer to fresh soil. The problem is persistent but does not spread through soil. However, the symptoms for both apple and cherry are similar. Phytoph thora collar rot disorder of apple produces cankers below the ground line where the roots are attached to the crown or lower trunk. These cankers girdle the roots and lower trunks, causing poor terminal growth, foliar discoloration, and eventual tree death in severe cases (Jones 1971b). Describing “stem pitting” and necrosis in bodystocks of apple, Smith (1954) noted typical symptoms of dwarfing, development of “wood pitting,” and breakdown of body-stocks themselves. The formation of “black-hearted wood,” together with death of parenchyma cells and occlusion of vessels and rays, has been included in the apparent symptoms of cold injury to the apple trees (Steinmetz and Hilborn 1938). Simons (1970) reported trunk splitting in scions of ‘Stark-
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ing Delicious’ and ‘Golden Delicious’ apples on M 7 rootstock as a result of subfreezing temperatures. Apple union necrosis and decline are characterized by tree girdling, sparse, small, and pale green leaves, reduced terminal growth, bunchy-type twigs, fragile graft union with brown necrotic tissue imbedded in the union interface, and breaking-off of the scion portion of the affected trees (Stouffer et al. 1977). Sitepu and Wallace (1974) observed marked variability in apple tree growth, where the main visual symptom was extensive reduction in tree growth, particularly the trunk circumference. Colbran (1953) noted very poor and unthrifty growth of apple trees affected by “baffling slow decline.” This unsatisfactory growth of stunted trees was associated with the development of an abnormal root system with an abundance of discolored fibrous roots which later decayed. The symptoms of declining trees on “sick soil” as described by Borner (1959) include the manifestation of retarded growth and shortened internodes, which resulted in a rosette-like appearance, with varying degrees of root discoloration and reduced growth of the tap root. These symptoms were reversed when the plants were shifted from sick to normal soil. Pear decline has been characterized by phloem necrosis that occurs as a result of a mycoplasma vectored by Psylla pyricola Foerster, an insect of pear (Hibino and Schneider 1970; Westwood and Cameron 1978). Blattny and Vana (1974), Blodgett et al. (19621, Rallo (1973), and Seemuller and Kunze (1972) observed that sieve-tube necrosis is accompanied by various reactions leading to a girdling effect, deterioration of collar and feeder roots, callose development, early fall reddening of leaves, sparse foliage, decline in vigor, and wilting, with rapid or slow death of trees. Batzer and Schneider (1960) noted that a gradual loss of vigor in declining pear trees was associated with a series of anatomical changes initiated by sieve-tube necrosis immediately below the bud union. In advanced stages of pear decline, leaves became sparse, small, and pale green, and trees usually made no terminal growth and often suddenly wilted and died during the periods of high summer heat. Affected trees lacked the fibrous root systems of normal healthy trees (Woodbridge and Lasheen 1960). Sands and Kollas (1974) described the symptoms of “pear blast” condition in Connecticut as black leaf spots, sometimes with yellow halos, and frequent death of whole leaf and petiole, but no bacterial ooze or cankers on trees. Although frequently confused with fire blight, physiological disorders, or pesticide toxicity, severe outbreaks of “pear blast” in Chile have been characterized by blasting of flowers, leaf necrosis, and cankers of fruit spurs and small branches, but with no exudates on lesions (Cancino et al. 1974). In Greece, Agrios (1972) characterized stem pitting, graft incompatibility, and pockets of necrotic wood parenchyma from pear scions on quince rootstock as decline or “moria” symptoms.
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HORTICULTIJRAL REVIEWS
Clayton (1968) observed that the replants of peaches often were stunted, grew poorly, and died from the bacterial canker-Cytospora cankercold injury complex where tops were typically killed to the soil line and roots remained alive. He mentioned th at PTSL is more common in light soils than in heavier soils, and more prevalent on old orchard sites (Clayton 1977). Gilmore (1959) noticed slower growth of peach on replant sites than on new peach sites. Th e difficulties frequently encountered in the establishment of peach replants on old sites in Ontario are characterized by Koch (1955) as variable from slight stunting to a complete absence of growth; in addition to stunting, Savory (1966) reported chlorosis of peach trees on replanted land. Hung and Jenkins (1969) described the death of peach trees as either a slow decline over a period of several years or a quick decline within a year or two of planting on an old orchard site. In California, the decline of peach trees has been reported to be a chronic root disease of uncertain etiology often characterized by poor growth of the trunk and branches, by underdeveloped and chlorotic leaves, and by the frequent death of young trees during winter (De Vay et al. 1967). Davidson and Blake (1936) described some macro-nutrient deficiency symptoms in declining young peach trees: die-back following leaf discoloration, leaf necrosis and mottling, defoliation, inhibition of linear as well as spatial growth of shoots, restricted root growth, and breakdown, necrosis, and weakening of feeder roots. Dekock and Wallace (1965) have reported phosphorus and iron chloroses in decline-affected peach trees as a result of excess nitrogen. Taylor et al. (1970) described the condition called peach tree decline as induced by cold injury with symptoms of tissue discoloration above ground level. Daniell and Crosby (1968) noted anatomical abnormalities in cold-injured trees, including occlusion of xylem elements with a “gum-like” substance and “slime-like” material, and damaged ray cells. Later, cambial browning, bud mortality, and retardation of leaf development were observed a s additional symptoms of cold injury (Daniell and Crosby 1971). Yadava and Doud (1977, 1978a,b) reported th at the severity of trunk cambial browning (TCB) in early spring was directly proportional to the cold injury th a t trees suffered. Cold injury resulted in death of those trees th a t showed visual T CB ratings of 8 or 9 on a scale of 1 to 9. According to the observations of Chandler et al. (1962), the trees affected by PTSL showed symptoms of wilting o f immature foliage, with cambial browning on trunks and limbs accompanied by yellowish exudate from bark and a characteristic sour-sap odor. Bacterial canker, which is also called blast, bacterial gummosis, and sour-sap, occurs in the southeastern and western United States, and causes death of trees and limbs by cankers th a t girdle the trunks, crotches, and limbs (Petersen 1975; Petersen and Dowler 1965).
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS F R U I T TREES
13
These observations indicate a progression of disease from infected dormant buds to the development of cankers in the limbs. “Bacterial gummosis” has been found in phloem, xylem, tracheae, and fibers (Babos et al. 19761, with symptoms of bark cracking, leaf curl, persistence of wilted leaves, and death of trees within a year or so (Dorozhkin and Griogortsevich 1976). Prunier, Gardan and Luisetti (1970) and Prunier, Luisetti, and Gardan (1970, 1973a,b) reported additional symptoms of bacterial canker on peach and apricot in France to be cortical necrosis in winter followed by die-back of new growth in the spring, and twig necrosis on established trees followed by decline of all branches. This disease in France was first noticed in the Rhone Valley in 1968 (Prunier, Luisetti and Gardan 1970), and was characterized by small bud lesions appearing in fall, developing into a die-back in winter. Shortly after budburst in spring, trees partly dried out or died and numerous leaf spots and fruit gummosis were observed, while cankers caused the death of branches during summer. Root-knot nematode infestation is another weakening factor in the peach orchards suffering from PTSL (Clayton 1968; Hutchins 1936; Malo 1967). In Connecticut, Johanson (1950) presented evidence on the importance of nematodes, Pratylenchus and/or Macroposthonia, a s a factor in the short life of peach planted after peach in an orchard rotation where the nematodes attacked root tips and finally caused induction of ‘‘witches’-broom’’ root system. Johnson e t al. (1978) from Ontario attributed significant growth reduction of Siberian C rootstock seedlings to infection by Pratylenchus penetrans. Lownsbery (1959) and Lownsbery et al. (1968, 1973) attested th a t the growth reduction was the principal effect of the nematode infestation. Hung and Jenkins (1969) concluded from their greenhouse and laboratory experiments th a t the feeding by Macroposthonia curvatum Loof de Grisse on peach caused extensive lesions and pits on roots, which were later affected by other factors contributing to low vigor of the root system, finally resulting in the decline symptoms. Orion and Zutra (1971) demonstrated the role of Meloidogyne javanica (Treub) Chitwood as predisposing almond trees to infection by canker bacteria. Mountain and Patrick (1959) found th a t Pratylenchus caused peach root necrosis even in the absence of invading bacteria and fungi. Banko and Helton (1974) reported th a t tree wilting due to Cytospora canker was associated with gum-plugging in the xylem of affected trees. Studies of Hampson and Sinclair (1973) on Valsa (Cytospora) canker in New York peach orchards showed th a t wilting and resulting defoliation of infected branches not girdled by the cankers were characteristic of the condition. Additionally, the greenhouse tests gave evidence of xylem dysfunction as an inportant cause of canker symptoms. In Georgia, PTSL symptoms have been characterized a s
14
HORTICULTURAL REVIEWS
scanty growth, leaf chlorosis, and eventual tree death due to lack of feeder roots, probably caused by P y t h i u m infection (Hendrix and Powell 1970a; Hendrix et al. 1966; Owen et al. 1965; Spivey and McGlohon 1973; Taylor et al. 1970). In addition to P y t h i u m spp., other fungal organisms, such as species of Fusarium and Rhizoctonia, also have been found to cause poor growth of peach replants (Hine 1961b). Savage et al. (1953) reported that Clitocybe causes root and trunk rot of peach trees in Georgia with characteristic symptoms of whitish mycelial mats beneath the bark on the lower trunks of trees which are dying or already dead. Another fungal organism, Cylindrocladium floridanum sp.n., has been associated with PTSL and was found to cause wilting, root-rot, and death of seedlings of several peach cultivars in the greenhouse (Sobers and Seymour 1967; Weaver 1971). “Blister canker,” incited by Physalospora persicae, appears as a swelling of newly invaded bark tissue leading to rough and blistered appearance with gum exudation later on and eventual twig death (Abiko and Kitajima 1970). Weaver (197413) characterized a gummosis bark disease of peach trees caused by Botryosphaeria dothidia, with typical symptoms of sunken lesions around lenticels, circular- to oval-shaped necrotic areas in bark beneath infected lenticels, and blisters on the surface of shoots and twigs. Numerous gum deposits on trunks, limbs, and twigs of affected trees are commonly seen. Chirilei et al. (1970) distinguished two types of gummosis: xylem gummosis which typically produces water-insoluble gums (pectic acid), and cortical and cambial gummosis which results only in water-soluble exuding gums (pectins). The first gummosis is responsible for apricot apoplexy, whereas the second type causes the slow decline of apricots. X-disease, which affects peaches, nectarines, and cherries, shows symptoms of inward curling of leaves in early summer, followed by development of watersoaked spots on these curled leaves which become yellow to reddishpurple and fall prematurely starting a t the basal end of shoots (Jones 1971b). Affected trees often are winter-killed after a few years (Lukens et al. 1971). Klement et al. (1974) accounted for apoplexy symptoms on apricot in Yugoslavia as a consequence of infection by Pseudomonas syringae, which caused the phloem and cambium to die during the course of winter. If the phloem and cambial necroses are not of such an extent that they girdle the branch or the trunk, then in summer following the infection the surrounding healthy tissues will try to overgrow the necrotized areas resulting in cankerous wounds. When cambial necrosis completely engirdles the branch or the trunk, the healthy parts above the infected area suddenly die in spring or in the course of summer. If the cambial necrosis girdles only one or two branches, partial apoplexy occurs; but if the trunk is engirdled, the result is complete apoplexy or tree death. Apoplexy
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
15
of apricot in Bulgaria (Iliev 1968) has been described as a necrosis of bark on young trees on their own roots, the damage being severe a t the collar and lower parts of the trunk with xylem remaining unaffected. The characteristic symptoms of bacterial canker of sweet cherry, caused by Pseudomonas mors-prunorum, are shot-hole leaves, infected buds, shoot cracks, and die-back of branches and young trees (Lyskanowska 1976). Cherry replants following cherry on the same land either made very poor growth or died as a result of Pratylenchus penetrans infestation (Mai and Parker 1967). The symptoms of cherry decline, as associated with a mycoplasma, have been described by Fos (1976) as growth irregularities and leaf and flower anomalies-lack of production with tree death soon following when growth is rapid. Plum decline, incited by Prunus necrotic ring-spot virus, has been symptomized as a general growth reduction followed by progressive tree decline with necrotic “incompatibility” between rootstock and scion (Posnette and Cropley 1970). As reported by Cochran (1975), Prunus stem pitting induces serious derangement in the xylem with abnormal lignification. Trees infected early in their life are dwarfed, tend to break off a t the ground line, and usually die after one to five years of infection. The woody cylinder near the ground line of affected trees is variously but characteristically pitted and fluted. The symptoms of tree decline in some stone fruits also include leafing out four to eight weeks early, general growth suppression, and discoloration of wood with occasional stem pitting (Agrios 1971). 11. METHODS TO STUDY THE PROBLEM
A. Electrophysiological Electrolytic conductivity (EC) of tissue is recorded in pmhos on the conductivity bridge after emersing an electrode in leachate; whereas in the case of electrical resistance (ER) the points of electrodes are clamped into plant tissues and the resistance is determined directly in ohms (Wilner et al. 1960). A highly significant correlation exists between EC and ER methods (Wilner 1961). Greenham and Cole (1950) found electrical capacitance measurements on diseased plants to be the reciprocal of ER measurements. A method of exotherm analysis also has been used to determine the condition of plant tissue in relation to cold temperatures (Quamme et al. 1973,1975; Yelenosky 1975). This method gives a direct measurement of the temperature a t which the experimental tissue is injured. Oscilloscope technique, as described by Ferguson et al. (19751, uses oscilloscopic square wave form, the pattern of which changes in relation to periods of plant dormancy, activity, or death. “Index of injury” is a simple method for expressing freeze injury since the per-
16
HORTICULTURAL REVIEWS
centage of released electrolytes is converted to a scale where the unfrozen sample is given a value of 0 and the heat-killed sample a value of 100 (Flint et al. 1967). Stuart (1939) showed that the ratio between the conductivity produced by complete killing of tissue and that produced by injured tissue termed “percent electrolytes” (5% EC), is more reliable than EC of a sample alone. De Plater and Greenham (1959) proved that measuring ER a t both low (1 K Hz) and high (100 K Hz to 1 M Hz) frequencies, and using a ratio between these measurements resulted in more sensitive determinations of injury than with either alone. Measuring the flow of an electric current in the trunk of black cherry, P r u n u s serotina, Levengood (1973) determined that trees infected with crown gall had lower ER than did healthy trees. Gardner et al. (1974) found that the toxic chemical produced by Helminthosporium fungus caused a rapid hyperpolarization in membrane electropotentials of tissues from susceptible lines of corn, but not from resistant lines. Using an exosmotic method, Filinger and Cardwell (1941) successfully determined cold injury in bramble canes which, following death by freezing or by boiling, offered 72 to 82% less resistance to electric current than when alive. Dostalek (1973) reported that the roots of apple trees infected with the proliferation disease were much lower in electrical impedance than roots of healthy trees in late fall. No differences were found when root impedance measurements were taken in late summer; stem tissue showed no difference a t either time. De Plater and Greenham (1959) found that a low/high frequency ratio of ER in healthy tissue usually would be about 4, while in tissue that has been severely injured by cold the ratio would be less than 1.5. Swingle (1932) showed that higher EC readings as a result of speedy exosmosis from frozen apple tissue samples indicated a corresponding high degree of cold injury to the woody tissue. Osterhout (1922) mentioned in an earlier report that the increase in the membrane permeability, which usually accompanied death of tissue, was paralleled in a striking manner by a simultaneous increase in EC of tissue leachate. Changes in membrane permeability and tissue respiration have been found to be characteristic of most plant disorders (Wheeler and Luke 1963). Similarly, Stadelmann (1969) concluded that an increase in permeability often reflects pathological or premortal conditions. Golus (1935) reported that lower permeability of the membranes and, hence, low EC normally characterized more winter-hardy plants. Wilner et al. (1960) presented data on decreasing trends in cold resistance of outdoor roots and shoots of apple trees which agrees closely with the increasing trend in EC of tissue extracts. Diffusion of electrolytes from roots, however, did not follow the same pattern as from shoot tissue (Wilner 1959). Wilner (1960) also established quantitative values for the ultimate frost hardiness
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
17
of apple trees, viz., no sign of any appreciable injury when EC from hardened tissues was 200 to 250 pmhos or less. An EC of above 350 to 450 pmhos generally signified total killing; whereas, intermediate readings indicated partial injury to the twigs. In another study on apple rootstocks, Stuart (1941) showed that freezing injury increased the EC of the stems of all the rootstock types studied. Yadava et al. (1978), Ketchie and Beeman (1973), and Stergios and Howell (1973) compared EC with other methods to assess cold hardiness in fruit trees. Tree mortality has been correlated to greater EC readings from acclimated as well as dormant twigs of fruit trees (Ketchie et al. 1972; Nesmith and Dowler 1976; Yadava et al. 1978).
B. Chemical and Biochemical Chirilei et al. (1970) suggested that the decline disorder of fruit trees is a complex pathological phenomenon caused by major physiological and biochemical disturbances. Most plant disorders are characterized by changes in cell permeability and tissue respiration (Wheeler and Luke 1963). Allen (1953) studied in detail the respiration of roots in relation to soil toxins. He found that the toxins would act on some of the many steps in the respiratory process and that their effect would be reflected by a change in the respiratory rate of the actively respiring meristematic region of the root. Bergman (1959) stated that the ability of roots to survive an oxygen-deficient period in wet soils varies greatly between species; some plants die within a few days, others survive for weeks or months, or, in some particular trees, even for several years. But death always ensues. Rohrbach and Luepschen (1968) discussed the relationship among polyhydric alcohols in peach tree bark, winter injury, and the initiation of Cytospora canker infection. They stated that the least winter-hardy cultivar, ‘Earlyglo’, was found to have a slightly higher mannitol level. Siminovitch et al. (1967) found the augmentation of protoplasm to be a part of the mechanism of freezing resistance, since they noted in early fall an abrupt rise in RNA from the low summer value, closely followed by a similar rise in protein, protein synthetic capacity of tissue, and freezing resistance. Thus, they developed a quantitative method of estimating resistance to freezing injury based on ninhydrin-reactive compounds (NRC) which measures amino acids that are released from the injured cells. Yadava et al. (1978) used the NRC method of Siminovitch et al. (19671, modified by Wiest et al. (1976), and successfully correlated with peach tree survival and trunk cambial browning; however, due to greater variation in NRC values of fresh tissue, they were not satisfied with the modification made by Wiest et al. Yadava et al. (1978) found
18
HORTICULTURAL REVIEWS
that the triphenyl tetrazolium chloride (TTC) reduction method as refined by Steponkus and Lanphear (1967a), when used with artificially frozen tissue, was significantly correlated with peach tree survival, trunk cambial browning, as well as NRC method, but not with EC. However, the work on dormant twigs under natural freezing conditions showed no consistent correlation among any of the methods (Yadava et al. unpublished). Similarly, Stergios and Howell (1973) found that the T T C method was not as suitable as EC for cherry and raspberry. Gallaher et al. (1975) studied the levels of leaf calcium (Ca) from healthy and declining ‘Loring’ peach trees on limed as well as unlimed field plots. They found that most Ca was nonextractable in acetic acid and that the concentration of extractable leaf Ca was less than 100 ppm. They also reported that concentration of total leaf Ca was highest from declining trees but that declining trees had fewer and smaller leaves, resulting in less total Ca than in healthy trees. Higher concentrations of soluble Ca in the leachate from dormant peach twigs have been found to be closely correlated with tree survival on short-life and non-short-life sites (Yadava et al. unpublished). The contents of prunasin, the predominant cyanogenic glucoside in peach roots, have been correlated with the peach replant problem in Japan (Mizutani et al. 1977). Patrick (1955) carried out an extensive study to evaluate the importance of soil toxins (toxins from peach roots and pure amygdalin) in relation to their interaction with certain microorganisms in old peach sites. Such inhibitors were not produced when old soil was autoclaved before amygdalin was added, when other soils were used in which no breakdown of glycoside had occurred, or when roots from species other than peach were added. However, in California, no differences in the rate of amygdalin hydrolysis and resulting production of hydrogen cyanide (HCN) were found in peach replant problem soils, peach non-replant soils, or soils used for a crop other than peach (Hine 1961a). The rate of amygdalin breakdown varied significantly only with soil depth-deeper soils showed less activity than shallow and light soils. Thus, it was theorized that amygdalin hydrolysis probably does not account for the difficulty of establishing peach replants in some areas of California. Amygdalin added to autoclaved soil was toxic to growing peach seedlings only if they were planted immediately after its addition; whereas two weeks following this, no HCN was detected in the soil and, likewise, no signs of HCN injury on plants were noticed. C. Isolation, Culture, and Bioassay
The subject of phytotoxins produced by plant parasites has been covered in detail in a review by Strobe1 (1974). Sands and Kollas (1974)
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
19
isolated Pseudomonas syringae from diseased (pear blast) pear trees and the isolates produced characteristic blast symptoms when inoculated into pear. In Michigan, green fluorescent bacteria were isolated from cherry trees diseased with bacterial canker and, when bioassayed, the organisms were found to be pathogenic (Jones 1971a). Dowler and Weaver (1975) were able to readily isolate pathogenic and non-pathogenic fluorescent pseudomonads from twig and trunk tissues of apparently healthy peach trees on a monthly routine, except in summer. These pathogenic isolates were found to be closely related to Pseudomonas syringae. In a review on Pseudomonas pathogens of deciduous fruit trees, Crosse (1966) specified two distinct biochemical types of flourescent pseudomonads causing disease, corresponding to Pseudomonas syringae and Pseudomonas mors-prunorum, respectively. De Vay e t al. (1968) reported t ha t the isolates of Pseudomonas syringae th a t causes canker of peach trees produce a wide spectrum antibiotic, syringomycin, whose production is reduced with the loss of pathogenicity by Pseudomonas syringae. Weaver (1971) isolated Cylindrocladium floridanum from soil around roots of dying or dead peach trees on a short-life site. In bioassays on peach seedlings, the fungal isolates caused root rot of the seedlings. Water-soluble extracts from root, shoot, and seeds of peach were toxic to the seedling growth of peach, apple, and beans when applied to soil of potted plants (Oh and Carlson 1976). However, synthetic amygdalin, when bioassayed with potted peach seedlings, did not produce a phytotoxic effect, although it did alter the levels of certain nutrient elements. Patrick (1955) isolated from peach roots a highly physiologically active inhibitor which resembled amygdalin. Upon bioassaying, the inhibitory response was obtained only when amygdalin was hydrolysed by emulsin enzyme in the treatment consisting of amygdalin emulsin. Ross and Crowe (1973) studied the presence of apple replant disease in pot bioassays using different orchard soils and fumigation with chloropicrin. For the development of apoplexy of apricots, Rozsnyay and Barna (1974) bioassayed Cytospora toxin obtained from three different isolates of the fungus, which caused leaf collapse, gum production, and necrotic wounds when absorbed by young attached apricot shoots.
+
D. Inoculation Weaver (1974b) reported 28°C as the optimum temperature for mycelial growth of Botryosphaeria dothidia, the incitant of peach bark gummosis disease; however, good growth a t 36°C and slight growth a t 38°C were not uncommon. A greenhouse test from New Zealand (Dye 1957) indicated t hat the optimum temperature for stone fruit stem infection by Pseudomonas syringae was 18.3"C. According to Crosse and Garrett
20
HORTICIJLTIJRAL REVIEWS
(19661, little or no recovery of Ps. syringae could be expected (after inoculation) when daily maximum temperature averaged 30°C. Canker length and peach seedling mortality in containers, filled with soil from a short-life site, were positively related to temperature (Daniel1 and Chandler 1974). Seedlings held a t v iriable outdoor temperatures (-17” to 14°C) with mean minimum of 3 3 ° C and maximum of 8.5”C, respectively, developed longer cankers than a t a constant temperature of 8°C. Dormant season hypodermic inoculations of several isolates of Ps. syri n g a ~into the bark of ‘Bin$ and ‘Berryessa’ sweet cherries, ‘Blenheim’ apricot, ‘Eldorado’ and ‘President’ plums, and ‘French’ prune showed that these trees were highly susceptible to infection and pathogenesis from mid-December until early February under California conditions (English and Davis 1969).Additionally, they found th a t Ps. syringae was more pathogenic to ‘Lovell’ peach seedlings a t 12°C than a t 28°C’ but caused essentially no infection near 7°C. When 3-month-old ‘Lovell’ seedlings were exposed to 6°C for 25 to 30 days prior to inoculation with Ps. syringae, then held a t 16”C,they were more susceptible to canker development than those held constantly a t 16°C or those in a greenhouse. Relative population development of Macroposthonia xenoplax on a good host (Thompson Seedless grape) and on poor hosts (Lovell and S-37 peaches) is influenced greatly by soil temperature (Lownsbery 1961). A soil temperature of 26°C is more favorable for population increase of M. xenoplax than 13”,18”,21”’ or 28°C. Weaver and Wehunt (1975) showed the effect of various soil p H levels on the performance of ‘Elberta’ peach seedlings grown in pots of soil from a peach orchard with a bacterial canker history, and artificially inoculated with Ps. syringae after they had become dormant. Seven weeks later, sizeable mortality occurred in soils with a pH of from 5.6 to 6.1, but no plants died in soils with p H levels adjusted to 6.4 to 7.2. In addition, it was found th a t the number of propagules of Pythium spp. in the soil and recovery from roots were positively correlated with soil pH. In December, highest population of M. xenoplax was recorded in soil having a p H of 6.1, but differences during March or April were not significant. On the other hand, Lownsbery (1961) detected no differences in population levels of M. xenoplax on ‘Lovell’ peach grown in soil between p H 5.0 and 7.0. Further, in a lathhouse pot test, peach seedlings were not injured by the nematode a t populations as high as any yet found in California peach orchards. Luisetti and Paulin (1972) and Luisetti et al. (1973) studied the pathogenicity of Ps. mors-prunorum f. sp. persicae in relation to inoculum concentration, and concluded th at incubation time was inversely related to inoculum concentration. Prunier et al. (1973a) successfully reproduced decline symptoms on peach and apricot by inoculations with concentrated cultures of the same bacterium.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
21
At Geneva, New York, apple breeders (Cummins 1977; Cummins and Aldwinkle 1974b) emphasize the importance of screening by utilizing inoculation for resistance to several important fungal organisms before beginning actual horticultural testing. Similarly, in Oregon Westwood (1976), while working on the inheritance of pear decline resistance, graftinoculated the progeny of resistant, susceptible, and resistant X susceptible crosses, using them as rootstocks for ‘Bartlett’ pear. By inoculating Virginia crab K 6, a virus indicator clone, with certain isolates of apple stem grooving virus (ASGV), Stouffer et al. (1977) observed apple decline and union necrosis symptoms comparable to those occurring on clones of ‘Delicious’ apple propagated on M M 106 rootstock. Since Malling and Malling-Merton apple rootstocks had not been reported to be affected by the ASGV-induced disorder, the authors declined to include ASGV as the causal factor for the union necrosis and decline syndrome of apple in Pennsylvania. Campbell (1971) ascertained the importance of the amount of virus inoculum in assessing its effect on the growth of apple trees. His observations of four apple cultivars, bud-grafted on virus-infected rootstocks in England, have revealed varying degrees of growth reduction which were proportional to inoculum strength in both the first and second years of growth. Kunze (1972) used a graft inoculation technique to study apple proliferation disease in a series of tests where 80% of the surviving grafts developed typical symptoms within 2 years. Mircetich et al. (1977) inoculated peach seedlings with root chips from peach orchard trees carrying Prunus stem pitting (PSP) or yellow bud mosaic (YBM). These later developed only PSP or YBM symptoms, depending on the inocula used. However, ‘Mazzard’ cherry seedlings that received inoculum through root chips from root chip-infected peach, or buds from naturally-infected trees of cherry, remained symptomless. The studies of Smith and Stouffer (1975) established that PSP was graft-transmissible, and that root bark patches were more efficient sources of inoculum than budwood. Posnette and Cropley (1970) used the inoculation method in a ten-year field trial to study the effect of five different viruses on the decline of three plum (Prunus dornestica L.) cultivars. They noticed the first appearance of symptoms after five years, whereafter the trees declined progressively with necrotic “incompatibility” between rootstock and scion. Rosenberger and Jones (1977) studied seasonal variation in virulence of peach X-disease inoculum, and found that infection rose from 8%for May to 100% for June inoculations, then declined to 82%, 32%, and 20% for August, September, and October, respectively. Various other inoculation studies to test the role of bacterial canker in PTSL have been reported by several workers (Chandler and Daniell 1974, 1976; Daniell and Chandler 1976; Davis
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and English 1969b; Dowler and Petersen 1966; Dowler and Weaver 1975; Gardan et al. 1975; Yadava et al. 1978). Davis and English (196913) proved that the greatest expression of bacterial canker symptoms on peach results from inoculations made during the dormant period. They theorized that the susceptibility to Pseudomonas syringae inoculation varies directly with the degree of dormancy. Gardan et al. (1975) reproduced experimentally all the symptoms of bacterial canker on branches, stems, leaves, and fruits of peach by artificial inoculations with Ps. mors-prunorum f s p . persicae. Differences in susceptibility to Ps. syringae inoculations in presence of Phytophthora spp. on seven species of stone fruits in Greece were observed by Kouyeas (1971). Inoculations of injured and uninjured peach roots with several isolates of Clitocybe tabescens showed that most of the isolates had infected the injured roots, whereas only few isolates infected the uninjured roots (Weaver 1974a). In a three-year-study under Colorado conditions, Luepschen e t al. (1975) found seasonal differences in canker development on ten peach cultivars as a result of inoculations with Cytospora leucostoma. Benomyl sprays on peach trees before inoculating the limbs with C. leucostoma gave up to 98% and 80% control of inoculations made in May and June, respectively (Luepschen 1976). In New York, Hampson and Sinclair (1973, 1974) studied the pattern of Leucostoma canker development due to water stress on potted peach plants by inoculating the plants during the active growth period in greenhouse. They used eosin dye to learn about the infection’s movement in the xylem, since they suspected that the xylem dysfunction was the important cause of symptoms. Helton and Randall (1975) inoculated ‘Italian’ prune trees with a virulent strain of Cytospora cincta, and examined the infected branches to determine the longitudinal extent of visible gum in the cambial zone. Internal gummosis apparently was associated with the commonly observed wilting of terminals following infection. Rosik e t al. (1971) were able to artificially induce gummosis on apricots with C. cincta inoculations. Wilbur e t al. (1972) studied the seasonal development and pathogenicity of four clones of Armillaria mellea inoculations on peach trees and interclonal differences. Abiko and Kitajima (1970) established, on the basis of inoculation tests, that the blister canker fungus (Physalospora persicae) was specifically pathogenic only to peach. By using inoculation with Macroposthonia xenoplax as a routine procedure, Lownsbery et al. (1973) reported reduced growth of ‘Carolyn’ peach on Love11 rootstock as well as increased susceptibility to both Pseudomonas syringae and “wet-feet.” The full effect of the nematode was evident after only three growing seasons. Soil inoculations with P y t h i u m species a t planting time increased susceptibility to Ps. syringae less than the inoculation with M. xenoplax. P y t h i u m spp. did not reduce growth
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
23
of peach trees significantly and no correlation between M. xenoplax and Pythium sp. was noted. Hung and Jenkins’ (1969) greenhouse and laboratory experiments on peach inoculation with Macroposthonia curuatum and Pratylenchus penetrans produced typical symptoms of PTSL; however, under nonsterile conditions, the pits and lesions produced by feeding of these nematodes were invaded by other microorganisms, causing general discoloration and low vigor of the root system. Penetration, migration, establishment, and development of Meloidogyne javanica in the roots of two resistant (Okinawa and Nemaguard) and one susceptible (Lovell) peaches were histologically studied by Malo (1967), after inoculation with second-stage larvae of the nematode. It was concluded that the nature of resistance of ‘Okinawa’ and ‘Nemaguard’ to M. jauanica infection was based on a “walling-off’’ of the giant cells, followed by their breakdown. This was not the case with ‘Lovell’ roots where giant cells reached the reproductive stage 20 to 22 days after inoculation.
E. Discoloration and Tissue Integrity Daniell (1977) has reviewed the subject of PTSL, citing discoloration and tissue integrity as important criteria for determination of tree condition. Other workers also have used these methods for determining tissue disorders caused by different factors (Chandler et al. 1962; Daniell 1975; Daniell and Crosby 1971; Lapins 1961; Nesmith and Dowler 1976; Petersen 1961; Prince 1966; Prince and Horton 1972; Stergios and Howell 1973; Taylor et al. 1970; Yadava et al. 1978). Stergios and Howell (1973) compared five viability tests for cold-stressed plants and found that tissue browning was one of the most reliable, although it required considerable time and was only a qualitative measure. On the other hand, Yadava et al. (1978) compared trunk cambial browning (TCB) of orchard trees in early spring with laboratory tests for cold hardiness and bacterial canker development (BCD) and finally, peach tree survival (PTS) later in the season. TCB proved to be a quick, convenient, reliable, and quantitative method. A highly significant correlation was observed between TCB in mid-March and PTS through the end of June. Yadava and Doud (1978b) have found a close correlation between the ease of bark plug removal from the tree trunks and the TCB ratings. Bark removal was easiest (particularly in early spring) in the case of injured trees, thus indicating a direct relation with the degree of injury to the trunks.
F. Regrowth Lapins (1961, 1962) found that the hardiness differences between cultivars and seedling progenies were more reliable by tissue regrowth
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following artificial freezing than by EC readings of the leachate from shoot sections. In a ten-year-study on peach budbreak as influenced by temperature, Weinberger (1967) found that the length of physiodormancy correlated with mean maximum November and December temperatures, respectively, but not with mean minimum for these months. On the basis of controlled freezing experiments and forcing, Meador and Blake (1943) showed that peach buds were most hardy near the coldest part of winter and that hardiness did not follow a smooth curve throughout, but fluctuated up and down during winter. Ormrod and Layne (1974) forced whole trees under controlled conditions following acclimation a t set regimes of day/night temperature and photoperiod. They found that temperature and scion cultivars had much greater effects on cold hardiness of buds and bark than did rootstock and photoperiod. Prince (1966) investigated the possible relationship between winter temperature patterns and tissue injury in the cambial zone of peach tree trunks and crotches during four winters in central Georgia. Injury was detected only on trees which had accumulated all or a substantial portion of their chilling, followed by exposure to abnormally warm weather, and then to a relatively sharp drop in temperature to below freezing. Hodgson (1923) provided guidelines for assessing regrowth. If the cuttings from dormant trees failed to start growth within two weeks of forcing, they were judged to be in deep dormant state. Yadava and Doud (1977) studied the effect of applied phytohormones and rootstocks on the budbreak and growth of scions by forcing two-year-old potted trees of ‘Babygold-5’ in the greenhouse. Differences due to rootstock and phytohormone treatments were significant for budbreak and shoot length but not for other characters studied.
G . Other Methods Based on a histological evaluation of cold injury to apple trees, Steinmetz and Hilborn (1938) concluded that if about 50%of the parenchyma cells were killed the branch might not recover; but if only 20% were killed, recovery was probable. Further, it was shown experimentally that the compression of cambial cells and the lateral displacement of wood rays were characteristic of low temperature injury in woody plants. Dorsey and Strausbaugh (1923) explained in a cytological study that the browning in the wood was due, a t least in part, to a condensation of storage materials apparently transformed into gums and tannins. An anatomical examination of Cytospora canker infection on one-year-old ‘Elberta’ peach seedlings confirmed that the wilting due to this cankerous disorder was associated with gum-plugging in the xylem (Banko and Helton 1974). Batzer and Schneider (1960) showed that positive
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25
diagnosis of pear decline could be made only by anatomical examination of phloem a t the bud union, although macro-symptoms of a faulty bud union were helpful in determining the affected trees. Anatomical abnormalities in cold-injured peach trees also were observed by Daniel1 and Crosby (1968). Harvey (1923) measured winter cambial temperature of trees and correlated it with cold injury. He was most concerned with the cambial temperatures because injury is most serious within this layer. Tree trunks painted with white latex paint on sunlit sides were found to be 30°C cooler than non-painted trunks during mid-winter (Eggert 1944; Martsolf et al. 1975). According to Jensen et al. (1970), trunk cambial temperature appeared to be a sensitive indicator of peach tree vitality during growth; trees with low vitality had higher cambial temperature than trees in good health. Potter (1924) reported that apple roots, dried until 5% of their total moisture was removed, sustained less freezing injury than turgid roots, and high root moisture content contributed to winter root injury. Wildung et al. (1972a) determined root moisture levels and soil temperature in the root zone, concluding that roots with 3 to 4% less moisture in 1967 hardened to a greater extent than in 1968 when rainfall was above normal. Weekly root hardiness changes in 1967 also were highly correlated with the soil temperature during the week preceding hardiness testing. Tukey (1970) published an excellent review on the leaching of substances from plants, as applied to the removal of substances from plants by the action of rain, dew, mist, and fog. He mentioned that the young leaves from healthy and vigorous plants are much less susceptible to leaching than are leaves which are injured, whether by microorganisms, insect-pests, adverse climate, nutritional and physiological disorders, or by mechanical means. Leaching also may reduce physiological disorders in certain cases. Injections, but not foliar sprays, with several derivatives of tetracycline, under the bark or into the wood of peach trees infected with peach rosette, resulted in remission of rosette symptoms, and thus, confirmed the involvement of mycoplasma-like organism in peach rosette (Kirkpatrick et al. 1975a). Israel et al. (1973) reported that soil-applied potassium cyanide, mendelonitrile, benzaldehyde, peach root bark, and amygdalin reduced the total population of microorganisms, actinomycetes, Pythium, and pathogenic nematodes in an old peach soil. In search of the causative factors in PTSL, Gilmore (1963) designed experiments in soil pot culture using soils composted with peach root wood. This compost stimulated biological activity, thereby suppressing nitrogen content-hence, the stimulation of “replant” effect. Havis and Gilkeson (1947) studied toxicity of old peach roots in high-nutrient sand culture in 3-gal. earthenware crocks. Evidently, there was no “toxic” substance
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in peach roots or leachate that adversely affected the growth of young ‘Elberta’ peach on ‘Lovell’ seedling rootstock that had failed under field conditions. However, Proebsting and Gilmore (1941) reported that root bark, but not wood, was phytotoxic in sand culture. Furthermore, the alcohol extract of bark was also toxic, while the residue from alcohol extract did not show any toxic effect in sand culture. Another study on soil treatments in the greenhouse (Prince et al. 1955) showed inconclusive results applicable only to the particular soil used. Van Gundy et al. (1962) measured the oxygen diffusion rate in the soil pore spaces and correlated it with nematode activity and their survival. The results revealed that the oxygen availability in soil was largely related to moisture content. Heuser (1972) obtained callus cultures from peach and two grafting understocks, ‘Nanking’ cherry (Prunus tomentosa Thumb.) and sand cherry (P. besseyi Bailey), to study their growth pattern, structure, and tolerance to cyanide toxicity. Peach callus was more tolerant to high cyanide concentration, whereas callus cultures from the two understocks were more sensitive to cyanide. This study suggested the existence of a detoxification system in peach. 111. CAUSAL FACTORS
A. Environmental Factors An understanding of the physiological responses of particular crops to changes in the environment must precede an evaluation of causal agents in the short life syndrome. It is generally agreed that environment exerts the most important controlling effect on the geographic distribution of organisms on earth. Of the various climatic factors, temperature often plays a leading role in its influence on plants. Thus, climatological data seem to furnish the most plausible explanation for a favorable tree condition (Cowart and Savage 1941). For this reason, those factors related to environment in both the broad sense (those natural factors affecting the entire region or growing areas) and the strict sense (those having influence on individual orchards or a group of plants or orchards on a limited area) are included in this section. 1. Macroclimatic (Natural).-In this section, we will emphasize such controlling factors as temperature, rainfall, and wind and their combinations. The impact of these prime forces as related to the prevailing weather in a specific fruit growing area is considered under the following headings.
a. Cold (Winter, Freeze or Frost) Injury.-Throughout the world, the most consistently and effectively hostile element of climate in a fruit tree’s environment is low temperature (Proebsting 1970). There is a
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relatively small temperature interval between that causing slight injury and that which virtually eliminates the crop (Proebsting et al. 1966). Low temperature, either background, hardening, or damaging (Drozdor et al. 1976), usually limits the organic reactions that constitute the processes of plant life (Parker 1963). Langridge (1963) has reviewed a t length the biochemical aspects of temperature response. Sometimes both fall and spring damages occur, one kind of injury being additive to the other. Gerber et al. (1974) concluded that, aside from the winter injury, spring frost in temperate climates constitutes the most serious climatic hazard to the fruit trees. Once the tree is damaged, this injury is further complicated by secondary organisms that gain entry through injured tissue and become part of the complex that kills the trees (Blake 1938; Helton 1961; Hickey 1962; Lyons 1973; Panagopoulos and Crosse 1964; Savage 1970; Savage and Cowart 1942a). Blake (1928) stated t h a t cold injury may change the growth status of an entire or a sector of a tree within any one season with the effects continuing for an indefinite period of time. Furthermore, the extent of resulting injury often is affected by growth processes preceding a freezing spell (Dennis 1977; Olien 1967). Longevity of cold-injured trees is substantially shortened (Campbell 1948). I t is generally accepted that cold injury, which occurs to the bark and wood of tree trunks and limbs during sub-freezing winter weather following an unusually warm period, is alone more than enough to kill trees even in the absence of other agents. Cold or frost injury has been heavily implicated as the major cause in the short life syndrome of fruit trees by several research workers (Clayton 1968, 1972; Cowart and Savage 1941; Daniel1 and Crosby 1970; Edgerton and Harris 1950; Jensen et al. 1970; Paclt 1972; Prince 1966; Sarasola and de Bustamante 1970; Savage 1970, 1972; Savage and Cowart 1942a, 1954; Weinberger 1949). General aspects of freezing and chilling injuries to plants have been thoroughly reviewed (Burke et al. 1976; Lyskanowska 1976; Mazur 1969). In woody plants, consisting of tissues of more than one kind and age, frost killing occurs over a range of temperatures. The relative influence of such factors as length of growing season, tissue maturity, states of dormancy, nutrition, moisture, and temperature variations upon injury cannot be separated definitely from that of other factors, but all factors acting together determine the ability of a tree to withstand winter conditions (Dorsey and Bushnell 1925).
i. Dormancy. The subject of dormancy has been thoroughly reviewed by Lyons (1973), Olien (19671, Samish (19541, Samish et al. (1967), Taylorson and Hendricks (1976), Vegis (1964), and Wareing and Saunders (1971). A rest period (referred to as physiodormancy throughout this text) is characterized by an internal inhibition of growth resulting from physiological factors, and having certain distinct features such
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as onset, intensity, and duration; dormancy, however, is when most woody plants would not grow where even the physiodormancy is not the controlling factor. In other words, the physiodormancy refers to that portion of the state of dormancy when a given species cannot be induced to grow even if suitable conditions prevail. According to Vegis (1964), dormant plant organs have especially high resistance; thus, growth cessation and the onset of dormancy before the unfavorable season begins ensure the survival of the plants in question. He further stated that dormancy is often considered as a hereditary property with the beginning, duration, and end of the dormancy period. Frost in the fall season can be quite serious, especially on plants t h a t have not become dormant. Thus, suitable biochemical preparations for the development of resistance against cold weather are necessary for the survival of overwintering plants with aboveground parts (Parker 1963). Samish (1954) has pointed out that photoperiodism is not a factor universally involved in dormancy, but that cultivar differences in photoperiodic response with corresponding variance in chilling requirement indicate that photoperiodism is a factor in dormancy, a t least in some species and cultivars. Moreover, Piringer and Downs (1959) demonstrated that previous photoperiod(s) had no effect on the survival of apple and peach trees a t Beltsville, Maryland during the 1957-1958 winter. Similarly, Ormrod and Layne (1974) found temperature and scion cultivar to have greater effects on cold resistance of peach buds and bark than did photoperiod and rootstocks. Along with low temperature, light has been found to be the most notable of environmental factors to greatly enhance the rate and degree of cold acclimation as a photosynthetic rather than a photoperiodic stimulus (Steponkus and Lanphear 196713).Samish et al. (1967) reported that with peach buds light was of particular importance during the period of emergence from dormancy. However, this effect was preconditioned through preparation in the course of mid-dormancy darkness, since darkness during chilling increased the subsequent effect of light. T o produce normal growth under favorable conditions, it is necessary that physiodormancy be broken by certain periods of cold or low temperature during which growth may be interrupted. The length of this period, which differs with plant species, cultivars, and physiological conditions, is termed by Samish (1954) as the chilling requirement. T h e chilling requirement, in all its phases, is controlled by genetic factors (Vegis 1964). Lesley (1944,1957) emphasized that chilling requirement in peach depends on multiple genes, and transgressive segregation occurs in both directions. Generally, flower buds have a shorter chilling requirement than vegetative buds, and terminal vegetative buds have a lower chilling requirement than lateral buds. Symptoms of inadequate chilling include delayed and sporadic foliation, deformed and non-viable flower parts,
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29
and flower bud abscission (Lammerts 1941). Continuous chilling breaks physiodormancy of more buds than alternating warm and cold periods even with similar total hours of chilling (Overcash and Campbell 1955). This is because the periods of warm temperatures interspersed with cold temperatures counteract some of the cumulative chilling effect. Cold injury is common on those trees which have accumulated all or partial chilling hours, followed by their exposure to abnormally warm and cold periods (Prince 1966). A heat requirement also is necessary for growth resumption after the chilling requirement has been satisfied (Lammerts 1941). However, high temperatures of from 15" to 23°C during winter have been shown to antagonize the dormancy-releasing effect of chilling (Bennett 1950). Chilling probably accomplishes more than a decrease in growth inhibitor content and synthesis of growth promoters; rather, a change in metabolism occurs, dependent in part on a higher oxygen supply permitted by low demands for respiration during winter (Taylorson and Hendricks 1976). Wareing and Saunders (1971) published an excellent account of dormancy in relation to phytohormones. Roots are not thought to have a true physiodormancy (Dorsey 1929; Samish 1954), although some roots may go through a partial one. Other parts, which are exposed to external environment, experience true dormancy to escape injury during varying and adverse conditions of winter weather. Dormant plant organs have maximum cold hardiness (Vegis 1964), but after spring dehardening the killing point begins to rise (Dorsey 1929). A rapid rate of cold hardiness development is better than slow rate to withstand cold. Moreover, loss or inability to regain cold resistance reduces the survival value of the plants (Brierley 1947). In peach buds, cold resistance is lost and regained repeatedly depending on the fluctuations in the winter weather. A peach cultivar in middle Georgia would suffer from prolonged dormancy if its chilling requirement were not satisfied and physiodormancy were broken by mid-February (Weinberger 1950a). Chilling early in the dormant period appears to be less effective than later chilling, and interruption of chilling with periods of high temperature reduces subsequent growth (Thompson et al. 1975). Prolonged dormancy of peaches, according to Weinberger (1950b), is a condition in which budburst is beyond the usual time for opening in the spring, even though favorable growing temperatures occur. Prolonged dormancy trouble with peaches has been experienced in all southern regions of the U.S.A., as well as in Italy and part of Latin America, where it is a serious problem. In China, races of peach that are resistant to prolonged dormancy have developed. This problem is associated with high mean temperature in winter. Continuous exposure to cold or periods of extreme cold is not necessary or even desirable to break physiodor-
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mancy. However, high winter temperatures and sunlight have a delaying effect in breaking dormancy. The chilling requirement of peaches, while creating a hazard to production in southern regions, is very beneficial in other parts. I t keeps peach trees dormant during cold weather, while otherwise growth might begin very early and be susceptible to frost. Delayed, but not prolonged, dormancy provides an added advantage of escaping spring frosts.
ii. Extent of Injury. General weakening of tissue as a result of cold injury increases its susceptibility to decay or other disorders. The duration of exposure to low temperature, the maturity of plant tissue, the time of the year, and the dormancy status of the tissue all appear to have a bearing on the extent of injury. With the approach of maturity the killing point due to cold drops gradually, while during the break in the dormancy period it rises again (Dorsey 1929). Campbell and Hadle (1960) noted that between trees of different ages but of same cultivar considerable variation in amount of winter injury resulted from an extremely low temperature of -34°C experienced in Kansas in January, 1959. One-year-old trees of ‘Halehaven’ and ‘Redhaven’ peach suffered slight injury while five-year-olds sustained medium injury. Cullinan and Weinberger (1934) reported that buds on peach trees which were low in nitrogen and where shoot growth was short did not survive as well as those on more vigorous trees. Gerber et al. (1974) gave a comprehensive account of spring injury. Deciduous fruit trees undergo a transition a t spring blossoming and leafing that is intermediate between foliation and defoliation. This transition time is critical because the crop is setting and the threshold of lethal temperatures is rising rapidly. Aside from midwinter temperature injury, spring frosts in temperate climates constitute the most serious climatic problems in fruit production. The “black” frosts, which are the freezes occurring without white hoar due to lower dew point than ambient temperatures, are usually more damaging than the “white” frosts, which occur on nights with dew point near freezing and produce abundant white frost. Usually, black frosts feature very cold weather. iii. Type of Injury. Two types of injuries, viz., bud injury occurring on both flower and leaf buds, and bark and/or cambial injury which may occur on trunks and/or limbs, constitute the most common kinds of cold injuries. Probably both types of injuries result from insufficiently matured tissues’ inability to withstand low temperature (Brown 1943). Two types of bark injuries have been described by Blake (1938). One form of bark injury is the near- or complete-killing of a band of bark several centimeters in width on the main trunk just above ground level. This results in a girdling effect, and fungi soon cause rapid decay of
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
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the wood. Another form of injury to peach trunks is bark splitting, sometimes confined to the lower 5 tolOcm of the trunk,but often extending to a height of a t least 30 to 50 cm. Although the bark on other areas of the trunk is uninjured, fungi enter from the injured side and cause weakening and decay of the inner wood. There is not always a correlation between resistance to bark and bud injuries (Blake 1935, 1938). Thousands of peach trees in middle Georgia were found severely damaged, principally on the windward side, due to cambial injury which occurred as a result of subfreezing temperature and high wind in the spring of 1949 (Weinberger 1949).
iu. Mechanism o f Injury. A number of mechanisms have been proposed to help explain the physiological and biochemical changes associated with cold injury. Perhaps the most spectacular effect of chilling temperatures on sensitive plant tissue is that on protoplasmic streaming (Lyons 1973). The external symptoms of injury and ultimate death of the tissue would reflect the inability of cells to withstand increasing concentrations of metabolites as a function of time. The mechanism of cell injury by chilling encompasses several factors operating simultaneously or independently-imbalance in metabolism, accumulation of toxic chemicals, and increased permeability. In nature, temperature decreases a few degrees per hour and the woody plant tissue freezes a t a slow rate, resulting in ice formation first occurring outside the protoplasm where the water is purest. As temperature continues to decrease, intercellular water increases a t the expense of intracellular water, resulting in cell dehydration. T h e review by Burke et al. (1976) centers around water in living tissues as related to freezing injury. They mention that water content or degree of dehydration in plants which acclimate (the hardy plant species that go through the seasonal transition from tender to hardy condition) almost always decreases with increasing hardiness and increases as plants deacclimate. Plants which are tolerant to freezing generally undergo extracellular freezing, while intracellular freezing is probably invariably lethal. The differences between hardy plants and those tender plants which withstand freezing to some extent can, therefore, be stated simply: hardy plants tend to survive when more of their water is frozen than do tender plants. Mazur (1969) theorized t h a t damage to cells from intracellular ice seems due to direct interaction of ice crystals with membrane systems rather than to indirect effects associated with the loss of liquid water. Cooling velocity and permeability of the cell to water are the primary factors determining the kind and extent of intracellular ice formation. Except when cooled at the highest of velocities, cells approach equilibrium during freezing. However, the fate of the cell is greatly influenced by whether it approaches equilibrium
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by intracellular freezing or by dehydration and extracellular freezing. Cells that are cooled too slowly to freeze intracellularly, as is the case with most plant cells, equilibrate by dehydration which produces a t least six types of physical alterations: concentration of solutes, precipitation of solutes, reduction in cell water content, cell shrinkage (plasmolysis), changes in pH, and reduction in spatial separation of macromolecules. Several of these alterations, including changes in ionic strength, concentration of specific electrolytes, pH, and concentrations of protein, can lead to irreversible denaturation of proteins a t subzero as well as a t elevated temperatures. Four of them, viz., change in electrolyte concentration, removal of essential water, cell shrinkage, and reduction in the spatial separation of macromolecules, have been the bases of unitary theories of freezing damage. Another study showed rapid and more uniform ice spread in unhardened than in cold-hardened stems (Yelenosky 1975). Exothermic tests showed that a small fraction of water may remain unfrozen to as low as -42°C after freezing of the stems’ bulk water (Quamme et al. 1973). In view of the report by Scarth (19441, the protoplasm’s most important property in frost resistance is its ability to prevent coagulation or some other mechanical injury following freezing. Histologically the effects of low temperature injury become apparent first as death of the protoplasts in the parenchyma cells followed by an occlusion of the vessels by a gummy substance; thus, “blackhearted” wood is formed (Steinmetz and Hilborn 1938). I t has been shown experimentally that the compression of cambial cells and the lateral displacement of wood rays are characteristic of low temperature injury in woody plants. u. Effect on Tree Life. Campbell (1948) stated that those trees most severely injured by cold probably have reduced longevity. He further maintained that the mechanical strength of those branches with severe blackheart-type injury is likely to be reduced, resulting in splitting and breaking. When splitting and breaking do occur in the blackheart wood, it becomes more susceptible to wood-decaying organisms than uninjured sapwood or normal heartwood. Any such injured wood, when exposed to the air, rots rapidly; thus, the productivity and life span of the injured tree are decreased. Cold injury has been implicated as a prime predisposing factor for such disorders as Cytospora canker (Helton 1961; Hickey 1962), bacterial canker (Klement et al. 1972), blossom blight (Panagopoulos and Crosse 19641, other insects and diseases (Cowart and Savage 19411, and PTSL syndrome (Daniel1 and Crosby 1970). Brierley (1947) asserted that cold injury or easily lost resistance to it certainly would lessen tree survival.
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ui. Cold Hardiness. Cold resistance refers to the ability of plant cells to survive ice formation in the tissue or the ability of the plant to withstand low winter temperature or frost in the spring (Chandler 1954). A complete knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage and resulting losses in fruit production, since cold hardiness has been directly associated with tree longevity (Nesmith and Dowler 1976). During the period of rapid growth in the spring, plants are exceptionally susceptible to cold injury (Dorsey 1918a). T he ability of plants to withstand cold depends on an inherent annual rhythm of complex metabolic functions t h a t have evolved through a n interaction between plant and environment. Levitt (1966) and Alden and Hermann (1971) agree th at development of cold hardiness in woody plants is inversely proportional to growth rate, and th a t the environmental factors th at influence growth will affect cold hardiness accordingly. Levitt (1951) theorized th at frost, drought or desiccation, and heat resistance are all basically similar, and any resistance to one of these factors carries with it a corresponding resistance to the others. Numerous factors affect cold hardiness of fruit trees: soil and air temperature, photoperiod and light intensity, soil and tissue moisture, rainfall, air movement, rate of cooling, tissue maturity, growth rate and factors controlling it, cultivar and tissue type, physiological stage, dormancy, stomata1 density, and defoliation (Alden and Hermann 1971; Brierley 1947; Chandler 1954; Dennis 1977; Edgerton 1954, 1960; Hildreth 1926; Howell and Weiser 1970; Irving and Lanphear 1967; Kennard 1949; Ketchie and Beeman 1973; Knecht and Orton 1970; Knowlton 1936; Levitt 1966; Meador and Blake 1943; Pellett 1971; Proebsting 1963; Proebsting amd Mills 1961; Wildung et al. 1972a, 1973). Temperature prior to freezes can strongly influence cold hardiness and survival of peach trees (Dennis 1977). Peach trees do lose hardiness following periods of warm weather during the dormant season (Edgerton 1960). Both soil and air temperatures during the dormant season affect hardiness, although the duration of cold appears to be more important than the degree of cold (Proebsting 1963). Loss of hardiness could occur before the end of physiodormancy if hardiness greater than the minimum level had been achieved previously. Peach scions have greater influence on cold hardiness of bark than do rootstocks (Ormrod and Layne 1974); however, apple rootstock hardiness is not influenced by scion (Wildung et al. 1972b). Comparing root and shoot differences in hardiness, Pellett (1971) showed th a t stem tissue achieved much greater hardiness than root tissue under similar conditions. This conforms with the details given in reports by Chandler (1954), and Dorsey and Bushnell(1920).Chandler said th a t roots of most orchard species are considerably less resistant to cold in winter than
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parts aboveground. For example, roots of apple whose tops would withstand a temperature of -35" to -40°C are killed by a temperature of -10" to -15°C when frozen slowly in air. Pear, peach, P r u n u s cerasifera, and P. auium roots are about as tender as apple roots or slightly more so; however, P. mahaleb roots seem to be more resistant than the others'. Wildung et al. (1972a,b) correlated root hardiness with rainfall and soil and root moisture levels. Time and degree of defoliation have been reported to affect winter hardiness (Kennard 1949). There is evidence in plums, apples, and other such species that the maternal parent may transmit cold tolerance better than the paternal parent (Stushnoff 1973; Wilner 1965). Lantz and Pickett (1942) found that hardy apple cultivars transmit their hardiness to a relatively high percentage of progenies, even when crossed with a tender cultivar like 'Delicious'. They also found that a portion of the seedling trees produced by crossing two cold-tender cultivars may be hardier than either parent, and further indicated that apple progeny hardiness is predictable but comes from multiple factor inheritance.
b. Other Stresses.-i. Water (Drought, Desiccation). Brierley (1947) reported that when a large portion of tissue water is lost, some plants, or their younger wood, are severely injured by cold and cannot recover. Brown (1943) showed under Illinois conditions that both trunk and tree top injury in peach were the result of the inability of immature tissues to withstand cold. The immaturity of the tissues was associated with summer drought in 1941, followed by heavy rains in October and warm weather in November and December. Subsequent spring and early summer rains in 1942 to the verge of soil saturation may have contributed to cold injury during the following January. Under nearly adequate soil moisture conditions a t all times, even moderately injured trees live and maintain productivity. However, under the conditions of high temperature and frequently inadequate moisture supply, any injury to peach trees, no matter how slight, quickly weakens the trees and makes them even more susceptible to winter injury and other disorders (Cowart and Savage 1941). Howard (1924) reported that soil moisture seems important to root hardiness and survival in a variety of ways. Emerson (1903) and Howard (1924) found greater root injury under dry soil conditions than in moist soils. Hampson and Sinclair (1974) have detailed the development of Valsa canker of peach in relation to water supply. ii. Oxygen Deficiency (Wet-Feet). The ability of plants to survive a period of oxygen (02) deficiency varies greatly among species (Bergman 1959). An extensive review of literature by Rowe and Beardsell (1973) showed that waterlogging produces many adverse changes in the root environment which basically can be attributed to O2 deficiency. In ad-
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35
dition to indirect effects on the soil, 0, deficiency has a direct effect on root metabolism itself. Literature also shows that the effects of O2 deficiency on plants may be compounded by the formation of hydrogen sulfide in some waterlogged soils and by the auto-toxic production of hydrogen cyanide (HCN) by the roots of species which contain cyanogenic glycosides. Waterlogging caused a rapid decrease in root prunasin (the predominant cyanogenic glycoside in peach roots) and in the chlorophyll content of the leaves (Mizutani et al. 1977). Excess carbon dioxide and ethylene formation in waterlogged soils can add to the direct effects of deficiency. Poor performance of plants under such conditions can therefore result from a complex of interacting factors which make it extremely difficult to isolate any one change as being more important than others. This is complicated by two additional factors. Firstly, the importance of each factor varies with the plant species, and secondly, not all soils undergo the same changes when they become 0, deficient due to waterlogging (Bergman 1959; Rowe and Beardsell 1973). Rowe and Catlin (1971) reported differential sensitivity to waterlogging and cyanogenesis by peach, apricot, and plum roots. Individual plants varied considerably, but peach and apricot were more sensitive to waterlogging than was plum. All three species became more sensitive with a temperature increase of between 17°C and 27”C, and a scion of a more tolerant species did not overcome the sensitivity of the roots. They also reported that both cyanogenic glycoside content and its proportion that was hydrolysed during waterlogging were higher in peach than in plum roots. An exposure of detached root systems of all three species to anaerobic conditions caused HCN to be released (cyanogenesis), and cyanogenetic rate was increased with both temperature and time. They found a close correlation between differential sensitivity, hydrolysis of glycoside, and cyanogenesis under anaerobic conditions; however, the latter may have been secondary, though contributory, to cellular disorganization as a cause of sensitivity. Anaerobic soil conditions cause cyanogenesis in peach roots but aeration reverses it (Mizutani et al. 1977). Chaplin et al. (1974) reported cultivar differences in peach root tolerance to waterlogging and “wet-feet” resistance, with ‘Rutgers Red Leaf’ being most tolerant and ‘Lovell’ least tolerant under Kentucky conditions. The cultivar differences for severe root damage in one-yearold peach seedlings with roots submerged for two to four days was noted also by Marth and Gardner (1939). In the case of apple roots, prolonged periods of submersion during tree dormancy caused little damage; however, if any leaf surface was present during root submersion there was likely to be more damage (Heinicke 1932). Adverse effects by O2 deficiency in terms of disease problems also have been cited. Biesbrock and Hendrix (1970) reported that the condition of
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soil water and temperature had a marked and differential influence on peach root necrosis caused by P y t h i u m uexans d.By and P. irregulare Buis. Saunier (1966) evaluated a number of widely used rootstocks, which were subjected to controlled flooding, for their capability to recover (asphyxiation) and classified them in the following three groups in decreasing order of susceptibility: (1) apricot, cherry, and peach seedlings; ( 2 ) plum seedlings and M 9 and M 1 apples; (3) M 2 and M 13 apples, P r u n u s marianna, and quince. There was a close correlation between resistance to winter flooding and resistance to summer flooding. In addition, a strong influence of scions on the rootstock resistance to “wet-feet” was also observed. Influence of O2 supply on plant parasitic nematodes in soil was studied by Van Gundy et al. (1962), where they correlated nematode activity and survival with O2 diffusion rate in the soil pore spaces, which was largely related to the soil moisture content. The rate of O2 supply critical for all nematodes tested (Meloidogyne, Pratylenchus, Xiphinema, etc.) was around 30 X l o s gcm - 2 minute - l . However, some species were more sensitive to the length of exposure than to concentration. Highest incidence of gummosis in apricot was observed following a heavy rainfall causing waterlogging, and it was suggested that clogging of the vessels by gum was related to an inadequate supply of O2 to roots (Heimann 1968).
iii. Temperature Extremes. Literature dealing with the effects of temperature extremes on plant growth processes has been thoroughly reviewed by Langridge (1963). In many species, it has been shown that growth ceases a t a temperature only slightly above the optimum, but may be restored by addition of a single factor. If the growing temperature is raised a little higher, a further factor becomes necessary, and thus, these requirements become progressively more numerous with increased temperature. The process of chlorophyll formation appears to be very sensitive to cold. I t seems probable that the inactivation of enzymes a t low temperature can be attributed to an increase in intramolecular hydrogen bonding and is compatible with the concept of H-bond forming a t low temperature and H-bond breaking a t high temperature. Thus, a single enzyme reaction may become limiting to growth above or below a critical temperature. In another review, Levitt (1951) clearly showed that frost, drought, and heat resistance are all basically similar. In the peach-growing areas where high temperatures do not prevail over an extensive period, long-lived orchards are to be expected (Cowart and Savage 1941), whereas high temperature with inadequate water supply adversely affects survival. Also, root submersion accompanied by high temperature is likely to cause severe damage (Heinicke 1932). Bennett (1950) showed the antagonistic effect of high temperature on dormancy development in pears. T h e negative effect of direct solar ra-
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
37
diation during winter was emphasized by the benefits of winter shading to reduce bud injury. High temperatures of 15" to 23°C during winter on the West Coast were shown to antagonize the dormancy-releasing effect of cold. High cambium temperatures occurring in late winter as a result of solar radiation impinging on the bark of peach trunks caused a loss of hardiness following dormancy break. When these high daytime temperatures were followed by a rapid drop of temperature to near freezing a t night, severe injuries often resulted, contributing greatly to PTSL (Jensen et al. 1970). While working with the physiological dwarfing in peach seedlings, Pollock (1962) noted that germination a t 22°C produced almost normal plants whereas the plants produced a t 25°C were severely dwarfed. All tested peach cultivars responded in the same general way.
iu. Combination of Above Factors. The literature reviewed in preceding sections indicates that there are many instances where a combination of anaerobiosis, drought, and heat, when coupled with cold, can severely affect the plant processes, leading to complete plant destruction, devitalization or predisposition to other disorders. For example, Chandler et al. (1962) indicated that physical factors probably were responsible for PTSL in the Southeast. Excessive rainfall in late winter, resulting in waterlogged soils, and a freeze in February, following a period of unseasonably warm weather, definitely were contributing factors to the death of 200,000 peach trees in Georgia in the early spring of 1962. Similar informationon apple is provided by Wildung et al. (1972a, 1973). Thus, it is obvious that it is not easy to separate the effects of individual factors, especially when they act simultaneously or follow in succession. 2. Microclimatic (Cultural).-This portion of environmental factors will cover those items that affect plant microclimate in the immediate vicinity of trees or individual orchards in a limited area. The main consideration will be given to cultural practices and nutritional aspects.
a. Cultural Practices.-Such contributory practices as crop rotation, pruning and training, cover crops, irrigation, and tillage operations will be discussed in this section as related to their effects on short life and replant problems. Cultural practices play a vital role in hardiness (Hung and Jenkins 1969; Nesmith and Dowler 1976; Stuart 19391, and thus, bad cultural practices contribute significantly to the cause of PTSL (Savage 1970; Savage and Cowart 1942a). Any practice that stimulates a high level of vigor and/or retards normal hardening, increases the potential hazard of cold injury (Rollins e t al. 1962).
i. Crop Rotation. Most short life or replant problems may be avoided simply by switching to new land if it is available; however, new land suitable for orchards is unavailable in many fruit regions. Often the same
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land is used repeatedly for the same crop because of specificity of certain crops to their respective areas of cultivation. Several reports indicate that successive plantings of peach trees on the same sites contribute to PTSL (Clayton 1977; Savage and Cowart 1942a; Taylor et al. 1970; [Jpshall and Ruhnke 1935). Most peach replants dying are those established on locations of previous peach trees. Mountain and Boyce (1958a) found three to four times greater soil populations of Pratylenchus penetrans in soils with previous peach history than in those with no such history of peach production. Similarly, repeated croppings with apple andcherry were found toaffect their respective specific replant diseases (Pitcher et al. 1966). On the other hand, Proebsting (1950) did not find any evidence of peach failure when peach succeeded apple; other fruits did well after peach. Smith and Stouffer (1975) have suggested that establishment of new orchards by interplanting young trees in mature orchards of the same crop should not be started until the ground has been thoroughly worked, the old roots removed, and the land planted to a grain in a rotation for a t least one to two years. As Savory (1966) noticed in greenhouse culture, crop rotations are seldom feasible since replant diseases are so persistent in the soil. In such cases, pre-plant fumigation following rotation should be beneficial (Miller and Dowler 1973). Good (1960) established th at nematode injury to peaches can be reduced substantially by use of crop rotations, in addition to fumigation a n d planting with resistant plant material. Rotation of deep-rooted cover crops between orchards has proved to be beneficial for tree longevity (Savage 1970).Day and Serr (1951) observed severe short life of peach in a repeated peach rotation in California.
ii. Pruning and Training. Both time and extent of pruning influence short life and replant problems. Hibbard (1948) found no great differences in size of the trees under various systems of pruning, viz., moderate, light, and corrective. The trees more heavily pruned made wood and shoot growth a t the expense of fruit production, a n d therefore corrective pruning was done accordingly. Different pruning methods can cause marked differences in the strength of peach wood (McCue 1915). Cain and Mehlenbacher (1956) did not find trunk growth to be a reliable guide to controlled pruning. The apoplexy problem of apricots has been directly connected, in relation to its severity, with the height and type of the trunk, damage being absent or very minor on high-budded trees with clean trunks (Iliev 1968). Increased pruning severity tends to decrease yield and red color on fruit and delay peach fruit maturity, but increases fruit size, terminal growth, and percentage of nitrogen in the foliage (Schneider and McClung 1957). Heavier pruning materially reduces horizontal root extension; however, the degree of pruning does not alter the nature of the root system other than its total growth and distribution
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
39
since there is generally a proportional reduction in weight of all sizes of roots in heavily pruned trees (Savage and Cowart 1942b).Cummings and Ballinger (1972) obtained highest yields with lightest pruning although fruit size was reduced. Daniell (1975) reported significant yield increases reflecting tree survival in peach due to time of pruning, where February, March, and May pruning proved superior to November- January pruning. Fall pruning of many leading apple cultivars is likely to result in severe injury if prolonged periods of sub-zero temperatures follow (Burkholder 1936). However, Way (1954) reported that fall pruning had no measurable effect on the hardiness of ‘Cortland’ apple twigs. Pruning time is very critical from the standpoints of tree short life and survival, vigor, trunk cambial browning, hardiness, bacterial canker, and cold injury (Chandler 1974; Chandler and Daniell 1976; Clayton 1968, 1971, 1977; Nesmith and Dowler 1975; Prince and Horton 1972). Daniell (1973) reported that the time of pruning, however, had little or no effect on longevity and tree growth, when trees were grown on new peach land. Prince and Horton (1972) noticed little injury and no tree death when peach trees were pruned on different dates on a site with no short life problem. They found, however, greater trunk cambial browning in trees on a short life site that were pruned in November and December than in trees that were pruned in January, and still less browning in trees pruned in February. Tree mortality followed the same trend as that for browning. Similar deleterious effects of fall and early winter pruning in peach have been cited (Chandler 1974; Chandler and Daniell 1976; Clayton 1971, 1972, 1975a,b; Correll et al. 1973; Dowler 1972; Nesmith and Dowler 1973, 1975,1976).Weaver et al. (1974) reported that peach tree mortality on a PTSL site wasdue to cold injury and bacterial canker, and was not influenced by time of pruning. Further, they reported that on new land adjacent to the PTSL site early pruning caused trees to be more susceptible to cold damage, but the trees recovered and none died. Stene (1937) observed variable effects of pruning severity on winter-injured peach trees. Relatively severe pruning after leafing out was most beneficial for tree health.
iii. Cover Crops, Mulch, and Weed Control. In a four-year study, Boynton and Anderson (1956) found that the effects of mulching on tree behavior were similar and additive to the effects of nitrogen fertilization, and caused a substantial increase in potassium uptake by tree roots. Bell and Childers (1956) studied the effect of three systems of soil culture (clean cultivation, sod, and sod plus mulch) on growth, yield, and manganese content of peach trees in New Jersey. Trees grown in sod culture made comparatively less growth than did trees in other systems. In the same area, no significant differences in tree growth or yield resulted from
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HORTICIJLTIJRAL REVIEWS
sawdust mulch, straw mulch, or manuring, although corncob mulch supplemented with fumigation produced significantly more growth than other treatments (Shannon and Christ 1954). In peach orchards, the importance of cover crops in relation to nutrition and hardiness has been reported by Proebsting (1961) and Raw1 (1935). McBeth and Taylor (1944) suggested that in areas where root-knot nematode is a problem, peach tree performance can be significantly improved by growing only nematode-resistant and -immune cover crops. Yield was increased also by clean cultivation and trap cover crop treatments, but neither of these practices seems to be practical. Parker et al. (1966) found Sudan grass and both perennial and annual rye grass to be beneficial as cover crops to combat devastating effects of the lesion nematode. Deep-rooted cover crops like alfalfa, clover (Lespedeza sericea), and coastal bermuda grass used in a rotation between orchard plantings have increased peach tree longevity in Georgia (Savage 1970). In some cases, successful rouging programs for plant species which serve as alternate hosts for specific diseases have demonstrated the negative effects of poor sanitation and weeding practices. X-disease has been observed only in peach and nectarine orchards where infected chokecherry was found (Lukens et al. 1971). Where chokecherry was not weeded out, 72% of peach trees showed X-disease in 3 years but only 13% of the trees were affected where it was removed. Sarasola and de Bustamante (1970) obtained a sharp reduction in pear decline and apple collar rot in the western sectors of orchards in Argentina by planting Poplar windbreaks to protect apple and pear trees from the prevailing winds and to prevent abrupt changes of temperature a t sunset.
iu. Irrigation and Tillage Operations. Recent experiments in North Carolina showed that irrigation did not influence total yield, growth, or longevity of ‘Elberta’ or ‘Redhaven’ peach trees (Cummings and Ballinger 1972). On the other hand, Way (1954) reported that twigs from ‘Cortland’ apple trees that were irrigated in the fall suffered significantly greater freezing injury than did twigs from non-irrigated trees. Slater and Ruxton (1954) confirmed that on frosty nights the minimum air temperature immediately over uncultivated or compacted soil is higher than that over cultivated or loose soil. T h e studies of Hendrix and Powell (1969) as well as the ten-point program reported by Miller and Dowler (1973) stress modifications in some vital cultural practices to improve the chances of peach tree survival. According to these reports, tree root destruction by discing is harmful, though subsoiling following planting is beneficial, particularly where herbicides are used, to improve subsurface drainage and breaking of hardpan layers to allow better root colonization. Savage et al. (1968) presented the following view with regard to subsoiling in Georgia peach orchards. Many peach orchard soils in
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41
the Georgia Piedmont have O2 levels of 15% or less during a great part of the growing season. Under these conditions, preplant subsoiling to a depth of about 50 cm has nearly doubled the growth and yield of peach trees and greatly increased tree longevity. T h e increased growth, production and longevity were accomplished even though soil moisture was decreased in the subsoiled plots.
b. Nutritional.-To avoid short life and replant problems, nutritional considerations focusing on type, amount, balance, and time of application have been stressed (Clayton 1975a; Harrison 1958; Otto 1972b; Parker et al. 1966; Savory 1966; Spivey and McGlohon 1973; Taylor 1972). It is considered t hat improper nutrition is devitalizing; thus, weakening of the trees indirectly affects survival. However, Gilmore (1963) showed th a t a less fertile soil did not promote the peach replant effect in soil pot culture. Beattie (1962) evaluated ATD in Ohio and found symptoms normally associated with nutritional troubles. Later, Donoho et al. (1967) concluded th at cultural and management practices or nutrition did not appear to be related to ATD, except when they directly contributed to the lowering of soil pH.
i. Soil p H and Liming. Acidity of the growing medium does not appear to be a universally crucial factor for short life problems, although its contribution is significant. Savory (1966) has clearly demonstrated th a t the apple replant problem seems to be absent or unimportant in some places such a s in sandy soils with moderate soil acidity. Similarly, Hoestra (1968) found th at low p H soils are less heavily infested with SARD than near-neutral soils, and acidification of the latter leads to a growthstimulating effect. However, ATD, in Ohio, has been found closely associated with a low soil pH, ranging from 4.2 to 5.0 (Banta 1960; Beattie 1962; Beattie et al. 1963; Donoho et al. 1967). Similarly, in Australia, Sitepu and Wallace (1974) found positive correlation between growth decline of apple trees and such factors as species of P y t h i u m and Phytophthora, nematodes, and texture, moisture, and p H of soil. Out of these factors p H was suspected to be the most important. Extensive studies under both controlled and field conditions were carried out by Weaver and Wehunt (1975) to correlate effects of low p H on bacterial canker development and population growth of Macroposthonia xenoplax to PTSL in middle Georgia. Sizeable mortality of peach seedlings was noticed in soil with unadjusted pH, whereas no plants died in soils adjusted to pH 6.4 to 7.2. In December, populations of M. xenoplax were greater in soils adjusted to above 6.1 pH, but differences were not significant in March and April. In addition, numbers of propagules of P y t h i u m species in soil and recovery from roots were positively correlated with soil pH. In greenhouse studies, addition of high-Ca or high-Mg lime benefited peach planted in old peach soil with low p H (Havis 1962). However,
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HORTICULTURAL REVIEWS
soil treatment with lime and various fertilizers at two locations in Texas failed to show any effect on tree growth and survival (Havis et al. 1958). In addition to raising soil pH, lime also increased leaf Ca and Mg contents. In a similar study, Boynton and Anderson (1956) found that liming caused a decreased uptake of potassium by roots but a net gain in leaf magnesium. Parker et al. (1966) recommended lime application in New York orchards for combating replant problems, and a second application was suggested when soil pH appeared to be too low a t the start of planting. Another greenhouse study a t Beltsville, Maryland, showed that from treatments of high-Mg lime, CaS04, MgS04, and NaC03, the most striking growth response was obtained with the addition of a relatively low rate of high-Mg lime (Prince et al. 1955). It was recognized that much of the response obtained was not well understood and that the results of this study might be applicable only to the particular soil used. The present understanding in Georgia seems to be that yields can be maintained and tree survival extended by following good liming and balanced fertilization practices (Spivey and McGlohon 1973; Taylor 1972). Liming also has been included as an important practice in the 10-point program recommended by the PTSL Work Group (Miller and Dowler 1973). Based on well established field observations, the New Jersey Experiment Station has recommended a regular use of complete fertilization together with frequent liming in orchards planted on the light Coastal Plain soils (Davidson and Blake 1937). Havis (1962) reported that new peach trees had grown without any difficulty in old orchard locations a t Beltsville, Maryland, where about 1.5 tons of lime were thoroughly mixed into the loam soil. Supplemental nitrogen plus dolomitic lime produced a trend of further increases in tree survival and yield in Georgia (Giddens et al. 1972).
ii. Type and Amount of Fertilizers. In soil pot cultures designed to stimulate the peach replant problem, nitrogen suppression due to stimulation of biological activity of peachroot wood seemed to be the causative factor (Gilmore 1963). Soil as well as foliar applications of nitrogen on declining apple and peach trees have been found to help maintain yields and extend survival (Banta 1960; Spivey and McGlohon 1973; Taylor 1972). Hewetson (1953, 1957) and Higgins et al. (1943) were convinced that a readily available nitrogen supply gave replant trees a rapid early start, maintained vigorous growth, and increased their resistance to cold injury and hence, premature tree death. This treatment quickly establishes the trees, perhaps in turn helping to overcome any inhibiting effect of the trees previously grown on the same sites. It is further stated that if trees could be made to grow vigorously during their first year in the orchard, they might be expected to continue
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS F R U I T T R E E S
43
satisfactory growth and top performance in subsequent years. Supplemental nitrogen significantly increased survival and yield of peach trees even in a severe decline area (Giddens et al. 1972); however, a similar treatment did not stimulate growth and fruiting of affected apple trees (Donoho et al. 1967). Additional reports show the beneficial effects of nitrogen applications on vigor, survival, resistance to some diseases, and nutrient levels in plant tissues (Boynton and Anderson 1956; Kennard 1949; Nesmith and Dowler 1976; Sarasola and de Bustamante 1970). In the opinion of Raw1 (1935), application of nitrogen alone is improper since other plant nutrients are essential as well. In addition, a given dose of one form of nitrogen does not bring about the same growth response in a peach tree growing on a poor soil as compared to a rich soil, or in an unpruned tree as compared to a pruned tree (Blake 1928). Different forms of different nutrients show mixed effects-some beneficial, others harmful (Batzer and Benson 1958; Kennard 1949; Sarasola and De Bustamante 1970; Way 1954). Sodium nitrate (NaNOJ applied a t the rate of 350 lblacre on August 1 did not increase cold injury of sour cherry trees 50% defoliated by August 10, but the same amount of NaN03 decreased cold hardiness of trees fully defoliated by August 10 (Kennard 1949). Woodbridge and Lasheen (1960) obtained significant differences in nitrogen content of pear leaves from normal and decline-affected trees, which they suspected were a result rather than a cause of decline. Dekock and Wallace (1965) noticed iron chlorosis induced by nitrogen application in peach trees growing on calcareous soil. Nitrogen fertilization at rates adequately high to maintain vigorous peach tree growth increased cold hardiness and hence, resistance to premature death (Higgins et al. 1943). Increased levels of applied nitrogen do not appreciably affect cold hardiness (Edgerton and Harris 1950) or further growth increase (Chandler and Tufts 1933); however, nitrogen significantly interacts with pruning (Schneider and McClung 1957). Cummings and Ballinger (1972) reported increased peach tree loss with low nitrogen rates, although some random tree deaths occurred with higher nitrogen rates. However, Correll et al. (1973) did not find peach tree survival to be influenced by nitrogen levels. Nutrients other than nitrogen have not been so extensively studied in relation to short life and replant problems.
iii. Time of Fertilization. Edgerton (1957) applied nitrogen to ‘Cortland’ apple trees in the fall and early winter for three successive years to evaluate the effect on cold hardiness of twigs and bark, and on nitrogen accumulation in plant tissue. October and early November applications appeared to increase susceptibility of both twigs and bark to freezing, the effect being more noticeable in early than in mid-winter. Evidently, October applications with urea sprays were safer than an equivalent
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HORTIClJLTURAL REVIEWS
amount of ground-applied urea. However, ground application of NH4N0,r in December was not detrimental. In West Virginia Sudds and Marsh (1943) evaluated fall application of NaNOj to young apple trees in relation to winter injury. They concluded th a t under certain unknown conditions problems may occur when nitrogen is applied to orchards in the autumn, and that the nitrogen may help to predispose the trees to winter injury. In peach and some woody plants, time of nitrogen application does not seem to have much effect except for producing minor differences in foliar nitrogen levels (Schneider and McClung 1957) and cold acclimation (Pellett 1973). Late application of nitrogen significantly increases cold resistance of ‘Redhaven’ twigs (Chaplin and Schneider 1974) and wood hardiness in other peach cultivars (Higgins et al. 1943). Waltman (1937) reported that since root activity during the winter is minimal, peach trees fall-fertilized with calcium cyanamide may be less subject to winter injury because of the tissue’s lowered percentage of soluble nitrogen. Therefore, any nutritional practice increasing tissue nitrogen level during dormancy will seriously hamper cold hardiness and hence, tree survival. iu. Nutritional Deficiencies a n d Interactions. Davidson and Blake (1937) demonstrated th at an adequate amount of a nutrient may vary with the concentration of other nutrients present in the root medium. Based on extensive experiments on the response of young peach trees to nutrient deficiencies, Davidson and Blake (1936) produced an exclusive report on nitrogen, phosphorus, potassium, calcium, and magnesium deficiency symptoms in general, as well as on leaves, stems, and roots. Nutrient deficiencies may cause unbalanced metabolism, thereby initiating short life and finally tree death (Frenyo and Buban 1976; Parker et al. 1966). Nutrient deficiencies either in the plant tissues (Beattie 1962) or in the soil (Otto 1972b) have not been conclusively found to be associated with short life and replant problems. Lower calcium with higher manganese in the declining apple trees was thought to be associated with lower soil p H (Beattie et al. 1963); but soil potassium seemed to be related to decline, since decline soil contained lower potassium levels. Gallaher et al. (1975) reported higher concentrations of total calcium in peach leaves from declining trees, but since these trees had fewer and smaller leaves, less total calcium was found in decline than in healthy trees. Savage (1972) found th at there was a great increase in peach tree death (up to 83%)in field plots with low calcium level (soil and leaf analyses) as compared to plots with adequate calcium (up to only 10% mortality). Backman et al. (1969) found th a t calcium and magnesium ions suppress the toxicity of syringomycin, an antibiotic polypeptide t ha t is a toxin in bacterial canker (Pseudomonas syringa4 of peach. Stimulation of peach seedling growth by root-knot nematodes has
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
45
been associated with greater accumulation of calcium and magnesium (Chitwood et al. 1952). Batzer and Benson (1958) used Zn and Fe chelates to help overcome arsenic toxicity of peach trees in Washington. Zinc chelate was most economical in correcting arsenic toxicity, while iron chelate was phytotoxic and tended to intensify zinc deficiency. Bell and Childers (1956) found no relation between leaf Mn and peach tree growth which was positively correlated with Fe, P, Mg, or K in the leaves. Manganese deficiency was more pronounced a t soil p H of 6.5 or above, with intensity of deficiency symptoms directly related to the dryness of the season. Daniel1 and Chandler (1976) correlated Fe deficiency in liquid culture with bacterial canker development in peach, since plants receiving no Fe developed the longest cankers. No significant differences in canker length occurred between treatments containing Fe. An increase in bacterial canker severity also might be due to an Fe deficiency brought about by excess phosphate (Cameron 1962). Leaf chlorosis in peach has been attributed to deficiency of Fe or Mg or both (Chitwood et al. 1952). Hansen (1955) studied leaf and stem injury on almond and peach due to excess boron as influenced by the rootstock used. Almond and peach trees on almond rootstocks showed least injury. Bunemann and Jensen (1970) observed no improvement in the inhibition of apple seed germination and growth of seedlings and grafts by adding potassium to thoroughly washed quartz sand previously used as the medium. Beattie and Flint (1973) showed th a t optimum K level for frost hardiness seems to be within or below the optimum range for growth. With an increase in K supply, plant K levels increase with a corresponding decrease in plant nitrogen. Seedlings of several peach cultivars showed significant differences in the leaf levels of N, P, K, Ca, and Mg when grown in a sand medium supplied with nutrient solutions with high and low K (Thomas and White 1950). Leaves from seedlings grown in low K contained more P and Ca than those from high K solution. T he plant root system liberates into the surrounding medium a number of organic substances like amino and organic acids, the qualitative composition of which is markedly different with a change in the mineral composition of the medium (Tsitsilashvili 1977). Significantly discernible amounts of valine were found in the medium with abundant K, and oxalic acid was detected in K-deficient medium. Frenyo and Buban (1976) reported more distinct seasonal variations in the concentrations of ammoniacal N and phosphate P, but not K, in leaves from apoplexyaffected apricot trees than in leaves from healthy plum trees. Yablonskii (1975) identified several forms of P in buds and one-year-shoots of peach. The content of total P and its separate fractions in different cultivars did not correlate with their degree of winter hardiness. In comparison
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with less winter-hardy cultivars, the winter-hardy ones were characterized by a closer correlation of P metabolism with environmental factors and other metabolic processes.
B. Pathogenic Factors Numerous pathogenic factors contribute to short life and replant problems. However, as discussed in the subsequent sections, it should be clearly understood th at they are not soleiy responsible for the difficulties in question; rather, they act sequentially or simultaneously following predisposition of tissue by environmental factors, or the environmental injury is more likely to be severe if the tree is weakened by pathogens. Otto (1972a,b,d) ruled out the possibility of soil physical and nutritional factors for apple replant disease in Germany, but supported the involvement of microorganisms like bacteria or actinomycetes in the weakening of roots. Benson and Covey (1976) and Rallo (1973) agree on minor effects of some specific pathogens, but only a t certain stages of plant growth. Still we lack total agreement on the decisive role of pathogens in SARD and replant diseases of apple (Bollard 1956; Ross and Crowe 1973; Savory 1966). In the early spring of 1962, no pathogenic organism was consistently associated with the diseased tissue, although yeasts and bacteria seemed a t least partially responsible for killing thousands of peach trees in Georgia (Chandler et al. 1962). However, in addition to cold injury and nutritional disturbances, peach replant failures have been reported to be caused by the activity of insects, bacteria, certain fungi, and nematodes (Clayton 1975a; Koch 1955). 1. Bacteria.-Short life problems related to bacteria generally lead to the sudden death of a susceptible plant in spring. Bacterial canker, apoplexy, blast, bacterial gummosis, dead-bud condition, bacteriosis, lilac blight, and sour-sap are common names given to a disease of several stone fruits around the world which is caused by two related species of bacteria-Pseudomonas syringae and Ps. mors-prunorum. T h e bacterium attacks the plant tissues only after defoliation, and tissue damage occurs only during the dormant stage of trees (Gardan e t al. 1975; Klement et al. 1974) where the infection results in a characteristic cellular degradation in the phloem and cambial region (Davis and English 196913). Several predisposing and/or enhancing factors including cold injury, pruning time, phytotoxins in the rhizosphere, other pathogens, and physiological activities of the tissue closely interact with the bacteria (Chandler and Daniel1 1974, 1976; Davis 1968; Dowler and King 1967; Dowler and Weaver 1975; Klement et al. 1972; Petersen 1975; Rozsnyay and Klement 1973).T h e pathogen, green fluorescent pseudomonads, can be isolated from infected tissue only up to a certain time of the year
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT T R E E S
47
(Cameron 1970; Jones 1971a; Kouyeas 1971). The distribution and frequency of infection varies depending on fluctuations in seasonal moisture and temperatures (Cameron 1970). A study in England (Anon. 1966) more or less ruled out the possibility of nematodes and viruses as causal organisms in the apple replant problem, and emphasized the bacterial involvement. Bacterial blast of pear in Chile (Cancino et al. 1974) and Connecticut (Sands and Kollas 1974) has been caused by Pseudomonas syringae infection, usually following either cold stress or wet weather. In Belorussia, Ps. syringae is widespread where it attacks cherry and pear, then apple and plum following low temperature exposure, with trees dying in the first year or after several years in chronic cases (Dorozhkin and Griogortsevich 1976). In Greece, Ps. amygdali sp. nov. causes bacteriosis only in almonds where infection persists throughout the year and induces perennial swollen cankers (Psallidas and Panagopoulos 1975). Bacterial decline or apoplexy of apricots in southern Europe has been a serious problem for some time, due to Ps. syringae infection compounded by cold, Cytospora, Phytophthora, and other Pseudomonas species (Babos et al. 1976; Gardan et al. 1973; Klement et al. 1974; Kouyeas 1971; Prunier, Gardan and Luisetti 1970). Bacterial canker of sweet cherry, caused by Ps. mors-prunorum, recently has become a destructive disorder causing a shortage in cherry tree supply in Poland (Lyskanowska 1976). Pseudomonas syringae also a t tacks cherries, causing bacterial gummosis or canker (also called lilac blight and dead-bud condition in the western United States), and a t times reaches disastrous proportions (Blodgett 1976; Jones 1971a). Bacterial canker caused by Ps. syringae has been very closely associated with the short life and death of peach trees in many growing areas (Clayton 1968, 1977; De Vay et al. 1968; Dowler and Petersen 1966; English 1961; English and De Vay 1964; Lepidi et al. 1974; Petersen 1975; Petersen and Dowler 1965; Weaver et al. 1974; Zehr et al. 1976). However, Dowler and Petersen (1966) could not assign Ps. syringae as the only cause of all the observed PTSL-related difficulties, since cold injury and pruning time played important roles. Clayton (1968) pointed out that cold-injured peach bark often is invaded by the cankers or wood decay organisms and, a t times, cold injury alone is sufficient to kill trees even without the involvement of the canker-causing organisms. Gardan et al. (1975) correlated peach decline with sensitivity to Ps. mors-prunorum f s p . persicae only during fall and winter months, with a climax during defoliation. 2. Fungi.-Sitepu and Wallace (1974) found P y t h i u m species, nematodes, and soil p H together inhibiting apple tree growth, which is the first step towards decline. Jones (1971b) described Phytophthora collar rot of apples in Michigan as causing poor terminal growth, foliar dis-
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HORTICITLTITRAL REVIEWS
coloration, and eventual tree death in severe cases. In California, the Pear Research Task Group (Anon. 1971) has furnished a detailed account of decline and replant problems of pear and the general root rot and crown rot syndrome including Armillaria root rot. Several fungal organisms, such as Cstospora, Verticillium, and Phytophthora, have been noted to cause apoplexy and premature die-back of apricots (Babos et al. 1976; Kouyeas 1971; Paclt 1972; Rozysnyay and Klement 1973). In all these cases cold and/or pruning time and other predisposing factors have been recognized. Cambial gummosis in P r u n u s domestica infected with Cytospora cincta apparently is associated with cold injury as a prime contributing factor (Helton 1961; Helton and Randall 1975). In western Europe, Thielaviopsis basicola is involved in the cherry and plum replant problems (Hoestra 1965; Pepin et al. 1975; Sewell and Wilson 1975).Mircetich and Matheron (1976) implicated three species of Phytoph thora (P. cambivora (Petri) Buisman, P. megasperma Drechsler, and P. drechsleri (Tucker)) directly in the root and crown rots and death of cherry trees in poorly drained California commercial orchards. Further damage to nematode-injured cherry roots, and hence a loss in tree cold hardiness, may be caused by the invasion of certain fungi, disturbing the metabolism and water and nutrient uptake (Edgerton and Parker 195813). Blodgett (1976) explained recurring death of cherry trees in Washington state on the basis of Verticillium wilt, Phytophthora crown rot, Cytospora canker, and Armillaria root rot, all of which became severe under poor drainage and waterlogged conditions. T he most important fungal agent in PTSL is perennial canker complex of peach caused by the species of ValsalCytospora, which occurs most readily during the dormant season, with low temperature and Pseudomonas syringae canker implicated as important predisposing factors (Banko and Helton 1974; Cameron 1971b; Clayton 1971, 1975a, 1977; Hampson and Sinclair 1973; Hickey 1962; Hildebrand 1947). Cytospora fungi often finish killing the peach trees after cold and bacterial canker injuries (Clayton 1968, 1977). Another fungus closely linked with the PTSL problem is Clitocybe tabescens (Fr.) Brez. (Chandler 1969; Cohen 1963; Petersen 1961; Rhoads 1954; Savage and Cowart 1942a, 1954; Savage et al. 1953). However, this fungus has not been found to be the sole factor responsible for early mortality (Rhoads 1954; Savage and Cowart 1954), although it may cause very heavy losses on old sites. Phycomycetous fungi (water molds), especially Phytophthora and P y t h i u m species, appear to be the most damaging factor in PTSL under excessive soil moisture conditions (Biesbrock and Hendrix 1970; De Vay et al. 1967; Hendrix and Powell 1970a,b; Hendrix et al. 1966; Hine 1961b; Mircetich 1971; Mircetich and Keil 1970; Powell et al. 1965; Taylor e t al. 1970). However, Lownsbery e t al. (1973) did not find sig-
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT T R E E S
49
nificant growth reduction due to Pythium, and no interaction between the fungus and nematode (Macroposthonia xenoplax) was noted. Root necrosis and related effects of these organisms are secondary factors in PTSL, and the severity of tree-killing varies depending on temperature and soil moisture. Armillaria root rot is another cause of tree mortality, which often attacks already weakened tissues (Cameron 1971b; Savage and Cowart 1942a). Poor growth of peach replants, and severe decline and death of peach trees also have been associated with the disorders caused by Fusicoccum amygdale Del., Cylindrocladium floridanum, Botryosphaeria dothidea, Physalospora persicae, and some species of Fusarium and Rhizoctonia (Abiko and Kitajima 1970; Hine 1961b; Hung and fJenkins 1969; Sobers and Seymour 1967; Weaver 1971, 1974b). 3. Nematodes.-Nematodes play a significant role in the short life and replant problems of deciduous fruit trees. Hoestra (1961) reported that 65% of the apple orchards in Holland appeared to be infected with Pra tylenchus penetrans, and damages were severe. Further, nematodes form a part in the complex of‘ factors contributing to replant problems of apple, but they are not the cause of SARD (Hoestra 1967). Stylet-bearing parasitic nematodes were found to be partially responsible for stunting of apple trees in Australia (Sitepu and Wallace 1974). An earlier report by Colbran (1953) established that root-lesion nematode (Pratylenchus coffeae Zimm.) was widely distributed in the Stanthorpe district of Australia and was the most important contributor to the unthrifty growth of replants in many old orchards. Nevertheless, reports from some European countries and Canada show that nematodes are not involved in such apple problems as replant, decline, or SARD, despite the fact that soil steaming and fumigation alleviated growth reduction (Anon. 1966; Pitcher et al. 1966; Ross and Crowe 1976; Savory 1967; Winkler and Otto 1972). The longevity and productivity of ‘Montmorency’ cherry on both Mazzard and Mahaleb rootstocks in New York state were seriously hampered by the parasitic nematode (Pratylenchus penetrans Cobb.); pre-plant fumigation restored normal cold hardiness and survival (Edgerton and Parker 1958a,b; Mai and Parker 1967; Parker and Mai 1956). Although nematode involvement in specific cherry replant disease in England has been ruled out (Pitcher et al. 1966; Savory 1967), the disease is probably caused by a soil microbial organism(s), since soil sterilization often has eradicated it. Wehunt and Good (1975) have reviewed the literature regarding nematode involvement in PTSL. They said that the role of nematodes in the PTSL complex has not been determined; however, nematicide treatment of orchard soil usually brings improvement, indicating that nematodes
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are somehow involved. Increasing evidence suggests that one or more species of nematodes contribute to the PTSL syndrome, and th a t nematode control would, a t least partially, eliminate PTSL (Davis 1968; English 1961; English and De Vay 1964; Hendrix and Powell 1969, 1970a; Savage and Cowart 1942a). Root injury is usually the result of the combined effect of root-knot galling by root-knot nematodes, root pruning by dagger nematodes, and necrosis and decay by root-lesion nematodes and associated microorganisms (Good 1960). Root-knot nematodes, including several species of Meloidogyne, have been found in the vicinity of certain declining peach trees, particularly in light soils, but have not been directly associated with PTSL (Burdett e t al. 1963; Chitwood et al. 1952; Dhanvantari et al. 1975; Foster 1960; Foster and Cohoon 1958). Clayton (1977) demonstrated th a t trees on root-knot resistant rootstocks, e.g., Yunnan, ,937, Nemaguard, or Okinawa, are more susceptible to PTSL than are those on root-knot susceptible Love11 rootstock. Ring nematodes (Macroposthonia xenoplax and M. curuatum) have been associated with PTSL, affecting tree growth and longevity during winter and/or spring when they are a t highest population density (Barker and Clayton 1973; Chitwood 1949; Chitwood et al. 1952; De Vay et al. 1967; Foster 1960; Hung and Jenkins 1969;Johanson 1950; Lownsbery 1959; Weaver et al. 1974; Zehr et al. 1976). Lesion nematodes (Pratylenchus penetrans and P. uulnus) are important primary parasites and true plant pathogens. Their main role in peach replant seems to be the ability to incite root degeneration by providing extensive infection sites for other pathogenic soil microorganisms (Foster 1960; Mountain and Boyce 1957; Mountain and Patrick 1959). These nematodes are associated with decline and PTSL, especially when peach follows peach in an orchard rotation (Barker and Clayton 1969; Bird 1968; Chitwood 1949; Johanson 1950). Mountain and Patrick (1959) reported that the main mechanism involved in the formation of lesions is the production of phytotoxic substances through hydrolysis of cyanophoric 0-glucoside (amygdalin). They reported th a t P. penetrans is capable of hydrolysing amygdalin in uitro. Other predominant nematode species t ha t received attention regarding their role in PTSL-related disorders are Belonolaimus, Trichodorus, Tylenchorhynchus, and X iphinema (Chitwood et al. 1952; Foster 1960).Smith and Stouffer (1975) reported t ha t the soil-borne nematode (Xiphinema americanum Cobb.) transmits the virus which causes P r u n u s stem pitting in peach. 4. Viruses an d Mycoplasma-Like Organisms (MLO).-Although viruses, along with nematodes, have not been thought to be so important in the replant problems in England (Anon. 19661, it is believed th a t the causal agent of apple decline in the Valtellina area of Italy is a virus or
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mycoplasma (Refatti 1970a).Cameron (1971b) discussed the synergistic reaction between new cultivars and some viruses, which sometimes results in the death of apple trees. Apple stem grooving virus was found not to be the causal factor in the union necrosis and decline syndrome of apple on the East Coast; however, some scionlrootstock combinations were very severely affected (Stouffer et al. 1977). Pear decline probably is caused by an MLO carried by pear psylla (Anon. 1971; Blattny and Vana 1974; Cameron 1971b; Hibino et al. 1971; Hibino and Schneider 1970; Nyland and Moller 1973; Westwood and Cameron 1978). Blodgett (1976) used the term “induced incompatibility” when viruses or MLOs are involved in pear decline. Pear decline in Greece appears to be the result of union incompatibility, stem pitting, and wood necrosis, possibly due to some unidentified transmissible factor (Agrios 1972). Westwood and Cameron (1978) established th at remission of pear decline symptoms is dependent on the environment since it occurs during some dormant seasons, and th at reinfection by the psylla vector may be necessary for the disease to continue. Western X-little cherry disease and X-disease of cherry are caused by MLOs, where complete wilting and death of mature trees result in serious losses (Blodgett 1976; Granett and Gilmer 1971). Cherry decline in western Europe results from an MLO infection vectored by leafhoppers and other efficient virus vectors (Fos 1976; Kegler et al. 1973). A widespread incidence of Prunus stem pitting (PSP)in California’s cherry and other Prunus orchards has been revealed (Mircetich et al. 1977). PSP also has been reported from the East Coast (Smith et al. 1973; Mircetich and Fogle 1969). Posnette and Cropley (1970) associated decline disease of plum with Prunus necrotic ringspot virus (PNRSV) which is specific to only certain cultivars. Based on observations, PNRSV and related agents contribute to increased sunburn, perennial canker, chronic die-back, short life, rosetting and decline, and predisposition to other infections (Cameron 1971b; Scotto La Massese et al. 1973; Smith and Neales 1977; Stubbs and Smith 1971). PSP of peach is a recent disease which occurs sporadically all over the United States and affects almost all cultivars (Cochran 1975). According to Cameron (1971b), PSP appears to be a virus-induced rootstock-scion reaction responsible for severe problems in some parts of the United States. Ringspot viruses have been implicated as the causal factors of PSP (Smith and Stouffer 1975; Smith et al. 1973), though Agrios (1971) suspected MLOs a s the cause. MLOs also have been cited as being responsible for phony disease, Western X- and X-disease, and peach rosette, all of which, in one way or another, are involved in PTSL and related syndromes th a t cause heavy tree losses (Hutchins 1933; Jensen 1971; Kirkpatrick et al. 1975a; Sands and Walton 1975; Savage and Cowart 1942a).
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5. Insects.-In most cases related to short life, insects act as vectors for disease agents. The prevalence of 17-year locust or cicada (Majicicada spp.), in addition to low pH, has been associated with ATD (Donoho et al. 1967). Heavy populations of cicada nymphs were found under most, if not all, declining apple trees (Banta 1960; Beattie 1962). Several research groups have confirmed pear psylla (Psylla pyricola) as the main vector for MLOs which cause pear decline (Cameron 1971b; Hibino et al. 1971; Hibino and Schneider 1970; Nyland and Moller 1973; Westwood and Cameron 1978). Psylla carries MLOs in the salivary glands and foregut (Hibino et al. 1971). However, attempts to transmit pear decline in Argentina by budding or psyllids failed (Sarasola and De Bustamante 1970). Cherry decline (caused by MLOs) in Tarn-et-Garonne, France is transmitted by leafhoppers, especially Fieberella florii (Fos 1976). Peachtree borer (Sanninoidea exitiosa Say) and lesser peachtree borer (Synanthedon pictipes Grote and Robinson) have been added by Savage and Cowart (1942a) to the list of factors in PTSL. However, these borers do not appear to play a major role as do cold injury, bacterial canker, and other similar factors. MLOs responsible for Western X-disease of peach are transmitted by Colladonus montanus (Van Duzee) leafhopper to the host plants (Jensen 1971).
6. Pathogenic Interaction.-Interaction and synergism frequently are noted among different pathogenic causal factors in producing severe short life and replant effects. Cameron (1971b) showed that PNRSV contributes to increased incidences of Cytospora canker, and that peach trees do not show symptoms of Armillaria root rot unless they have previously acquired PNRSV. In a glasshouse test a t Harrow, Ontario, Meloidogyne hapla injury on peach, with a 62-day incubation period, resulted in an increased infection by Agrobacterium tumefaciens, but no such interaction was noted when the incubation period was 157 days (Dhanvantari et al. 1975). Similar results in almonds were found by Orion and Zutra (1971). Lownsbery et al. (1973) reported that the addition of Pythium spp. a t planting time increased peach susceptibility to Pseudomonas syringae less than did the inoculation with Macroposthonia xenoplax. No interaction between M. xenoplax and Pythium spp. was noted. However, nematodes also are important in carrying, aiding entry of, or otherwise interacting with bacteria and fungi (Lownsbery and Thomason 1959). An interaction between M. xenoplax and Ps. syringae was responsible for the death of plum tree tops a s a result of cankers (Mojtahedi et al. 1975). The consistent association of PSPagents, Tom RSV and TbRSV, with the capability of Xiphinema americanum to transmit the agents has been established (Smith et al. 1973; Smith and Stouffer 1975). Rozsnyay and Klement (1973) reported that Valsa cincta and Ps. syringae produce similar symptoms of apricot
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apoplexy, since simultaneous inoculations with both pathogens caused more extensive cankers than those produced by either alone.
C. Physio-Biochemical Factors I. Phytotoxins.-For a long time, “soil sickness” and phytotoxins in the soil have been suspected as factors responsible for the unsatisfactory growth of second and subsequent plantings of the same crop on the same sites (Gilmore 1949; Savory 1966; Otto 1972b). Phytotoxins may cause disease symptoms, by inhibiting or changing membrane permeability (Owens 1969), which are characteristic of most plant disorders and represent the initial response of plants to any pathogenic or non-pathogenic causal factor. Phytotoxins predispose the plant to infection as well as to stress and thus, are actively involved in the establishment of the disorders in the host plants (Wheeler and Luke 1963).
a. Microbial Phytotoxim-Literature on the phytotoxins from plant parasitic microorganisms has been thoroughly reviewed by Strobe1 (1974) and Wheeler and Luke (1963). Wheeler and Luke (1963) concluded that, in contrast to most phytotoxins, hydrocyanic acid or hydrogen cyanide (HCN), which is produced by an unidentified group of basidiomycetes and other organisms, may be directly involved in disease development. HCN is toxic to plants under most conditions (Hine 1961a). Patrick (1955) discussed the microbial phytotoxins in relation to the peach replant problem in Ontario. It was demonstrated that substances which inhibit the respiration of excised peach root tips are produced when peach root residues or chemically pure amydgalin is acted on by certain microbes occurring in old peach orchard soils. This reaction did not take place when other soils or root residues were used or when the soil was autoclaved before amygdalin addition. In tests on peach root tips aqueous extracts of phytotoxins showed 40 to 90% physiological activity within 30 minutes. In addition to inhibiting respiration, these substances also induced tissue darkening and finally necrosis of meristematic cells. All of these effects were irreversible after tips had been in the toxic leachates for five hours, whereafter the tips apparently were killed. On the basis of further studies with water solutions of pure chemicals and enzymes, it was concluded that the microbial action on the amygdalin fraction of peach roots is mainly responsible for the toxic factor frequently encountered in old peach sites. Rowe and Catlin (1971) reported that temperature and 0 2 deficiency played an important role in amygdalin hydrolysis and cyanogenesis. They also reported that differential sensitivity among peach, plum, and apricot roots existed for both cyanogenesis and HCN toxicity. Gardner et al. (1974) reported a rapid hyperpolarization in membrane electropotentials in the tissue susceptible to
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HORTICULTURAL REVIEWS
the phytotoxin. A phytotoxin obtained from three isolates of Valsa cincta caused leaf collapse, gum production, and necrotic wounds when absorbed by young intact apricot shoots (Rozsnyay and Barna 1974). Furthermore, this toxin was an exotoxin of high molecular weight, where protein and lipid components of the toxin did not produce toxic effects; however, the presence of a carbohydrate component was believed to be an important part of the toxic agent. Syringomycin is another such phytotoxin which is produced by Pseudomonas syringae, the inciter of bacterial canker on peach and other stone fruits (Backman et al. 1969).
b. Plant Residues.-In some sites where root damage has been especially severe, new trees cannot be established when old orchards are removed. Toxic chemicals released from old roots occupy an important position in the list of causal factors of replant problems on old sites (Gilmore 1949; Havis and Gilkeson 1947; Israel et al. 1973; Oh and Carlson 1976; Parker et al. 1966). Borner (1959) presented the following account of the apple replant problem in Germany. Experiments were carried out to investigate the cause of the apple replant problem from the standpoint of a possible action of substances released from plant residues into the soil. Addition of as little as 2 g/liter dried apple root bark to water cultures produced a strong reduction in apple seedling growth. Paper chromatography revealed five phenolic substances from bark held in nutrient solutions for about a month. The same toxins were present in cold-water extracts from soils containing apple root residues. Of the five phenolic toxins present in the nutrient solution and water extracts of soil, only phloridzin could be identified as a natural constituent of the apple root bark and wood, although quercitrin also was detected. The other four phenolic toxins were detected in soils within two to ten days following addition of pure phloridzin to different soils. I t is quite obvious, therefore, that these other phenolics were the decomposition products of phloridzin. The detected compounds were identified, and were found to occur in soils as follows: Phloridzin +phloretin
f
phloroglucinol p-hydroxyhydrocinnamic acid +p-hydrobenzoic acid
Of these toxins, phloridzin and phloretin caused the strongest effects. T o what extent these phenolics participate in the apple replant problem is not clear a t this time. In discussing apple and cherry replant problems in England, Savory (1967) stated that although the cause(s) of replant disease is not yet known, it does not include phytotoxins, once thought to be released from the decomposing roots of the previous crops, since it was found that root residues were not harmful to the replants.
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Peach trees growing on a severe decline site did not respond to peach root residue applications (Giddens et al. 1972). However, there are reports that the leachate from different tissues of peach shows a definitive role in reducing apple and peach seedling growth by directly affecting their root systems (Chandler and Daniell 1974; Israel et al. 1973; Oh and Carlson 1976; Patrick 1955; Proebsting and Gilmore 1941). Davis and English (1969a) and Chandler and Daniell (1974) correlated the effects of peach seed and root leachates with bacterial canker incidence in peach. The latter workers postulated that when trees are replanted on old peach sites, their uptake of some water-soluble toxic substance(s1 from dead peach roots may predispose them to bacterial canker and contribute to PTSL. Proebsting and Gilmore (1941) reported that addition of peach root residue inhibited growth of peach seedlings even in virgin soils. Further, in sand culture, the root bark-not the wood-was found to be toxic. The alcohol extract of bark also was toxic, while the residue from alcohol extraction was not. No specific compounds were identified or estimated. However, Havis and Gilkeson (1947) found no evidence of any toxic substance in peach roots or peach leachates which adversely affected the growth of young peach trees in high-nutrient sand culture. In fact, they found that new roots of trees, planted in crocks to which chopped old roots had been added, actually penetrated well into the bark and along the cambial zone of the old roots without apparent injury to themselves. Ward and Durkee (1956) studied seasonal and tissue variation in amygdalin content of peach trees. I t was shown that amounts varied from none in the woody tissue to more than 50 mglg of dry tissue in some roots, with highest concentrations found in the root bark. Factors such as cultivar and season significantly affected the content of this glycoside. Amygdalin breakdown probably does not account for the difficulty of establishing peach trees in certain old peach soils in some areas of California (Hine 1961a). This theory is based on the observations that amygdalin addition to non-autoclaved soils was toxic to growing peach seedlings, but if a 14-day period elapsed between these additions and planting, tests for HCN were negative and cyanide injury was not evident. Studies by Israel et al. (1973) in Georgia showed that peach root bark contained appreciable amounts of HCN, which was released into the medium from live roots following mechanical injury. Furthermore, extracts from peach soils caused greater inhibition to respiration of peach root tips than extracts from non-peach soils. They also observed that peach root bark and amygdalin reduced the total microorganisms, actinomycetes, Pythium, and pathogenic nematode population of an old peach soil.
c. Spray Residues.-Benson and his co-workers (1974a, 1976, 1978) studied arsenic (As) toxicity in Washington state apple orchard soils.
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Lead arsenate residues from insecticide sprays used for codling moth prior to DDT were still present in the soil in moderate to high concentrations in the 1970’s. Apple seedling growth has been negatively correlated with soil As concentration where 450 ppm total As completely inhibited growth. Total As is not a good measure of As toxicity, and is a minor factor in apple tree growth when the total soil As concentration is less than 150 ppm. Apple seedling growth decreases linearly with corresponding increments of freshly added As to the threshold above which there is no growth. Greenhouse studies of a soil without the As factor showed a 4.4fold seedling-growth increase with methyl bromide fumigation. Correlation coefficient values indicated that a large portion of As is not available to plants, and thus some other factor is a t least as important as the soil As in apple replant problem. Consequently, soil As concentrations less than the threshold of 150 ppm, which are often found in orchard soils, contribute less to the replant problem than their biological counterparts. However, in peaches, apricots, prunes, and cherries, As residues cause systemic As toxicity (Blodgett 1976). It was also reported that young apple trees grow poorly in As soils, whereas cherries are probably the least affected among the stone fruits. Batzer and Benson (1958) experimentally showed that zinc chelate economically corrected As toxicity in peach trees.
d. Other Phytotoxins.-Callus cultures derived from Prunus besseyi and P. tomentosa were more sensitive to sodium cyanide than were those from peach (Heuser 1972). Bernstein et al. (1956) studied the effect of
salt accumulation on growth of several stone fruits. They found that about half of the growth reduction was due to chloride toxicity, the other half to increased osmotic pressure of the saline solution. Aluminum (Al) toxicity also is considered a potent factor in PTSL (Kirkpatrick et al. 1975b). Data from this study suggested that an available concentration of soil A1 greater than 3 ppm which injured peach roots and inhibited plant growth, may do so by inducing an imbalance in such nutrients as Ca, Mg, Mn, and P in peach seedlings. Jones et al. (1957) found extracts from peach buds, twig bark, and leaves to cause growth inhibition in pea bioassay, which exceeded the inhibition caused by sodium cyanide solution containing an equivalent amount of cyanide. Any treatment which removed the cyanide from the extracts caused a loss of inhibitory activity. Later, Jones and Engie (1961) identified the toxic substance in peach extracts as mandelonitrile. Israel et al. (1973) reported that benzaldehyde and potassium cyanide were toxic to rooted peach trees in the greenhouse, and both chemicals inhibited respiration of peach root tips. They also reported a similar suppression of respiration by benzoic acid, mandelonitrile, and aqueous isolates of peach root bark incubated in peach and non-peach soils.
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2. Biochemicals.-Although major biochemicals, carbohydrates, proteins, lipids, nucleic and organic acids, and phenolics may not be the direct causes of short life and replant problems, they exert tremendous influence on plant condition. In fact, biochemical differences set the stage for action by other primary factors. In one way or another, almost all of these major cell biochemicals play critical roles in the replant problems (Bachelard and Wightman 1973; Borzakovska et al. 1975; Kaminska et al. 1971; Lasheen and Chaplin 1971; Lasheen et al. 1970; Lebedev and Komarnitskii 1971; Rozsnyay and Barna 1974).
a. Carbohydrates (CHO).-After growth ceases in late summer, maturation of wood and buds of deciduous plants begins with a corresponding accumulation of CHO, and then cold hardiness develops, due largely to conversion of insoluble starch to soluble sugars (Chandler 1954; Lasheen et al. 1970; Lebedev and Komarnitskii 1971; Levitt 1959; Raese et al. 1977). Dowler and King (1966) reported that in early fall peach twigs and branches contain large amounts of reserve CHO, which the tree may use during dormancy to maintain cold hardiness. Removal of these reserves through early pruning may render the plant more susceptible to PTSL. In addition, older trees are less sensitive than younger ones to such removal, possibly because greater CHO reserves are stored in large trunks and branches. Williams and Raese’s (1974) report indicated that sorbitol and sucrose are important reserves of storage CHO in apple trees during physiodormancy. Rozsnyay and Barna (1974) believed that a CHO component of the phytotoxin from Valsa cincta isolates was evidently responsible for toxicity to apricot trees. High and stable levels of soluble sugars usually have been correlated with the condition of frost resistance (EL-Mansy and Walker 1969; Lasheen et al. 1970; Lebedev and Komarnitskii 1971; Levitt 1959; Raese 1977; Raese et al. 1977; Williams and Raese 1974). However, Layne and Ward (1978) found that both bud and shoot hardiness of peach were closely correlated with total sugars, sucrose, and reducing sugars in the shoots from autumn to spring. They found no correlation between hardiness of buds and apical shoots and total CHO or starch. Lasheen and Chaplin (1971) have reported similar results between hardiness and endogenous levels of these CHO. Levels of starch usually are inversely related to soluble sugars (Raese et al. 1977). Stanova (1977) found that several isolates of Cytospora cincta, which caused typical canker symptoms on peach and apricot, effectively assimilated fructose and xylose but not glucose. Polyols (polyhydric or sugar alcohols), which make up another group of CHO amounting to about 40% of the total sugar content in some fruit species, are considered to play some part in the increase of frost resistance of plants (Sakai 1961). This is based on the observations t h a t seasonal variation (increase in polyol contents during cold period and decrease during warm weather)
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is often observed (Sakai 1966; Williams and Raese 1974). Raese (1977) reported that in most cases the combined content of soluble sugars and polyols, particularly sorbitol, in two-year-old apple trees was slightly higher in treatments that induced cold hardiness than in controls. In peach, however, Rohrbach and Luepschen (1968) found that sucrose, glucose, fructose, and mannitol increased significantly from August to January, while sorbitol decreased significantly. The least winter-hardy peach, ‘Earlyglo’, was found to contain a slightly higher mannitol concentration. Polyols in peach tree bark were correlated with winter injury and the initiation of Cytospora canker infection.
b. Proteins and Other Nitrogenous Compounds.-Proteins play a major role in plants’ development of freezing tolerance. Brown and Bixby (1975) reported that soluble protein concentrations remain relatively constant during early stages of freezing tolerance development, but increase significantly during later stages; whereas, insoluble proteins remain comparatively unchanged throughout the induction period. Qualitative changes in protein contents, evident by their appearance and disappearance corresponding to changes in hardiness levels, indicate some possible connections between hardiness and levels of soluble protein (Craker et al. 1969; Donoho and Walker 1960). Other workers also have associated proteins with cold hardiness in different species under varying conditions (Bachelard and Wightman 1973; Borzakovska et al. 1975; Holubowicz and Boe 1969, 1970; Kenis and Edelman 1976; Lasheen et al. 1970; Siminovitch e t al. 1967). In apple seedlings, a relationship exists between cold hardiness and certain amino acids (Holubowicz and Boe 1970). Kaminska (1973b) and Kaminska et al. (1971) showed that free amino acids were involved in the proliferation disease of apples. Alanine has been reported to play a positive role in defoliation (Larsen 1967; Rubinstein and Leopold 1962). According to Lasheen and Chaplin (1971), total free amino acids in peach leaves were high in the spring, but decreased quickly to a minimum in the fall. In shoots, the level was relatively high in spring, decreased in early summer, increased to a maximum in late summer, then gradually leveled off during fall and winter. c. Fatty and Organic Acids.-Phospholipid degradation in frozen cells of less hardy trees has been intimately associated with freezing injury (Yoshida and Sakai 1974). However, Siminovitch et al. (1975) found that quantitative augmentation of phospholipids per se, or of whole membranes in the cells, is the important component of the hardening process. The increased ratio of unsaturated to saturated fatty acids with increased hardening is the most striking change in the relation of fatty acids to hardiness in peach (Ketchie 1966). An increase in the unsatur-
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ated fatty acids in the various membranes of the plant cell would change the structure and some properties of the membranes, which might be suitable for frost protection. The increased levels of free unsaturated fatty acids also might alter the properties of the cytoplasm, thereby making it less viscous and more flexible, and hence the cytoplasm might be less vulnerable to freeze injury. St. John and Christiansen (1976) concluded that chilling resistance is related to the level of linolenic acid in the polar lipid fraction in the developing root tips. Lepidi et al. (1974) isolated and examined bacteria from the inner rhizosphere of young peach replants in normal and diseased sites in Italy. Bacteria from the diseased site were more numerous and more active in metabolizing compounds other than organic acids. The utilization of organic acids by rhizosphere bacteria was, however, greater in the control plants on the normal site. In another study on the peach replant problem in Japan (Mizutani et al. 1977), benzoic acid and other ultraviolet-absorbing substances were detected from roots sensitive to waterlogging and soil sickness.
d. Phenolics.-Borner (1959) investigated the cause of the apple replant problem in relation to a possible involvement of phenolics released from residues in the soil. All five phenolic substances revealed by paper chromatography strongly inhibited growth of apple seedlings. Cultivar differences in phenolics from apple trees with and without proliferation disease were noted by Kaminska et al. (1971). Masking of proliferation symptoms by other disorders reduced this variation. Decrease in phenolic inhibitors’ activity as a result of polyphenol oxidase activity was found to be an important event in the sequence of phenomena which lead to the dormancy release in peach (Kenis and Edelman 1976). e. Other Biochemicals.-Dorsey and Strausbaugh (1923) indicated that browning in the wood was due, a t least in part, to a condensation of storage materials, which apparently were thereby transformed into gums and tannins. Chirilei et al. (1970) distinguished two types of gummosis in apricot problems in Romania. The first, “xylem gummosis,” which produced water-insoluble gums (pectic acid), causes apricot apoplexy. The second, known as “cortico-cambial gummosis,” produces water-soluble and exuding gums (pectins), and is responsible for a slow decline of apricots. Siminovitch et al. (1967) ascertained that a rhythmic pattern of seasonal changes in water-soluble proteins, RNA, and protein synthetic capacity in living bark cells closely parallel similar rhythms in bark cells’ resistance to freezing injury. The cyclic variations begin with striking abruptions in the early fall with a rise in RNA from the low summer value, followed closely by similar rises in protein, protein synthetic capacity, and freezing resistance. Thus, augmentation of protoplasm becomes a part of the mechanisms of freezing resistance.
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Enzymes play a vital role in the biochemistry and physiology of replant problems through resistance and susceptibility reactions of plant tissues. Langridge (1963) reported that the probable inactivation of such enzymes a t low temperature may be due to an increase in intramolecular hydrogen bonding. Thus, below a critical temperature a single enzyme reaction may become limiting to growth. Conversely, Steponkus and Lanphear (1967a) showed that the high correlation between cold hardiness and T T C reduction might be due to a co-factor and substrate limitation rather than inactivation of dehydrogenases. McCown et a l . (1969) found in winter hardy plants a gradual synthesis of two to four new peroxidase isoenzymes during the hardening period, whereas only a relatively weak initiation of one isoenzyme was noted in tender plants. In addition, the formation of the new isoenzymes preceded the period of hardening by several weeks, depending on the specific isoenzymes and the plant type. Ladd et al. (1976) reported differentially-decreased soil enzyme activities, lowered viable bacterial population, and an increased ninhydrin reactivity as a result of soil fumigation. However, they found a non-consistent relationship between the release of ninhydrin-reactive compounds following fumigation and changes in bacterial population or changes in soil enzyme activity. 3. Phytohormones and Growth Regulators.-The evidence outlined in this section will strongly suggest that some degree of hormonal control is present over such physiological phenomena as dormancy, cold hardiness, disease condition, resistances to different problems, and overall plant growth and development. For details relative to these controls, the reader is referred to the articles by Taylorson and Hendricks (1976), Wareing and Saunders (1971), Samish et al. (1967), Jacobson (19771, and Viglierchio (1971). Current knowledge suggests that control of plant growth and development involves complex interactions of phytohormones in a system of checks and balances, and thus it would be expected that the above responses also would involve phytohormonal imbalances. Abscisic acid (ABA), gibberellins (GA), auxin (IAA), cytokinins (CYK), and perhaps ethylene may each be implicated in the variations of responses, plant species, and tissues or organs. Samish et al. (1967) explained the concept of dormancy regulation in peach with reference to phytohormones. An accumulation of inhibitors induces dormancy. This is followed by mid-dormancy, during which low temperatures and short photoperiods are connected with initial reduction in inhibitors and subsequent appearance of promoters. Finally, the release from dormancy is obtained through additional patterns of phytohormone balances. A full understanding of hormonal regulation can be achieved only by knowing the precise action of the phytohormones and the state of dormancy a t the molecular level (Wareing and Saunders 1971). In this respect, Jacobson
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(1977) believed that RNA synthesis and its regulation are required for all phytohormonal responses. Endogenous phytohormones controlling dormancy and growth can be employed to modify plant chemistry, thereby manipulating dormancy regulation to prevent untimely frost injury (Walker 1970). Viglierchio (1971) concluded that, along with mediating causes of growth disorders reflecting disease symptomology, one must, of necessity, consider synthetic and degradatory mechanisms that result in the establishment of pathological phytohormonal levels. a. Promoters-i. Auxins. Increased cell permeability often reflects pathological or premortal conditions, and IAA and GA have been reported to change permeability depending on concentration (Stadelmann 1969). According to Carter (1976), PTSL appears to be caused by coldinjury to the vascular cambium. He found an elevated IAA level in fallpruned trees and those growing in non-fumigated soil, as compared to control trees. I t was suggested that early breaking of the vascular cambium's dormancy, caused by an altered phytohormonal balance, was responsible for predisposing certain trees to death by cold injury. Blommaert (1955, 1959) reported high concentrations of several indole auxins in peach buds preceding bloom, which reached maximum a t the end of dormancy when the buds began to open. Kochba and Samish (1972a) reported significant differences in the activity of several basic-ether soluble auxin-like phytohormones between Meloidogyne jauanica-resistant (Nemaguard) and -susceptible (Baladi) peaches. Viglierchio (1971) concluded in his review that viruses and fungi have been shown to reduce endogenous IAA levels in hosts and that IAA-degrading enzymes have been implicated in phytopathological symptoms of some disorders caused by nematodes. Exogenous applications of auxins have effectively modified certain physiological processes. Raese (1977) reported a 5.0"C increase in apple tree shoots' cold hardiness in November when 100 ppm naphthaline acetic acid (NAA) was applied 11 days after a 500 ppm ethephon application. NAA treatments of 0.25 to 1.0% applied to pruning cuts on 'Sungold' peach induced gummosis around the cuts but controlled sprouting, both of which were generally proportional to NAA concentration (Couvillon et al. 1977). Kochba and Samish (1971, 1972a) discussed the role of NAA application in nematode susceptibility of peach rootstocks. They found that NAA supplied by wick-feeding increased root growth, but reduced top growth of the trees. NAA also caused the development of swelled and non-suberized branch roots which became susceptible to M. jauanica. In addition, NAA application in combination with kinetin produced a synergistic stimulating effect on the endogenous cytokinin-like activity in roots and hence, an increased nematode susceptibility of both resistant and susceptible cultivar roots. Auxin treatments on apple trees,
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when applied ten and four days before Phytophthora cactorum infection, suppressed collar rot disease development; however, the same application four days after infection showed no effect on collar rot development (Plich 1976).
ii. Gibberellins (GA). Only limited work has been done on endogenous GA as related to regulation of cold hardiness, dormancy, and disease resistance. Bottini et al. (1976) concluded that the trend in seasonal variation in endogenous GA points to a differential action of GA during physiodormancy, its break, and the subsequent resumption of growth. Walker and Donoho (1959) compared the effectiveness of exogenouslyapplied GA on dormancy break of detached shoots from young apple and peach trees, and found that GA broke dormancy of peach trees but not of apples. GA applications a t 100 ppm to apple seedlings showed no influence on the development of cold hardiness, killing point, or levels of amino acids (Holubowicz and Boe 1969, 1970). However, Holubowicz (1976) reported that GA, when applied to one-year-old apple trees a t weekly intervals in August and September, produced varying degrees of cold resistance a t different times during the winter season. GA alone, or in combination with ABA, did not induce or enhance cold acclimation of defoliated branches under short days (Fuchigami et al. 1971). Plich (1976) found no significant effect of GA application on the development of collar rot (Phytophthora cactorum) on apple trees. Dennis (1976) reported moderate to severe winter injury to cherry cambium and buds as a result of GA sprays. Furthermore, Proebsting and Mills (1974) showed that cherry trees treated with GA on August 22 and September 12 had much more severe winter injury than the trees sprayed earlier or later. Deleterious side effects caused by GA treatments include gummosis (Dennis 1976; Proebsting and Mills 19691,twig die-back prior to freezing injury (Proebsting and Mills 19691,bud abscission or failure to open, and reduced fruit set in cherries and peach (Dennis 1976; Yadava and Doud 1977). Bottini et al. (1976) reported that, with GA application, peach foliage persisted two weeks longer than on control trees. Davis and English (1969a) found that Pseudomonas syringae cankers were reduced in size and number when leaf senescence was inhibited by GA application, while the cankers were increased by the acceleration of senescence with peach seed leachate. GA nullified the effect of peach seed leachate. Unchilled ‘Lovell’ seedlings sprayed with 250 ppm GA prior to inoculation with 2 isolates of Ps. syringae were more resistant to canker development than untreated seedlings (English and Davis 1969).
iii. Cytokinins (CYW. Krupasagar and Barker (1966) reported that plant roots infected with Meloidogyne incognita contained substances exhibiting CYK-like activity. However, extracts from healthy roots
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showed only about 16% CYK activity compared to extracts from galled roots. They detected CYK in roots 75 days after inoculation with M. incognita, but attempts were unsuccessful after 35 days. The CYK activity in the roots of Nemaguard and Okinawa peach rootstocks, which are resistant to M. javanica, was significantly lower when compared with susceptible Baladi and L 198-12 peach rootstocks (Kochba and Samish 1972a). Discussing the peach replant problem in Japan, Mizutani et al. (1977) showed that waterlogging caused a rapid decrease in root CYK levels, resulting in reduced chlorophyll content of the leaves. Cytokinin application through wick-feeding increased endogenous CYK levels in roots of peach rootstocks resistant to M. javanica which had lower levels initially (Kochba and Samish 1972a). However, this CYK application had no visible effect on peach seedling growth (Kochba and Samish 1971). According to Weinberger (1969), the CYK, SD 8339 a t 100 to 200 ppm, most effectively stimulated normal peach bud development when only a little additional chilling was needed to break dormancy. A combination of CYK and abscisic acid was found by Yadava and Doud (1977) to delay budbreak and improve subsequent balanced growth (with no blind wood) of peach plants which had their physiodormancy broken before phytohormonal application. Benzyladenine application has been reported to induce mobilization of cold hardiness promoters (Steponkus and Lanphear 1967b). Plich (1976) studied modification of Phytophthora collar rot susceptibility of apple trees as influenced by exogenous phytohormones. He found that CYK application greatly increased the size of necroses. The effect of CYK and ABA depended on the cultivars used. He suggested that phytohormones act indirectly on susceptibility through their effect on plant metabolism. b. Inhibitors-Wareing and Saunders (1971) are convinced that dormancy regulation and, hence, susceptibility of plants to stresses involve an interaction between growth promoters and inhibitors. The induction of physiodormancy is determined by the accumulation of growth inhibitors (Samish e t al. 1967). It also was indicated that the mid and end phases of dormancy are characterized by an initial reduction of inhibitors with the subsequent appearance of, or increase in, certain growth promoters. This view has been confirmed by several workers who found inhibitors disappearing from dormant tissues as the dormancy progressed (Blommaert 1959; Bottini et al. 1976; Eagles and Wareing 1964; Henderschott and Bailey 1955; Henderschott and Walker 1959). Eagles and Wareing (1964) showed that reapplication of an inhibitor isolated from plants apparently could induce normal dormancy in actively growing seedlings of the same species. More growth inhibitors were excreted from the peach replant roots under anaerobic conditions than when the soil was aerated (Mizutani et al. 1977).
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i. Abscisic Acid (ABA). High endogenous ABA levels could not be correlated with the initiation of cold acclimation of apple tree bark (Hammond and Seeley 1977). However, decreasing temperatures after growth cessation and increasing endogenous ABA levels during the same period did correlate with further cold acclimation. Some anomalous stock/scion effects on cold hardiness have been suspected due to indirect effects of several factors including imbalances of IAA, GA, CYK, and ABA (Westwood 1970). Lipe and Crane (1966) were the first to isolate ABA from peach seeds, and to correlate the endogenous ABA levels with peach bud and seed dormancy. They also were able to induce conditions indicative of dormancy in peach seedlings with exogenously-applied ABA. Fuchigami et al. (1971) reported that ABA separately or in combination with GA did not influence cold acclimation under short-day conditions. Holubowicz and Boe (1970) reported no correlation between soluble protein and killing point when ABA was included in the treatments. Moreover, i t was reported that 20 ppm ABA effectively increased cold hardiness of apple seedlings, but this treatment also decreased the seedlings’ rate of photosynthesis (Holubowicz and Boe 1969). Initial budbreak and growth on greenhouse peach plants which had their physiodormancy broken by chilling were inhibited by ABA treatment (Yadava and Doud 1977). Depending on time between inoculation with collar rot disease and ABA application, ABA can modify apple’s susceptibility to Phytophthora cactorum (Plich 1976). ABA application, both before and after inoculation with the disease, caused larger necroses on the trees.
ii. Other Inhibitors. The basic and most plentiful endogenous apple inhibitor that belongs to this category is phloridzin or dihydrochalcone (Kolomiets et al. 1970). The high winter hardiness of apple tissue following physiodormancy break is determined by the presence of phloridzin. Further, dormancy regulation in peach, unlike apple, is determined not by a single inhibitor but by an inhibitory complex. Also, peach plants do not possess the ability to synthesize the inhibitors with the physiological properties of phloridzin of apple during the transition to autumn-winter dormancy. This is apparently one of the factors behind low frost resistance of peach. However, the increase in flavonols towards the end of dormancy indicates t h a t they possibly may play a protective role in peach shoots similar to that of phloridzin in apple shoots. Raese (1977) obtained a slight increase in apple shoot cold hardiness for three winters with two annual applications of SADH in June. When applied a t weekly intervals in August and September, SADH produced varying degrees of hardiness in apple and peach a t different times during the winter season (Holubowicz 1976).SADH sprays followed by benomyl fungicide did not substantially improve Cytospora canker control over that of benomyl alone (Luepschen 1976). The benomyl and oil combination provided the
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best control of canker. However, no post-inoculation sprays reduced canker extensions. Kochba and Samish (197213)examined the effect of seven growth inhibitors on Meloidogyne jauanica development in the roots of the nematode-susceptible Baladi peach rootstock. Maleic hydrazide, thiourea, TIBA, and actidione most effectively inhibited gall formation as well as nematode maturation in the galls. The other three inhibitors, 7-aza-indole, 2-hydroxy-5-nitrobenzyl bromide, and 2,6 diaminopurine, effectively prevented gall formation, but once galls had formed nematode development was affected less. c. Phytohormonal Interaction-Dormant plant tissues apparently contain many promotive and inhibitory phytohormones. Thus, Walker (1970) proposed a balance concept between promoters and inhibitors. If the plant contains more “inhibition units” than “promotion units,” then the plant remains dormant and does not grow. When “promotion units” outnumber the “inhibition units,” dormancy is broken and growth may occur, provided adequate and suitable environmental conditions become available. Martin and Corgan (cf Walker 1970) have theorized that if the ratio of GA and CYK to ABA is high, growth will occur. If the two promoters are low relative to the inhibitor, growth ceases. They further postulated that the ratio may be influenced by suppressors or inducers of specific sites on DNA. DNA transfers the message to RNA, which passes it on to the specific proteins that form the enzymes necessary for either growth promotion or senescence and dormancy, depending on the environmental circumstances. Interaction between promotive and inhibitory phytohormones based on their balances has been reported to be an important factor in such processes as dormancy regulation, hardiness, chilling requirement, stock/ scion effects, disease resistance, etc. (Bowen 1971; Davis and English 1969a; Fuchigami et al. 1971; Holubowicz and Boe 1969,1970; Kochba and Samish 1971; Plich 1976; Samish et al. 1967; Wareing and Saunders 1971; Westwood 1970; Yadava and Doud 1977). Plich (1976) demonstrated interactions among IAA, CYK, and ABA which modify apple’s susceptibility to Phytophthora canker. H e showed that the phytohormones which were active in uiuo had relatively weak or no fungitoxic effects in uitro, and, thus, suggested that they act on susceptibility indirectly through their influence on plant metabolism. Kochba and Samish (1971) studied the role of NAA and CYK in peach rootstocks’ susceptibility to M. jauanica. These substances produced a synergistic effect, stimulating nematode development in roots of resistant rootstocks and increasing the nematode population in the susceptible rootstocks. Thus, NAA and CYK played a significant role in altering the host-parasite relationship in peach-nematode problem. GA application reportedly
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antagonizes peach seed leachate and nullifies its stimulating effect on Pseudomonas syringae canker development on peach (Davis and English 1969a).
IV. CONTROL MEASURES Controls for all the different fruit crop problems discussed in this review are not available. Whatever measures and management practices have been offered for the solution or minimization of these short life and replant problems are discussed under the following categories. A. Plant Improvement Through Breeding for Resistance A resistant plant is resistant usually for several different reasons, and no one single mechanism can be designated as the most important (Rohde 1965). Any loss of or lack of retention of resistance leaves plants with less survival value (Brierley 1947). Plants’ ability to protect themselves against more than one harmful factor leads to adaptive flexibility which enhances plant survival potential. Thus, knowledge of plants’ resistance to freezing, pathogens, and other stresses may help to substantially reduce damages. I t is not difficult for fruit breeders to justify improving fruit trees’ resistance to frost and plant pathogens, and their survival. Past fruit breeding and improvement programs, designed to incorporate desirable characters in cultivars as well as in rootstocks, have made dramatic contributions to fruit production, especially in extending their range of adaptation (Dorsey 1921; Parker 1963; Rohde 1965; Stushnoff 1972, 1973). Thus, the development of hardy and resistant cultivars and rootstocks by breeding appears to be the most effective and economic way available to combat short life and replant problems. Samish and Lavee (1962) stated that while the plant’sgenetic make-up controls the dormancy and chilling requirement of the various organs, its physiological state may modify the expression of these characters. This, they reported, is true for the entire tree as well as for different parts of any one plant. The inheritance of nematode resistance does not appear to differ in any significant respect from the inheritance of any other type of resistance or other qualities in plants (Hare 1965). Genetic studies have shown that slight differences in plants, controlled by one major gene in many cases, can make a plant resistant. Thus, it becomes logical to expect the presence of nematode resistance in most crops (Rohde 1965). It must be recognized, however, that some nematodes may feed on plants without response other than injury, and resistance to these types will be rare. According to Lownsbery and Thomason (1959), no available fruit cultivar or rootstock is resistant to all the kinds of nematode parasites
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which may be present. For this reason, the control measures most certain of success involve a choice of material resistant to the most common nematode species in a particular area, in addition to plant protection practices. Based on tests for root-knot nematode resistance in apple, peach, cherry, pear, plum, almond, and apricot seedlings, Tufts and Day (1934) suggested that one must consider the possibility that, in the absence of susceptible host plants, nematodes may attack partly resistant hosts. Furthermore, in the presence of very susceptible cultivars, these parasites may be attacked from the partly resistant hosts. On the basis of progeny analyses from reciprocal crosses between the hardy, less hardy, and tender apple cultivars, Wilner (1965) showed that frost resistance in apple appeared to be regulated by hereditary factors. He also reported that the resistance of the progenies tended to reflect that of their parental types, and was more favorably influenced by the maternal than the paternal parent. Lantz and Pickett (1942) reported that hardiness in apple progeny is based on multiple factor inheritance. Those apple rootstock types which start earliest in spring (M 9) seem most injured by cold, while those types which start latest in spring (M 16) are least injured (Stuart 1941).Apple rootstock breeders a t Geneva, New York have been working for some time towards developing improved and satisfactory replacements for the rootstocks presently available (Cummins 1977; Cummins and Aldwinkle 1974a,b,c).They perceive that problems, objectives, and breeding strategies in developing improved rootstocks are similar for most tree fruits in most parts of the world. Stock-related factors which are of particular importance from the breeding standpoint have been identified and assigned relative levels of priority. Large numbers of seedlings from controlled crosses are being screened during their first year for susceptibility to such pathogens as Phytophthora coctorum, Eriosoma lanigerum, and Erwinia amylouora. Criteria for later selection include propagability, freedom from suckering, cold hardiness, dwarfing, and induction of early, efficient production. The entire selection period is expected to require a minimum of 15 years. Their experience with this apple rootstock breeding program suggests that there is excellent potential for substantial improvement over existing rootstocks. However, no such program for developing improved rootstocks exists for the Southeast, except that rapid screening procedures have been developed for some pathogens only. Genetic variations in susceptibility to some pathogens, pear decline, winter hardiness, and chilling requirement have been observed among pear cultivars, rootstock clones, and certain species of P y r u s (Brown and Kotob 1957; Rallo 1973; Seemuller and Kunze 1972; Westwood 1976; Westwood et al. 1971; Wilcox 1936). This variation, depending on the type of heredity, could be utilized beneficially for developing more de-
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sirable rootstocks and cultivars. Westwood (1976) reported on the inheritance of pear decline resistance. This research to study rootstocks from resistant and susceptible parent types and those from resistant and susceptible crosses was initiated in 1968. All trees were grafted to ‘Bartlett’, and in most cases 14 to 32 seedlings of each cross were used as rootstocks. All the progenies of resistant parents were resistant to pear decline-though not to the same degree. Pyrus betulaefolia, P. calleryana, and several crosses of resistant P. c u m m u n i s showed a relatively low percentage of severe decline. Crosses of resistant and susceptible types were intermediate in response, whether or not the resistant parent was P. c u m m u n i s . The lack of complete resistance to decline in resistant crosses and gradation from healthy to severe decline in most cases indicated a complex inheritance involving multiple genes. Of all tested Pyrus species, P. betulaefolia is most resistant to the decline problem. Recent serious peach tree losses in most southeastern peach areas have prompted greater interest in breeding suitable rootstocks as a possible solution to PTSL. However, there has been little effort towards obtaining dwarfing, size control, or specific disease resistance (Sharpe 1974). Dwarfing in peach trees is an objective in the search for rootstocks resistant to cold and nematodes, and generally long-lived (Fogle 1975). Thus, continued research on peach scion and rootstock improvement by breeding and selection is essential to the peach industry’s economic viability and future (Carlson 1975; Layne 1974). Peach has been described as the most heterogeneous of temperate fruits, and cultivar variation has been reported for such characters as chilling requirement (Bowen 1971; Lesley 1944), cold hardiness (Blake 1935, 1938; Layne 1975, 1976a; Mowry 1960; Oberle 19571, status of important nutrients and phytotoxic chemicals (Rowe and Catlin 1971; Thomas and White 1950; Ward and Durkee 1956)’nematode resistance (Barker and Clayton 1969; Burdett e t al. 1963; Day and Tufts 1939; Hansen e t al. 1956; Hutchins 1936; Minz and Cohn 1962; Sharpe et al. 19691, resistance to other diseases (Luepschen et al. 1975; Lukens et al. 1971; Rowe and Catlin 1971; Smith and Neales 1977; Smith et al. 1977b; Vigouroux et al. 1972; Wensley 1966, 1970), “wet feet” tolerance (Chaplin et al. 1974; Marth and Gardner 19391, and growth and vigor (Conners 1922; Hutchins 1936). The chilling requirement in peach appears to be genetically controlled by multiple genes (Bowen 1971; Lesley 1944), and physiologically controlled by a phytohormone balance (Bowen 1971). Blake (1938) established that lower trunk hardiness and resistance to bark injury are not always correlated with hardiness of fruit buds. Lukens et al. (1971) reported that peach cultivars differ in susceptibility to X-disease, but none of the tested cultivars showed a high degree of resistance. Similarly,
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Luepschen e t al. (1975) found no significant resistance to Cytospora canker among ten peach cultivars; ‘July Elberta’ was the most susceptible of the group, while the rest were of intermediate susceptibility. Most of the breeding work for nematode resistance in peach has been on root-knot nematode species, with only a little on lesion nematodes. As surveyed in Israel, Shalil, Elberta, and Baladi peaches proved to be highly susceptible rootstocks to Meloidogyne jauanica, although Stribling’s 37 (S-37) peach showed a fairly high overall index of resistance to this nematode (Minz and Cohn 1962). On the other hand, Burdett et al. (1963) reported that, in addition to Elberta and Yunnan, S-37 supported a high population of M. jauanica, while M. incognita var. acrita reproduced only on Elberta. Under California conditions, Shalil, Bokhara, and Yunnan showed resistance to M. incognita var. acrita and were susceptible to M. jauanica, while seedlings of S-37 were reported to be resistant to the latter species. Hansen et al. (1956) reported that seedlings of Shalil and S-37 were immune or highly resistant to M. incognita var. acrita, whereas Lovell seedlings were very severely infected with this species as well as with M. jauanica. Five peach rootstock selections from a 1949 cross of P r u n u s dauidiana and a Chinese peach in Chico, California showed immunity to M . incognita and M. jauanica (Sharpe et al. 1969). I t was shown that resistance to both of these nematode species depends on different genes; to the former it was inherited as monofactorial dominant, while to M. jauanica it appeared to depend on two or more dominant genes. In 1966, a third type of root-knot nematode was discovered in Florida. I t reproduced readily on Okinawa, Nemaguard, and other lines which had been selected for resistance or immunity to both M. incognita and M. jauanica. Lesion nematodes (Pratylenchus u u l n u s and P. penetrans) are equally damaging to peach, and no resistant peach cultivars have been reported as yet (Barker and Clayton 1969). Lownsbery (1961) established that Lovell and S-37 peaches are poor hosts for Macroposthonia xenoplax. Since major breeding studies in the southeastern United States have concentrated on root-knot nematode resistance and general tree vigor, only a little attention has been paid towards obtaining tree size control or specific disease resistance. Sharpe (1974) suggested that wide crosses, involving various P r u n u s species, might offer dwarfing possibilities as well as resistance to nematodes and root rots. Clonal propagation of such material probably would be essential. Layne (1975, 1976b) has been involved for some time in breeding peach rootstocks a t Harrow, Ontario. His findings warrant that there is a need to find sources of resistance to nematodes and certain fungi, and tolerance to fine textured, imperfectly drained soils needs to be improved by testing peach X almond hybrids. More precise screening tests for evaluating rootstock hardiness and dis-
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ease and pest resistance, for testing resistance to waterlogging, and for assessing dwarfing capability and ease of propagation are also necessary. The breeding work on other P r u n u s species has not been so extensive. Pepin et al. (1975) found variation in cherry and other P r u n u s species, including their hybrids, for resistance to Thielaviopsis basicola root rot. Resistance to T. basicola in the P r u n u s pseudocerasus hybrids appears to be an important asset for these potential cherry rootstocks. Genetic variation among cultivars and species also has been reported for resistance to apoplexy of plums caused by Phytophthora spp. (Kouyeas 1971), and plum decline caused by P r u n u s necrotic ringspot virus (Posnette and Cropley 1970).
B. Rootstocks Sharpe (1974) emphasized that serious tree losses due to short life and replant problems have prompted greater interest in rootstocks as a possible solution. Rollins et al. (1962) suggested that consideration be given to cultivars, rootstocks, and interstocks prior to establishing orchards on problem sites. Foster et al. (1965) found that using resistant rootstocks along with more effective nematicides on a nematode-infected soil resulted in much more vigorous tree growth during the pre-fruitbearing years and much greater production in the early bearing years. Similarly, Ryan (1975b) stated that the use of resistant rootstocks contributes substantially to the control of specific replant diseases. Some rootstocks may enhance early winter hardiness simply by causing growth to cease earlier than on vigorous rootstocks (Westwood 1970; Layne et al. 1977). In addition to affecting tree vigor and growth, rootstocks are reported to considerably influence tree survival (Layne et al. 1976; Yadava and Doud 1978a). In some cases, tree mortality has been associated mainly with winter injury and canker infection but not with stionic incompatibility (Layne et al. 1976). Day and Serr (1951) noticed differential resistance to Pratylenchus vulnus among such crops as apricot, apple, pear, and quince rootstocks, as well as peach and plum cultivars used as rootstocks. Parker et al. (1966) reported that deeprooting rootstock types are less damaged by nematodes than are shallowrooting types, e.g., Mahaleb is a substantially better cherry rootstock than Mazzard for problem soils. Savory (1966) observed that rootstockscion combination had a significant effect on specific replant diseases of apple and cherry. Dorsey (1918b) showed that the cold hardiness of an apple scion was independent of the rootstock. However, a highly cold hardy scion does not give the rootstock measurably greater hardiness than does a less hardy scion (Chandler 1954). Filewicz and Modlibowska (1941) concluded that the freezing injury to the rootstock depends not
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only on its own resistance but also, to a large extent, on the scion cultivar growing upon it. They reported that root killing in Poland, during a cold snowless winter, was more influenced by the scion type. Stuart (1937) reported that scion hardiness was not measurably affected by rootstock hardiness, but that rootstock hardiness, on the other hand, was greatly influenced by the scion cultivar. However, Wildung et al. (1972b) recently reported that rootstock hardiness is not altered by scion cultivars. Saunier’s (1966) preliminary observations on rootstock resistance to root asphyxiation showed a strong influence of the scion on the rootstock resistance. Filewicz (1931) and Hilborn and Waring (1946) reported a reciprocal effect of rootstock and scion on cold hardiness. Certain apple scion/rootstock combinations seem to grow poorly and frequently show symptoms of tree decline, where affected trees often appear to be girdled (Stouffer et al. 1977). In this regard, clones of ‘Delicious’ propagated on MM 106 rootstock seem to be affected most severely; however, other scion/rootstock combinations exhibit similar symptoms which are typical of apple stem growing virus-induced disorders. Wildung et al. (1972b) investigated rootstock survival and root hardening pattern in apple. A comparison of M 9, M 7, M 26, MM 104, and M M 106 showed that M 26 was the most hardy and M 7 the least hardy of those tested. They concluded that scion hardiness seemed to be influenced more by maturity of the rootstock than by inherent hardiness in the rootstock. A sub-freezing temperature caused trunk splitting in scions on M 7 but these scions on seedling rootstocks were not injured, indicating that severity of cold injury was affected by the rootstock/scion combination (Simons 1970). Reporting on multiple-stock apple trees, Cummins and Forsline (1977) said that the effects of a rootstock on hardiness, anchorage, and suckering are somewhat altered by the interstem. The interstem tree is especially valuable for limiting certain disease problems and for permitting utilization of sites too wet or otherwise unsuitable for other apple rootstocks. Stuart (1937, 1941) indicated that the hardiness imparted to the rootstock by the scion bore no relation to the hardiness of the scion. Filewicz and Modlibowska (1941) emphasized that for rootstock hardiness, microclimatic conditions and, to a certain extent, the vigor of the rootstocks, are important. Rollins et al. (1962) pointed out that any practice tending to stimulate a high level of tree vigor and/or retarding normal hardening increases the potential hazard of cold injury. Campbell (1971) compared growth of young apple trees on virus-infected and healthy rootstocks. The amount of virus inoculum present was important in assessing the viruses’ impact on the growth. When four apple cultivars were bud-grafted on virus-infected rootstocks, substantial growth reduction resulted in the first two years depending on cul-
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tivars. The growth of ‘Jonathan’ and ‘Granny Smith’ apples on Sturmer seedling and MM 104 rootstocks, with and without apple mosaic strain of Prunus necrotic ringspot virus from mildly and severely diseased trees, showed significant interactions between cultivar and infection source, rootstock and infection source, and cultivar and rootstock (Johnstone and Boucher 1973). Ryan (1975a,b) strongly recommended the use of best rootstock (M 1 2 ) to control SARD in the Hawke’s Bay area of New Zealand. The recommendation of M 1 2 rootstock was made especially for those places where root diseases were a problem. In addition, the use of MM 115 and M 793 rootstocks in lighter soils and M 793 with fumigation on heavier soil was also recommended to ensure normal growth in orchards having SARD. Day and Serr (1951) reported that under California conditions, apple rootstocks were resistant to root-lesion nematode (Pratylenchus uulnus) attacks. Colbran (1953) reported from Stanthorpe district of Australia that the root-lesion nematode (P. coffeae Zimm.) was widely distributed in apple orchards, and that no apple rootstocks available in the district were immune to this species. Certain scion/rootstock combinations in Greece have been affected by pear decline with an increasing frequency in recent years (Agrios 1972). In these cases, graft union symptoms vary considerably with the scion/ rootstock combination, and often appear to be the result of graft incompatibility, particularly with pear on quince rootstock. Batzer and Schneider (1960) presented similar evidence indicating that pear decline in western United States is a bud union disorder closely associated with certain rootstocks. They also pointed out t h a t this disorder is not an inherent incompatibility of scion and rootstock, but appears to be an induced one. Furthermore, pear scions on oriental stocks like Pyrus serotina and P. ussuriensis were highly susceptible to pear decline, while those on imported French (P. communis) were intermediate, and trees growing on domestic Bartlett seedlings (P. communis) were highly resistant to decline. Blodgett et al. (1962) found no variation in the frequency and severity of decline symptoms due to scion cultivars or to origin of the scionwood. However, the variation was directly associated with the rootstock from light to severe as follows: P. communis ‘Bartlett’ followed by imported French, P. calleryana, P. ussuriensis, and P. serotina. Seemuller and Kunze (1972), who investigated pear decline in southwestern Germany, were able to experimentally transmit by grafting the decline symptoms which they suspected were responsible for the variation in rootstocks’ susceptibility. T h e most extensive pear rootstock research in relation to pear decline has been conducted in Oregon for a t least the past 50 years. Westwood et al. (1971) assessed pear plots established in 1923 and 1926 with trees composed of several rootstocks and trunk combinations for tree size and susceptibility to pear decline. In
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general, P. ussuriensis and P. pyrifolia rootstocks were dwarfing, P. communis and P. calleryana Decne. intermediate, and P. betulaefolia Bunge non-dwarfing. The latter was most resistant to decline, followed by P. calleryana and P. communis, with P. pyrifolia and P. ussuriensis being susceptible. The use of oriental hybrid cultivars ‘Variolosa’ and ‘Tolstoy’ as interstocks increased the severity of pear decline symptoms, whereas the use of P. communis cv. Old Home as scion-rooted trunkstocks decreased the degree of decline. Additional emphasis was placed on rootstock research for resistance to blight, decline, pear psylla, nematodes, etc., following severe occurrence of decline in 1956 (Westwood and Lombard 1977). In California, pear and quince rootstocks were reported to be resistant to attack by Pratylenchus vulnus (Day and Serr 1951). Fogle (1975) emphasized that dwarfing in peach is an important objective in the search for hardy, resistant, and long-lived rootstocks. For their various desirable characters, trees on Lovell rootstock have been heavily favored to control PTSL in the Southeast (Clayton 1975a,b; Correll et al. 1973; Miller and Dowler 1973; Yadava and Doud 1978a; Zehr et al. 1976). Siberian C rootstock gave best tree survival for northern conditions (Layne et al. 1976, 1977; Ormrod and Layne 1977), but tree mortality in the South, particularly on short-life sites, has been substantial on this rootstock (Yadava and Doud 1978a). Although Blake (1938) reported that lower trunk hardiness and resistance to bark injury are not always correlated with fruit bud hardiness, enhancement in bud hardiness as a result of rootstock effects has been found by several workers (Emerson et al. 1977; Layne et al. 1973,1977; Layne and Ward 1978; Winklepleck and McClintock 1939). In 1951, 14 of the 15 trees on Yunnan rootstock in Fort Valley, Georgia were injured by cold, while no trees on Lovell rootstock were affected (Weinberger 1952). The winter killing of trees on Yunnan was not confined to one cultivar alone, but all six cultivars lost some trees on this rootstock. Yadava and Doud (1978a) showed that Lovell, Halford, and NA8 rootstocks invariably imparted more cold hardiness to ‘Redhaven’ scions than other rootstocks tested, whereas maximum cold injury was sustained by trees on Siberian C and NRL4 rootstocks. Emerson et al. (1977) noted that graft incompatibility of scions on certain peach rootstocks resulted in excessive tree mortality. Nematode infestation is a weakening factor in peach orchards in most producing areas. The use of rootstocks resistant to causal nematode species offers a promising method to reduce tree losses. Zehr et al. (1976) feel strongly that tree losses are affected by rootstock as well as by nematode control. Several workers have studied peach rootstock resistance to root-knot nematode and found that S-37 and Okinawa were, in most cases, resistant to both Meloidogyne javanica and M. incognita
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(Burdett et al. 1963; Hutchins 1936; Kochba et al. 1972; Minz and Cohn 1962). Day and Serr (1951) presented evidence that Pratylenchus uuln u s was an important factor in peach decline on old sites. Peach rootstocks varied in susceptibility to this nematode, and Bokhara and Yunnan were, at least partially, resistant. The research group from Harrow, Ontario that reported Siberian C rootstock to be the most winter-hardy and otherwise desirable found that the seedlings of this rootstock were most severely affected by P. penetrans (Johnson et al. 1978). Lownsbery (1961) listed Lovell and S-37 peach rootstocks as very poor hosts for ring nematode (Macroposthonia xenoplax). Stem-pitting in peach has been reported to be a virus-induced rootstock-scion reaction which has been a severe problem in peach orchards in some parts of the United States (Cameron 1971b). Natural incidences of perennial canker (Leucostornu spp.) on ‘Dixiered’, ‘Babygold-5’, ‘Loring’, and ‘Redhaven’ peaches on Rutgers Red Leaf (RRL) and Harrow Blood rootstocks were significantly lower than on other rootstocks (Layne 1976a; Weaver 1963). Harrow Blood rootstock’s influence on promoting a lower incidence and severity of Leucostoma canker was postulated to be caused by its known effect on enhancement of stem hardiness of peach scions (Layne 1976a). Hutchinson and Bradt (1968) reported that on a clay loam soil in Vineland, Ontario ‘Golden Jubilee’, ‘Redhaven’, and ‘Veteran’ peach trees were of similar size on Elberta and Lovell seedling rootstocks, but were usually smaller on RRL seedlings. Tree losses which were greater on RRL than on the other two rootstocks were thought to be caused by incompatibility rather than cold injury or soil conditions. On the other hand, Chaplin et al. (1974) reported that, under Kentucky soil conditions, RRL seedling rootstock was most tolerant to waterlogging and Lovell was least tolerant. The rootstocks used for peach and almond have an influence on the amount of injury caused by an excess accumulation of boron in the leaves and stems (Hansen 1955). Unfortunately, almond, which is only partially satisfactory rootstock for peach, could not be recommended for use with peach even though it did reduce boron phytotoxicity. Compared to Lovell roots, the Shalil roots tended to produce somewhat higher chloride accumulation and less growth in both peach and almond scions (Bernstein et al. 1956). Westwood et al. (1973) tested 6 P r u n u s species, represented by 19 types, for their performance as rootstocks for prune ( P r u n u s domestica L.). Fewer trees on peach roots died from Pseudomonas syringae canker than did those on several clonal plum roots; however, some plum-rooted trees outgrew the canker and survived as well as trees on peach rootstock. Bacterial canker (Ps. syringae) ratings of ‘Napoleon’ and ‘Corum’ cherry and ‘Italian’ prune trees budded on various rootstocks were re-
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corded by Cameron (1971a). Under Oregon conditions, about half as many ‘Italian’ prune trees had trunk cankers when on peach seedling rootstocks as trees on plum rootstock. Infection was particularly severe on trees with P. tomentosa rootstock. On both the East and West Coasts of the United States, Mahaleb cherry rootstock was found to be more winter hardy than Mazzard (Blodgett 1976; Carrick 1920; Edgerton and Parker 195813).However, according to Carrick (1920) there is no basis for assuming that stock hardiness in cherries would directly influence hardiness of the scion. Western X-little cherry disease often results in a complete wilt and death of mature trees, and trees on Mahaleb rootstock suffer comparatively serious losses (Blodgett 1976). Cherry trees on Mahaleb rootstock in Michigan are killed suddenly in mid-summer by Xdisease, whereas trees on Mazzard rootstock decline slowly (Jones 1971b). A deep-rooting rootstock, like Mahaleb, is substantially better than shallow-rooting Mazzard for problem soils infested with Pratylenchus penetrans (Parker et al. 1966). Furthermore, a progressive decrease in tree growth on fumigated soils occurred sooner in trees on Mazzard than on Mahaleb rootstock (Mai and Parker 1967). One-year-old Mahaleb seedlings had higher mortality due to Phytophthora root rot than Mazzard seedlings within a period of three months in a soil artificially infested with Phytophthora cambivora and P. megasperma (Mircetich and Matheron 1976). Trees on Mahaleb rootstock on poorly drained soils were more severely affected with the disease than trees on Mazzard rootstock, or on well drained soils. Rootstock resistance to Thielaviopsis basicola, which is responsible for cherry decline (Pepin et al. 19751, differed significantly among various cherry clones. It was suggested that resistance to T. basicola in the P r u n u s pseudocerasus hybrids was an important asset to the potential hybrid cherry rootstocks. Bernstein et al. (1956) reported t h a t Yunnan rootstock definitely increased chloride level and hence toxicity in the apricot while Marianna rootstock effectively reduced chloride accumulation and improved plum and prune tree growth. Since almond and peach trees on almond roots suffered the least phytotoxicity due to accumulated boron, almond rootstocks were suggested only for almond trees in locations where excess boron is a problem (Hansen 1955).
C. Cultural Practices A well grown plant in good health will be better able to survive adverse conditions than a plant in marginal health. In addition, tissue maturity is necessary before a plant can develop any resistance to cold (Brierley 1947). Early development of cold resistance results from decrease in protoplasm activity before leaf fall, and in such cases fertilizer appli-
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cations reduce plants’ cold resistance (Chandler 1954). The greater susceptibility of late growth in deciduous fruit crops to winter injury gives some indication of how necessary it is to modify the cultural practices in those regions where low temperatures are encountered. Though environmental factors cannot be modified to reduce cold injury in the orchards, potential hazards can certainly be reduced by certain precautions, such as proper care taken to avoid those practices that will result in late and excessive growth and delayed hardening of trees (Rollins et al. 1962). Beattie et al. (1963) found no clear cut relationship between cultural practices and ATD in Ohio. They suspected that ATD incidence was associated with lower soil pH (Beattie 1962; Beattie et al. 1963); consequently, liming to adjust pH between 5.5 and 6.5 and to help other biological activities in the soil was recommended (Banta 1960; Parker et al. 1966). In England, however, acidification of soil was found to be effective against apple replant problem (Anon. 1966). Apple trees became more resistant to collar rot when treated with chemical fertilizers and green manure, but more susceptible when treated with animal manures (Sarasola and De Bustamante 1970). In addition, nitrogen fertilization improved the vigor of pear trees, though without considerably affecting the decline symptoms. I t also was reported that the use of windbreaks to protect apple and pear orchards from winds and to prevent abrupt changes of temperature a t sunset sharply reduced pear decline and apple collar rot. Soil moisture appears to be important to root hardiness and survival in various ways. From Nebraska, Howard (1924) reported greater apple root injury under dry soil conditions than under moist conditions. Conversely, Way (1954) observed that ‘Cortland’ apple trees that were irrigated in the fall suffered significantly greater freezing injury than non-irrigated trees. Similar trees treated with 3 to 7 Ib of ammonium nitrate suffered significantly greater cold injury than non-treated trees. H e also showed that artificial drought and fall pruning had no measurable effect on the cold injury. Burkholder (1936) suggested that when heavy pruning is to be practiced, the work should not be done until late February, because some cultivars, if fall-pruned, may be severely injured when pruning is followed by prolonged periods of sub-zero temperatures. When it becomes necessary to prune in the fall, it would seem best to work first on such varieties as ‘Rome’, ‘Delicious’, and ‘Grimes Golden’. Still another possibility would be to confine the pruning to mature trees where the pruning cuts should be relatively small and mainly in the outer surface, well removed from the crotch and lower parts of the scaffold branches. Cultural practices strongly affect cold hardiness, which in turn is associated with peach tree longevity (Nesmith and Dowler 1976). Hen-
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drix and Powell (1969) concluded th at peach growers can improve the chances of tree survival by modifying cultural practices. Cultural practices that delay hardening in the fall tend to prolong dormancy period in spring (Proebsting 1970). Avoidance of those practices that leave peach trees susceptible to cold injury will also lessen the chances of severe damage by bacterial canker (Petersen 1975). Oh and Carlson (1976) suggested prompt disposal of plant parts as a practical sanitation practice to possibly reduce PTSL in old soils. Smith and Stouffer (1975) suggested prompt roguing of diseased plants, no replanting in old orchards, effective weed control, and thorough tillage before planting a s practical points to be considered for an effective measure against infection and spread of Prunus stem pitting. T h e spread of peach rosette and decline disease in Victoria, Australia was reduced by almost 33'k over a 2-year period by grubbing all affected trees before flowering (Smith et al. 1977a). Savage (1970) showed th a t insulation of trunk and scaffolds immediately above the crotch would prevent cold injury under most circumstances. He suggested that, if any easily applied economical insulation were available, the tree losses could be greatly reduced. Metal chelates have been found to be beneficial in overcoming arsenic toxicity of peach trees (Batzer and Benson 1958). I t was suggested th a t zinc chelate was most economic in correcting arsenic toxicity without any adverse effects. Various kinds of cover crops and mulches have been recommended to initially benefit replants and to reduce soil population of certain nematodes in established orchards (McBeth and Taylor 1944; Shannon and Christ 1954). Hendrix and Powell (1969,1970a) cautioned t ha t if PTSL is to be controlled, the first step in any such program should be to avoid injury and destruction of roots by discing. However, preplant subsoiling has been strongly recommended for the southeastern United States (Miller and Dowler 1973; Savage et al. 1968). T h e latter workers reported t ha t under Georgia peach soils, where oxygen levels were 15% or less during a great part of the growing season, preplant subsoiling to a depth of 50 cm had nearly doubled the growth and yield of peach trees and greatly increased tree longevity. The improved performance and increased longevity were accomplished even though soil moisture was decreased in the subsoiled plots. Under adequate soil moisture supply, even moderately injured trees lived and maintained productive lives (Cowart and Savage 1941). Aeration of anaerobic soils reverses cyanogenesis in the peach roots (Mizutani et al. 1977) and could be used to control peach replant problems. Georgia scientists have claimed th at on short-life sites peach yields can be maintained and tree survival extended by following good liming and nitrogen fertilization practices prior to planting (Giddens et al. 1972; Spivey and McGlohon 1973; Taylor 1972). T h e PTSL research efforts,
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conveyed through a 10 point program, have very strongly recommended preplant liming to aid in reducing tree losses (Miller and Dowler 1973).In addition to raising the soil pH, lime also increases leaf Ca and Mg contents (Havis 1962), and greatly reduces leaf abnormalities arising from Ca and Mg deficiencies (McClung 1953). Dolomitic and high-Mg limes have proved to be beneficial and caused even greater growth improvements than in the non-short-life sites in some cases (Giddens et al. 1972; Havis 1962; Prince et al. 1955). Nesmith and Dowler (1976) reported t ha t nitrogen applied alone or in combination with fumigation reduced cold hardiness of peach in early winter, but nevertheless increased vigor and survival. This would mean th a t any practice serving to increase the level of soluble nitrogen in peach tissues during the dormant season might lower the resistance of these tissues to freezing (Waltman 1937). McCue (1915) ascertained th at the fertilizer which was so balanced to produce the most healthy growth also would promote the strongest wood, with considerable hardiness in the peach tree. Higgins et al. (1943) reported th at fall nitrogen application increased the wood hardiness of peach trees. Waltman (1937) explained the usefulness of fall application of nitrogen. Since root activity during the winter is relatively slow, it would appear th at harmful effects from using calcium cyanamide (CaCNJ fertilizer are not likely to occur, and th a t trees fall fertilized with CaCNz possibly may be less subject to winter injury because of the lowered level of soluble nitrogen in tissues. Application of nitrogen has been reported to induce iron chlorosis in peach trees grown on calcareous soils (Dekock and Wallace 1965). Similarly, Davidson and Blake (1937) warned against those practices involving heavy applications of single fertilizer materials on,light sandy soils which are low in organic matter. They emphasized th at the significance of nutrient balance must be recognized, particularly when dealing with such soils. They recommended the regular use of complete balanced fertilizers, together with frequent liming in orchards on these soils. Studies reported by Raw1 (1935) also disapproved the use of nitrogen alone a s a fertilizer, and strongly suggested th at application of other plant nutrients is equally essential. However, nitrogen fertilization a t rates sufficiently high to maintain vigorous growth of peach trees was reported by Higgins et al. (1943) to increase their cold hardiness, and hence reduce tree injury. Similarly, supplemental nitrogen fertilization significantly improved tree survival and yield of ‘Elberta’ peach trees grown on a severe shortlife site (Giddens et al. 1972). Hewetson (1953) studied the feasibility of liquid fertilizer in replant peach orchards in Pennsylvania. This report showed t ha t the liquid fertilizer employed had the capacity to produce strong, vigorous peach trees superior to those produced with either ma-
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nure or 1O:lO:lO fertilizer. The theory was th a t if replant trees could be made to grow vigorously during their first year in the orchard, they might be expected to continue satisfactorily in subsequent years. Four years later (Hewetson 19571, it was concluded th a t the readily available source of nitrogen gave the trees a rapid early start which quickly established the trees, perhaps in turn helping replants to overcome any inhibiting effect of the trees previously grown in these locations. McCue (1915) believed th at greater differences in peach wood strength could be obtained by different pruning methods than by fertilizer treatments. Stene (1937) reviewed the literature on pruning peach in relation to winter injury. His conclusion varied from no pruning until after defoliation to relatively severe pruning a t the usual time depending on the condition of late growth. Th e preponderance of opinion among present peach researchers favors very light to no pruning a t all until just before foliation time. Fall pruning is potentially a damaging practice which significantly contributes to PTSL (Clayton 1968; Correll et al. 1973; Nesmith and Dowler 1973,1975; Prince and Horton 1972; Weaver et al. 1974), and late winter pruning in February-March has been found to be beneficial to increase tree survival (Clayton 1975a, 1977; Correll et al. 1973; Miller and Dowler 1973).Luepschen and Rohrbach (1969) reported less likelihood of Cytospora canker infection on peach trees under Colorado conditions with pruning delayed until spring. However, Weaver et al. (1974) reported th at in middle Georgia peach trees grown on a n old site were killed by cold injury and bacterial canker, but the trees’ death was not influenced by time of pruning. On a n adjacent new site, early pruning caused susceptibility to cold, showing th a t early pruning is also a predisposing factor to cold and bacterial canker injuries. However, once these problems have set in, the pruning time has no bearing on death or survival of trees. Daniel1 (1973) reported th a t trees growing on old peach site and pruned in fall or early winter had greater mortality than nonpruned or those pruned in spring. Time of pruning, on the other hand, has little or practically no adverse effect on tree longevity when grown on new site. He found no consistent effect of pruning on tree growth.
D. Control of Pathogens Effective control of causal pathogens by chemical means has been very important in helping, a t least partially, alleviate some short-life-related problems. T he specific reasons for the success or failure of different soil treatments used to control SARD are not known, but appear to be related to their efficiency in destroying a wide range of microbial species, presumably the causal organisms (Savory 1966). Steaming soil a t 50°C for one hour reduced bacterial population to about 17% and benefited apple
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replants a t problem sites in Germany (Otto 1972c,d). Pseudomonas syringae infection on apple, pear, cherry, and plum has been satisfactorily controlled by wound treatments with “Santar M” paste and 3 subsequent treatments with 0.2‘,( benomyl or quinolin-fundazol a t budding, early petal fall, and after harvest (Dorozhkin and Griogortsevich 1976).Petersen (1975) reported th at no satisfactory chemical control was known for Ps. syringae canker of peach. The systemic existence of this microorganism explains the lack of effective control from protective bactericides applied to cherry tree surfaces (Cameron 1970). Such approaches as nematicide applications and fumigation with DD in the declining peach orchards in California reduced or completely controlled trees’ death due to bacterial canker (De Vay et al. 1968; English 1961; English et al. 1961). In field trials, copper compounds were only slightly effective against €?seudomonaa mors-prunorum f. sp. persicae, but autumn applications of oxytetracycline and kanamycin a t 1000 ppm each gave good control of the pathogen on peach trees and considerably reduced infection the following spring (Prunier et al. 197313). However, combined applications of copper compounds and antibiotic showed no further improvement over th at of either chemical alone. Very few fungi survived in soils which were fumigated with chloropicrin-methyl bromide (1:l mixture) applied a t 440 kg/ha a n d covered with polyethylene sheeting; but without polyethylene sheets some fungi did survive, especially a t or near the soil surface (Warcup 1976). Wensley (1956) reported similar results from peach replant studies in Ontario. Steaming a t 50°C for one hour almost eliminated microscopic fungi and reduced actinomycetes to 61% (Otto 1972c,d). At 60°C actinomycetes were reduced to 16%, and very few survived a t 70°C. Actinomycetes’ decreasing tolerance to increasing temperatures gave corresponding control of replant diseases (Otto 1972d). De Vay et al. (1967) and Hendrix and Powell (1970a) reported control of peach decline which was associated with reduced soil population of P y t h i u m spp. Of the several test chemicals which demonstrated systemic activity in one or more tests for control of Cytospora cincta invasion of peach trees, Na 2-pyridinethiol, 1-oxide and cycloheximide thiosemicarbazone were outstanding (Helton and Rohrbach 1967).Th e preventive effects were more pronounced than curative effects in all cases. Complete prevention of Cytospora cankers was achieved with cycloheximide thiosemicarbazone, whereas Na 2-pyridinethiol, 1-oxide promoted best healing of infection wounds. Both of these compounds demonstrated curative activity against established canker infections. Chandler (1969) reported th a t a t the Georgia Experiment Station preplant soil fumigation in peach orchards where the original planting was heavily infested with Clitocybe root rot resulted in significantly better tree growth for three years due to control of the fungus.
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Nematodes have not been associated often with short life and replant problems of pome fruits and, therefore, no specific literature is available concerning their control. Nematode control and elimination of reservoirs of infection are crucial to the effective control of PTSL, however (Scotto La Massese et al. 1973).Soil fumigation and nematicide application have been found to be effective against various nematode species in stone fruits (Barker and Clayton 1969, 1973; Chandler 1969; Foster 1960; Foster et al. 1965; Good 1960; Hendrix and Powell 1969; Hung and Jenkins 1969; Mountain and Boyce 1957, 1958b; Nesmith and Dowler 1975; Shannon and Christ 1954; Wehunt and Good 1975; Zehr et al. 1976). The growth and survival of peach trees have been substantially improved by effective nematode control. In New York cherry orchards, control of nematodes by soil fumigation caused increased cold hardiness and tree survival while all trees on non-fumigated soil were dead by the end of the third year (Edgerton and Parker 1958a; Mai and Parker 1967). Nyland and Moller (1973) chemically controlled pear decline using a tetracycline. Of the three basic effects of pear decline, viz., tree collapse, tree decline, and leaf curl, the latter two were prevented by transfusing a solution of oxytetracycline hydrochloride into affected trees. Six to eight quarts of a 100 ppm solution per tree given soon after harvest prevented leaf curl in autumn of the current season and greatly stimulated shoot and spur growth the following season. Two to three annual treatments in the autumn restored previously severely declined trees to a normal or near-normal condition. These tests, involving 75 growers and about 2,000 diseased pear trees, showed that such treatment is feasible. This chemical also inhibited peach rosette symptoms four to five times more effectively than other compounds (Kirkpatrick et al. 1975a). In this case, remission occurred when the chemicals were injected under the bark or into the wood, but not when sprayed on the foliage. The same chemical also has been used as injections in October via previously drilled holes beneath each scaffold limb to effectively control peach X-disease (Sands and Walton 1975). Following injection, the peach X-disease symptoms do not appear in early summer as they do on untreated trees. Treated trees, although still weak from X-disease of the previous year, produce more foliage and fruit, with continued improvement.
E. Miscellaneous Controls Soil sterilization by fumigation or steaming controls several soil-borne problems of fruit crops indirectly by eliminating a wide range of microbial species and nematodes (Bollard 1956; Hendrix and Powell 1969; Otto 1972c,d; Prince et al. 1955; Savory 1966; Warcup 1976; Winkler and Otto 1972; Youngson et al. 1967). Generally, pre-plant fumigation
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is more effective or desirable than post-plant treatments (Hendrix and Powell 1969; Lownsbery et al. 1968; McBeth 1954). McBeth (1954) suggested that the non-phytotoxicity and effectiveness of the fumigant should be given a high practical priority while choosing from various fumigants. Fumigation with methyl bromide (MB) has been reported to increase the effectiveness of liming (Havis 1962), but not to modify the depressing effect of soil toxins on the growth of peach replants which gradually diminishes with the passage of time (Wensley 1956). Ladd et al. (1976) and Beams and Butterfield (1944) have reported a differential decrease in soil enzyme activity and a corresponding increase in the amounts of ninhydrin-reactive chemicals extractable with acidified “Tris” buffer. Fumigation with M B has little effect, if any, on the rate of transpiration; however, since M B is heavier than air, it may cause some wilting by reducing O2 content of the soil by approximately 80% (Beams and Butterfield 1944). Dibromochloropropane (DBCP), a soil fumigant nematicide, is reported to be strongly absorbed by wet organic matter but not by wet clay. Therefore, when DBCP is applied with irrigation water, the depth of nematode control decreases with increasing soil organic matter (Youngson et al. 1967). Further, fumigation does not change the level of any nutrient from a deficiency to a sufficiency status (Aldrich and Martin 1952). 1. Fumigation.-For apple replant diseases, chloropicrin as a fumigant has been found to be a satisfactory control whether the problem is caused by nematodes (Colbran 1953), by microbial organisms (Savory 1967), or by causes still unknown (Hoestra 1967). Chloropicrin obviously eliminates the factor responsible for growth inhibition and tree loss, but it is dangerous, expensive, and unpleasant to handle (Anon. 1966). Several other workers found chloropicrin to be the best pre-plant fumigant for apples in different countries (Jackson 1973; Ross and Crowe 1973, 1976; Ryan 1975a,b; Savory 1966). However, Pitcher et al. (1966) found it more effective for cherries than for apple replants, but i t still proved to be better than other fumigants, including DD and MB. Soil fumigation with either M B or chloropicrin overcomes both non-specific apple replant disease and SARD in Washington state (Benson 1974b; Benson and Covey 1976; Benson et al. 1978). In greenhouse studies in a soil without the arsenic toxic factor, M B fumigation resulted in better growth of apple seedlings, however. For apple, fumigants which release methyl isothiocyanate are rarely of any benefit, nor usually are bromine compounds, although M B and DBCP are sometimes successful (Savory 1966). Pre- and post-plant fumigants play a crucial part in the control of PTSL (Clayton 1968, 1975a,b; English and De Vay 1964; Miller and Dowler 1973), by increasing tree survival (Correll et al. 1973; Nesmith
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and Dowler 1975) and alleviating severe tree losses on problem sites (English 1961; Johnson 1965; Nesmith and Dowler 1973). None of the nine soil fumigants, including M B and DD tested by Hayden et al. (1968), significantly increased peach tree survival, however. Soil fumigation also has been reported to substantially improve peach tree growth, vigor, and cold hardiness (Havis et al. 1958; Nesmith and Dowler 1973, 1975; Prince et al. 1955; Shannon and Christ 1954). Pre-plant soil fumigation reflected a lower index of root-knot nematode, and hence rapid tree growth in initial years (Foster 1960; Foster and Cohoon 1958; Foster et al. 1965,1972; Good 1960). Other nematode specieslike Pratylenchus (De Vay et al. 1967; Mountain and Boyce 1957), Macroposthonia (De Vay et al. 1967; Zehr et al. 1976), and Xiphinema and other nematode vectors of stem pitting virus (Smith and Stouffer 1975) also have been successfully controlled by soil fumigation. However, reports are conflicting concerning effects of fumigation on tree decline or death caused by bacterial canker and/or cold injury (De Vay et al. 1967; Zehr et al. 1976). Soil fumigation also inhibits several fungi in the rhizosphere of the peach replants (Wensley 1956), and improves tree stand on soils heavily infested with Clitocybe (Chandler 1969) and P y t h i u m (De Vay et al. 1967; Hendrix and Powell 1970a) by reducing the population of these fungal species in the soil. In the case of cherry, soil fumigation with chloropicrin proved to be outstanding on old cherry sites (Benson 1974b; Pitcher et al. 1966),but when cherry followed apple it was not so effective (Benson 1974b; Jackson 1973). In New York, sour cherry performed extremely well on old sites which were fumigated with DD (Mai and Parker 1967), while all trees on untreated sites were dead by the end of the third year. The fumigation controlled Pratylenchus penetrans nematode in these cherry plantings and resulted in increased cold hardiness and survival of ‘Montmorency’ cherry (Edgerton and Parker 1958a). For rate of survival, plum trees have been reported to respond better to fumigation with ethylene dibromide than other fumigants (Johnson 1965). 2. Steam Sterilization.-Steam sterilization of soil a t temperatures from 50” to 70°C considerably improved shoot growth of apple seedlings, leading to a complete soil recovery from pathogenic infestation (Otto 1972c, d). Steam sterilization of old soil in pot experiments in New Zealand permitted as much growth of apple on Northern Spy rootstock as in fresh soil, while normal growth on M 12 rootstock on decline soil was further improved following steaming (Bollard 1956). Winkler and Otto (1972) concluded that a higher temperature was necessary to eliminate apple replant problem than to inactivate most nematodes. Prince e t al. (1955) recognized the importance of steaming and fumigation to obtaining greater growth of peach trees in old peach soil; however, much of the
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response they obtained was not well understood. They suggested that results of this kind may not be applicable to all soil types. Hot-waterbath treatment of whole trees showed that thermal death time of peach rosette virus was less than one hour a t 4 5 T , about 18 minutes a t 50“C, and only 2 minutes a t 55°C (KenKnight 1958). 3. Other Methods.-Ketchie and Murren (1972,1976)used cryoprotectants (PVP, glycerol, ethylene glycol, and DMSO) as spray applications, individually or in combination with each other, on whole apple trees in the greenhouse and by terminal feeding to apple and pear trees in the field. In this study, excised apple bark was soaked in cryoprotectant. Freeze protection was tested by artificial as well as natural freezing. The cryoprotectant applications increased both cold hardiness and survival of test plants; however, cultivar variation was experienced. Effects of white latex paint on temperature differences between north and south sides of apple and peach tree trunks have been studied (Eggert 1944; Martsolf et al. 1975). The unpainted trunks showed a difference of 28” to 44°C between north and south sides, while the differences in painted trunks did not exceed 6°C. This kind of amelioration would certainly reduce trunk injury due to cold. Similarly, Bennett (1950) emphasized the beneficial effect of winter shade in lowering cold injury in pear.
V. CONCLUSION
A comprehensive review of the literature clearly reveals that short life and replant problems are seldom of a simple nature, but usually are established through the interaction of several environmental, pathogenic, and/or physiological factors. Control of any one factor does not necessarily overcome the problem, although i t may be an important prerequisite to subsequent effective treatments. In many cases, diagnosis, identification of causal factors, and agreement on nomenclature have proved to be as difficult as actual treatment of the specific problem. Successful alleviation of some problems provides a basis for continued progress. In general, it can be concluded that short life and replant problems reduce expected tree longevity, are not purely pathological in nature, and are usually related to repeated plantings of the same crop on a given site. Problems may be “specific,” involving the same species in succeeding plantings with no obvious causal organism, or “non-specific,” affecting related fruit tree species in the presence of certain causal organisms. Most deciduous fruit trees are affected on a worldwide basis, although the severity, form, symptoms, and time of occurrence may vary. Due to variation in problem severity from year to year and lack of precise data, it is difficult to place a monetary figure on the losses suffered by the fruit
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industry. It also is probable t h a t a number of short life problems remain undiagnosed or mistaken for other similar disorders. Past successes in methodology development, identification of causal factors, and implementation of control measures must be followed by continued progress in many areas. In most cases, it is no longer feasible t o plant new orchards on virgin sites or t o tolerate low tree populations and inefficient management. Therefore, plant improvement through breeding, selection a n d physiological amelioration, along with effective cultural practices a n d pathogen controls, will become increasingly essential to t h e future fruit industry.
VI. LITERATURE CITED ABIKO, K. and H. KITAJIMA. 1970. Blister canker, a new disease of peach tree. Ann. Phytopathol. SOC.Japan 36:260-265. AGRIOS, G.N. 1971. Premature foliation, cambial zone discoloration, and stem pitting of peach and apricot in Greece. Plant Dis. Rptr. 55:1049-1053. AGRIOS, G.N. 1972. A decline disease of pear in Greece: Pear decline or graft incompatibility? Phytopathol. Mediter. 11:87-90. ALDEN, J. and R.K. HERMANN. 1971. Aspects of cold hardiness mechanism in plants. Bot. Rev. 37:37-142. ALDRICH, D.G. and J.P. MARTIN. 1952. Effect of fumigation on some chemical properties of soils. Soil Sci. 73:149-159. ALLEN, P.J. 1953. Toxins and tissue respiration. Phytopathology 43:221228. ANON. 1966. Replant problem. Na tu re 211:1334-1335. ANON. 1971. Plant pathology. Calif Pear Res., p. 17-20. BABOS, K., Z.D. ROZSNYAY, and Z. KLEMENT. 1976. Apoplexy of apricots. V. Pathological and histological investigations of the apoplexy of apricots. Acta Phytopathol., Acad. Sci. Hung. 11:71-79. BACHELARD, E.P. and F. WIGHTMAN. 1973. Biochemical and physiological studies on dormancy release in tree buds. I. Changes in degree of dormancy, respiratory capacity, and major cell constituents in overwintering vegetative buds of Populus balsamifera. Can. J. Bot. 51:2315-2326. BACKMAN, P.A., J.E. DEVAY, and D. PENNER. 1969. Physiological activity of the toxin syringomycin, produced by isolate of Pseudomonas syringae pathogenic on P r u n u s persica. Phytopathology 59:1016 (Abstr.). BANKO, T.J. and A.W. HELTON. 1974. Cytospora-induced changes in stems of P r u n u s persica. Phytopathology 642399-901. BANTA, E.S. 1960. Apple orchard decline. Proc. Ohio S t a t e Hort. SOC. 113:88-90. BARKER, K.R. and C.N. CLAYTON. 1969. Relative host suitability of peach cultures to six species of lesion nematodes. Phytopathology 59:1017 (Abstr.).
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BARKER, K.R. and C.N. CLAYTON. 1973. Nematodes attacking cultivars of peach in North Carolina. J Nematol. 5:265-271. BATZER, L.P. and N.R. BENSON. 1958. Effect of metal chelates in overcoming arsenic toxicity in peach trees. Proc. Amer. SOC. Hort. Sci. 72:74-78. BATZER, L.P. and H. SCHNEIDER. 1960. Relation of pear decline to rootstock and sieve-tube necrosis. Proc. Amer. SOC. Hort. Sci. 76:85-97. BEAMS, G.H. and N.W. BUTTERFIELD. 1944. Some physiological effects of methyl bromide upon horticultural plants. Proc. Amer. SOC. Hort. Sci. 45:318-322. BEATTIE, D.J. and H.L. FLINT. 1973. Effect of K level on frost hardiness of stems of Forsythia. J Amer. SOC. Hort. Sci. 98:539-541. BEATTIE, J.M. 1962. An evaluation of the apple decline problem. Proc. Ohio State Hort. SOC.115:139-144. BEATTIE, J.M., C.W. DONOHO, JR., E.S. BANTA, and F. QUINN. 1963. Horticultural aspects of the apple decline problem. Proc. Ohio State Hort. SOC.116:83-91. BELL, H.K. and N.F. CHILDERS. 1956. Effect of manganese and soil culture on the growth and yield of the peach. Proc. Amer. SOC. Hort. Sci. 67:130-138. BENNETT, J.P. 1950. Temperature and bud rest period. Effect of temperature and exposure on the rest period of deciduous plant leaf buds investigated. Calif. Agr. 4:ll-16. BENSON, N.R. 1974a. Apple replant problem in Washington State-Effect of soil arsenate. HortScience 9290 (Abstr.). BENSON, N.R. 1974b. Apple replant problem in Washington State-Effect of soil fumigation. HortScience 9:290 (Abstr.). BENSON, N.R. and R.P. COVEY, JR. 1976. Specific apple replant disease (SARD) in Washington State. HortScience 11:331 (Abstr.). BENSON, N.R., R.P. COVEY, JR., and W. HAGLUND. 1978. The apple replant problem in Washington State. J. Amer. SOC. Hort. Sci. 103:156-158. BERGMAN, H.F. 1959. Oxygen deficiency as a cause of disease in plants. Bot. Rev. 25:417-485. BERNSTEIN, L., J.W. BROWN, and H.E. HAYWARD. 1956. The influence of rootstock on growth and salt accumulation in stonefruit trees and almonds. Proc. Amer. SOC. Hort. Sci. 68236-95. BIESBROCK, J.A. and F.F. HENDRIX, JR. 1970. Influence of soil water and temperature on root necrosis of peach caused by Pythium spp. Phytopathology 60:880-882. BIRD, G.W. 1968. Orchard replant problems. Can. Dept. Agr. Publ. 1375. BLAKE, M.A. 1928. Some serious weak points in field nutrition studies with Hort. Sci. 25:350-353. peaches. Proc. Amer. SOC. BLAKE, M.A. 1935. Types of varietal hardiness in the peach. Proc. Amer. SOC. Hort. Sci. 33:240-244.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
87
BLAKE, M.A. 1938. Hardy rootstocks for the peach should extend well above the surface of the soil. Proc. Amer. SOC. Hort. Sci. 36:138-140. BLATTNY, C. and V. VANA. 1974. Pear decline accompanied with mycoplasma-like organisms in Czechoslovakia. Biol. Plant. 16:474-475. BLODGETT, E.C. 1976. Why cherry trees die. Wash. State Uniu., Coop. Ext. Seru., Pullman. Ext. Bul. 668. BLODGETT, E.C., H. SCHNEIDER, and M.D. AICHELE. 1962. Behavior of pear decline on different stock-scion combinations. Phytopathology 52: 679-684. BLOMMAERT, K.L.J. 1955. The significance of auxins and growth-inhibiting substances in relation to winter dormancy of the peach tree. W. P. Fruit Res. Sta., Stellenbosch, Union of South Africa Sci. Bul. 368. BLOMMAERT, K.L.J. 1959. Winter temp in relation to dormancy and the auxin and growth-inhibitor content in peach buds. South African J. Agr. Sci. 2:507-514. BOLLARD, E.G. 1956. Effect of steam-sterilized soil on growth of replant apple trees. New Zealand J. Sci. Technol. 38:412-415. BORNER, H. 1959. The apple replant problem. I. The excretion of phlorizin from apple root residues. Contrib. Boyce Thompson Inst. P l a n t Res. 20:39-56. BORZAKOVSKA, I.V., I.M. SHAITAN, N.P. LEVCHENKO, and T.P. T E RESHCHENKO. 1975. Biochemical aspects of the rootstock effect on graft in relation to winter hardiness of the apple trees (English translation). Ukr. Bot. Zh. 32:708-716. BOTTINI, R., G.A. DE BOTTINI, and N.S. CORREA. 1976. Changes in the levels of growth inhibitors and GA-like substances during dormancy of peach flower buds. 11. Phyton 34:157-167. BOWEN, H.H. 1971. Breeding peaches for warm climates. HortScience 6: 153-157. BOYNTON, D. and L.C. ANDERSON. 1956. Some effects of mulching, N fertilization, and liming on McIntosh apple trees, and the soil under them. Proc. Amer. SOC. Hort. Sci. 67:26-36. BRIERLEY, W.G. 1947. Winter hardiness complex in deciduous woody plants. Proc. Amer. SOC. Hort. Sci. 5O:lO-16. BROWN, D.S. 1943. A report of injury by cold weather to peach trees in Illinois during the winter of 1941 and 1942. Proc. Amer. SOC. Hort. Sci. 42:298-300. BROWN, D.S. and F.A. KOTOB. 1957. Growth of flower buds of apricot, peach, and pear during the rest period. Proc. Amer. SOC. Hort. Sci. 69:158164. BROWN, G.N. and J.A. BIXBY. 1975. Soluble and insoluble protein patterns during induction of freezing tolerance in black locust seedlings. Physiol. Plant. 34:539-541.
88
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BUNEMANN, G. and A.M. JENSEN. 1970. Replant problem in quartz sand. HortScience 5:478-479. BURDETT, J.F., A.F. BIRD, and J.M. FISHER. 1963. The growth of Meloidogyne in Prunus persica. Nematologica 9:542-546. BURKE, M.J., L.V. GUSTA, H.A. QUAMME, C.J. WEISER, and P.H. LI. 1976. Freezing and injury in plants. Ann. Rev. Plant Physiol. 27:507-528. BURKHOLDER, C.L. 1936. December pruning in 1935 results in severe injury to Jonathan and Stayman trees at Lafayette, Indiana. Proc. Amer. SOC. Hort. Sci. 34:49-51. CAIN, J.C. and R.J. MEHLENBACHER. 1956. Effect of nitrogen and pruning on trunk growth in peaches. Proc. Amer. SOC. Hort. Sci. 67:139-143. CAMERON, H.R. 1962. Diseases of deciduous fruit trees incited by Pseudomonas syringae van Hall. A review of the literature with additional dates. Oreg. Agr. Expt. Sta. Tech. Bul. 66. CAMERON, H.R. 1970. Pseudomonas content of cherry trees. Phytopathology 60 :134 3 - 1346. CAMERON, H.R. 1971a. Effect of root or trunk stock on susceptibility of orchard trees to Pseudomonas syringae. Plant Dis. Rptr. 55:421-423. CAMERON, H.R. 1971b. Effect of viruses on deciduous fruit trees. HortScience 12:484-487. CAMPBELL, A.I. 1971. A comparison of the growth of young apple trees on virus-infected and healthy rootstocks. J. Hort. Sci. 46:13-16. CAMPBELL, R.W. 1948. More than thirty peach varieties survived minus thirty-two degrees Fahrenheit. Proc. Amer. SOC. Hort. Sci. 52:117-120. CAMPBELL, R.W. and F.B. HADLE. 1960. Winter injury to peaches and grapes. Proc. Amer. SOC. Hort. Sci. 76:332-337. CANCINO, L., B. LATORRE, and W. LARACH. 1974. Pear blast in Chile. Plant Dis. Rptr. 581568-570. CARLSON, R.F. 1975. Improved rootstocks for peaches. p. 62-66. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. CARRICK, D.B. 1920. Resistance of roots of some fruit species to low temp. Cornell Uniu., Agr. Expt. Sta. Mem. 36:609-661. CARTER, G.E., JR. 1976. Effect of soil fumigation and pruning date on the IAA content of peach trees in a short-life site. HortScience 11:594-595. CHANDLER, L.H. 1954. Cold resistance in horticultural plants: A review. Proc. Amer. SOC. Hort. Sci. 64:552-572. CHANDLER, W.A. 1969. Reduction in mortality of peach trees following preplant soil fumigation. Plant Dis. Rptr. 53:49-53. CHANDLER, W.A. 1974. Post-pruning sprays not effective in control of peach tree decline. Plant Dis. Rptr. 58:388-391. CHANDLER, W.A. and J.W. DANIELL. 1974. Effect of leachates from peach soil and roots on bacterial canker and growth of peach seedlings. Phytopa thology 64 :1 2 81- 1 284.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
89
CHANDLER, W.A. and J.W. DANIELL. 1976. Relation of pruning time and inoculation with Pseudomonas syringae van Hall to short life of peach trees growing on old peach land. HortScience 11:103-104. CHANDLER, W.A., J.H. OWEN, and R.L. LIVINGSTON. 1962. Sudden decline of peach trees in Georgia. Plant Dis. Rptr. 46:831-834. CHANDLER, W.H. and W.P. TUFTS. 1933. Influence of the rest period on opening of buds of fruit trees in spring and on development of flower buds of peach trees. Proc. Amer. SOC. Hort. Sci. 30:180-186. CHAPLIN, C.E. and G.W. SCHNEIDER. 1974. Peach rootstock/scion hardiness effects. J Amer. SOC. Hort. Sci. 99:231-234. CHAPLIN, C.E., G.W. SCHNEIDER, and D.C. MARTIN. 1974. Rootstock effect on peach tree survival on a poorly drained soil. HortScience 9:28-29. CHIRILEI, H., I. MOLEA, and I. IORGULESCU. 1970. Gummosis-one of the causes of premature decline of the apricot tree (English translation). Physiol. Plant. Rom. 1970, p. 139-148. CHITWOOD, B.G. 1949. Ring nematodes (Criconematinae) a possible factor in decline and replanting problems of peach orchards. Proc. Helminthol. SOC. Wash. D.C. 16:6-7. CHITWOOD, B.G., A.W. SPECHT, and L. HAVIS. 1952. Root-knot nematodes. 111. Effects of Meloidogyne incognita and M. jauanica on some peach rootstocks. Plant & Soil 4:77-95. CLAYTON, C.N. 1968. Peach canker, decline, and related problems (unpublished). CLAYTON, C.N. 1971. The perennial (ValsalCytospora) canker complex. Proc. Natl. Peach Counc. 30th Annu. Conu., p. 33-34. CLAYTON, C.N. 1972. Peach decline, hardiness, stocks, early fall vs. winter pruning. Natl. Peach Counc. Proc. 31:116-117. CLAYTON, C.N. 1975a. Peach replant problem. p. 139-145. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. CLAYTON, C.N. 1975b. Peach tree short life, hardiness, stocks, early fall vs. winter pruning. p. 244-245. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. CLAYTON, C.N. 1977. Peach tree survival. Fruit South 1:53-58. COCHRAN, L.C. 1975. Viruses. p. 363-366. Zn N. F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. COHEN, M. 1963. Infection of lychee and peach seedlings with cultures of Clitocybe tabescens. Phytopathology 53:358-359. COLBRAN, R.C. 1953. Problems in tree replacement. I. The root-lesion nematode Pratylenchus coffeae Zimmerman as a factor in the growth of replant trees in apple orchards. Austral. J. Agr. Res. 4:384-389. CONNERS, C.H. 1922. Peach breeding-a summary of results. Proc. Amer. SOC. Hort. Sci. 19:108-115.
90
HORTICULTURAL REVIEWS
CORRELL, F.E., C.N. CLAYTON, and G.A. CUMMINGS. 1973. Peach tree survival as influenced by stock, soil fumigation, time of pruning, and nitrogen level. HortScience 8:26 (Abstr.). COUVILLON, G.A., S. BASS, B.W. JOSLIN, R.E. ODOM, J.E. ROBERSON, D. SHEPPARD, and R. TANNER. 1977. NAA-induced sprout control and gummosis in peach. HortScience 12:123-124. COWART, F.F. and E.F. SAVAGE. 1941. Important factors affecting peach tree longevity in Georgia. Proc. Amer. SOC. Hort. Sci. 39:173-176. CRAKER, L.E., L.V. GUSTA, and C.J. WEISER. 1969. Soluble proteins and cold hardiness of two woody species. Can. J . Plant Sci. 49:279-286. CROSSE, J.E. 1966. Epidemiological relations of the Pseudomonas pathogens of deciduous fruit trees. Annu. Rev. Phytopathol. 4:291-310. CROSSE, J.E. and C.M.E. GARRETT. 1966. Bacterial canker of stone fruits. VII. Infection experiments with Pseudomonas mors-prunorum and P. syringae. Ann. Appl. Biol. 58:31-41. CULLINAN, F.P. and J.H. WEINBERGER. 1934. Studies on the resistance of peach buds to injury at low temp. Proc. Amer. SOC.Hort. Sci. 32:244-251. CUMMINGS, G.A. and W.E. BALLINGER. 1972. Influence of longtime nitrogen, pruning, and irrigation treatments upon yield, growth, and longevity of ‘Elberta’ and ‘Redhaven’ peach trees. HortScience 7:133-134. CUMMINS, J.N. 1977. Objectives of apple rootstock breeding projects and the needs of the North American industry. Compact Fruit Tree 10:13-16. CUMMINS, J.N. and H.S. ALDWINKLE. 1974a. Apple rootstocks for colder climates. Fruit Var. J . 28:9-11. CUMMINS, J.N. and H.S. ALDWINKLE. 1974b. Breeding apple rootstocks. HortScience 9:367-372. CUMMINS, J.N. and H.S. ALDWINKLE. 1974c. Broadening the spectrum of rootstock breeding. Proc. 19th Intern. Hort. Congr., Warsaw. Sept. 10-18. Wroclawska, Drukarnia Naukowa, Warsaw. p. 303-312. CUMMINS, J.N. and P.L. FORSLINE. 1977. Multiple-stock apple trees. Trans. Ill. State Hort. SOC.110:45-56. DANIELL, J.W. 1973. Effect of time of pruning on growth and longevity of peach trees. J. Amer. Soc. Hort. Sci. 98:383-386. DANIELL, J.W. 1975. Effect of time of pruning or non-pruning on fruit set and yield of peach trees growing on new or old peach sites. J. Amer. SOC. Hort. Sci. 100:490-492. DANIELL, J.W. 1977. Peach short life. p. 47-73. In H. M. Vines (ed.) Physiology of root-microorganisms associations. Proc. Symp. Southern Sec. Amer. SOC.Plant Physiol. Feb. 8, 1977. Atlanta, Ga. DANIELL, J.W. and W.A. CHANDLER. 1974. Effect of temperature on bacterial canker in peach seedling growth in old and new peach soil. Phytopathology 64:1284-1286. DANIELL, J.W. and W.A. CHANDLER. 1976. Effect of iron on growth and bacterial canker susceptibility of peach seedlings. HortScience 11:402-403.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
91
DANIELL, J.W. and F.L. CROSBY. 1968. Occlusion of xylem elements in Hort. Sci. 93:128peach trees resulting from cold injury. Proc. Amer. SOC. 134. DANIELL, J.W. and F.L. CROSBY. 1970. Effect of cold injury on peach trees. Peach tree decline in Georgia. Ga. Agr. Expt. Sta. Res. Bul. 77:35-41. DANIELL, J.W. and F.L. CROSBY. 1971. The relation of physiological stage, preconditioning, and rate of fall of temperature to cold injury and decline of peach trees. J. Amer. SOC. Hort. Sci. 96:50-53. DAVIDSON, O.W. and M.A. BLAKE. 1936. Response of young peach trees to nutrient deficiencies. Proc. Amer. Soc. Hort. Sci. 34:247-248. DAVIDSON, O.W. and M.A. BLAKE. 1937. Nutrient deficiency and nutrient balance with the peach. Proc. Amer. SOC. Hort. Sci. 35:339-346. DAVIS, J.R. 1968. A canker condition in peach (Prunus persica) induced by chilling and its relationship to bacterial canker (Pseudomonas syringae). Diss. Abstr. Intern. 28:4375-4376. DAVIS, J.R. and H. ENGLISH. 1965. A canker condition of peach seedlings induced by chilling. Phytopathology 552305-806. DAVIS, J.R. and H. ENGLISH. 1969a. Factors involved in the development of peach seedlings canker induced by chilling. Phytopathology 59:305-313. DAVIS, J.R. and H. ENGLISH. 1969b. Factors related to the development of bacterial canker on peach. Phytopathology 59:588-595. DAY, L.H. and E.F. SERR. 1951. Comparative resistance of rootstocks of fruit and nut trees to attack by a root-lesion or meadow nematode. Proc. Hort. Sci. 57:150-154. Amer. SOC. DAY, L.H. and W.P. TUFTS. 1939. Further notes on nematode-resistant Hort. Sci. 37:327-329. rootstocks for deciduous fruit trees. Proc. Amer. SOC. DEKOCK, P.C. and A. WALLACE. 1965. Excess phosphorus and iron chlorosis. Calif Agr. 19(4):3-4. DENNIS, F.G., JR. 1976. Trials of ethaphon and other growth regulators for delaying bloom in fruit trees. J. Amer. SOC. Hort. Sci. 101:241-245. DENNIS, F.G., JR. 1977. Dormancy and hardiness of fruit trees. HortScience 12:444. DE PLATER, C.V. and C.G. GREENHAM. 1959. A wide-range A-C bridge for determining injury and death. Plant Physiol. 34:661-667. DE VAY, J.E., B.G. LOWNSBERY, H. ENGLISH, and H. LAMBRIGHT. 1967. Activity of soil fumigants in relation to increased growth response and control of decline and bacterial canker in trees of Prunus persica. Phytopathology 57:809 (Abstr.). DE VAY, J.E., F.L. LUKEZIC, S.L. SINDEN, H. ENGLISH, and D.L. COPLIN. 1968. A biocide produced by pathogenic isolates of Pseudomonas syringae and its possible role in the bacterial canker disease of peach trees. Phytopathology 58:95-101. DHANVANTARI, B.N., P.W. JOHNSON, and V.A. DIRKS. 1975. The role of nematodes in crown gall infection of peach in southwestern Ontario. Plant Dis. Rptr. 59:109-112.
92
HORTICULTURAL REVIEWS
DHANVANTARI, B.N. and F. KAPPEL. 1978. Peach X-disease in southwestern Ontario. Can. P l a n t Dis. Suru. 58(3):65-68. DONOHO, C.W., JR., J.M. BEATTIE, E.S. BANTA, and H.Y. FORSYTH, J R . 1967. Possible cause of a disorder known as apple tree decline. HortScience 2:149-150. DONOHO, C.W., J R . and D.R. WALKER. 1960. The effect of temperature on certain carbohydrate and nitrogen fractions in the bark and roots on peach trees during the dormant season. Proc. Amer. Soc. Hort. Sci. 75:155-162. DOROZHKIN, N.A. and L.N. GRIOGORTSEVICH. 1976. Harmfulness of bacterial canker to fruit trees (English translation). Zashch. Rast. 12:39. DORSEY, M.J. 1918a. Adaptation in relation to hardiness. Minn. Hort. 46: 465-469. DORSEY, M.J. 1918b. Hardiness in top worked varieties of the apple. Proc. Amer. SOC. Hort. Sci. 15:38-45. DORSEY, M.J. 1921. Hardiness from the horticultural point of view. Proc. Amer. SOC. Hort. Sci. 18:173-178. DORSEY, M.J. 1929. A genetic conception of hardiness. Sci. Agr. 10:193199. DORSEY, M.J. and J.W. BUSHNELL. 1920. The hardiness problem. Proc. Amer. SOC. Hort. Sci. 17:210-224. DORSEY, M.J. and J.W. BUSHNELL. 1925. Plum investigations. 11. The inheritance of hardiness. Uniu. Minn. Agr. Expt. Sta. Tech. Bul. 32:34P. DORSEY, M.J. and P.D. STRAUSBAUGH. 1923. Plum investigations. I. Winter injury to plum during dormancy. Bot. Gaz. 76:113-143. DOSTALEK, J. 1973. The relation between the electric impedance of apple tree tissues and the proliferation disease. Biol. Plant. 15:112-115. DOWLER, W.M. 1972. Relationship between time of pruning and peach decline. Natl. Peach Counc. Proc. 31:116-117. DOWLER, W.M. and F.D. KING. 1966. Seasonal changes in starch and soluble sugar content of dormant peach tissues. Proc. Amer. SOC. Hort. Sci. 89230-84. DOWLER, W.M. and F.D. KING. 1967. Dormant season susceptibility of peach to bacterial canker not related to movement of Pseudomonas syringae. Phytopathology 575309-810 (Abstr.). DOWLER, W.M. and D.H. PETERSEN. 1966. Induction of bacterial canker of peach in the field. Phytopathology 56:989-990. DOWLER, W.M. and D.J. WEAVER. 1975. Isolation and characterization of fluorescent pseudomonads from apparently healthy peach trees. Phytopathology 65:233-236. DROZDOR, S.N., Z.F. SYCHEVA, N.P. BUDYKINA, N.I. BALAGUROVA, and N.P. KHOLOPTSEVA. 1976. Effect of prior temperature on the frost resistance of plants. Soviet P l a n t Physiol. 23:328-332. DYE, D.W. 1957. The effect of temp on infection by Pseudomonas syringae van Hall. New Zealand J. Sci. Technol., section A 38:500-505.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
93
EAGLES, C.F. and P.F. WAREING. 1964. The role of growth substances in the regulation of bud dormancy. Physiol. Plant. 17:697-709. EDGERTON, L.J. 1954. Fluctuations in the cold hardiness of peach flower buds during rest period and dormancy. Proc. Amer. SOC.Hort. Sci. 64:175180.
EDGERTON, L.J. 1957. Effect of nitrogen fertilization on cold hardiness of apple trees. Proc. Amer. SOC.Hort. Sci. 70:40-45. EDGERTON, L.J. 1960. Studies on the cold hardiness of peach trees. Cornell Uniu. Agr. Expt. Sta. Bul. 958. EDGERTON, L.J. and R.W. HARRIS. 1950. Effects of nitrogen and cultural treatment on Elberta peach fruit bud hardiness. Proc. Amer. SOC.Hort. S C ~ 55:51-55. . EDGERTON, L.J. and K.G. PARKER. 1958a. Cold hardiness of Montmorency cherry affected by nematode damage. Farm Res. 24:12. EDGERTON, L.J. and K.G. PARKER. 1958b. Effect of nematode infestation and rootstock on cold hardiness of Montmorency cherry trees. Proc. Amer. SOC.Hort. Sci. 72:134-138. EGGERT, R. 1944. Cambium temperatures of peach and apple trees in winter. Proc. Amer. SOC. Hort. Sci. 45:33-36. EL-MANSY, H.I. and D.R. WALKER. 1969. Seasonal fluctuations of amino acids, organic acids, and simple sugars in ‘Elberta’ peach and ‘Chinese’ apricot flower buds during and after rest. J. Amer. SOC. Hort. Sci. 94:184-192. EMERSON, F.H., R.H. HAYDEN, and K. KENSIL. 1977. Effect of rootstock on fruit bud initiation and hardiness of peach and nectarine cultivars. HortScience 86:131-311 (Abstr.). EMERSON, R.H. 1903. Experiments in orchard culture. 111. Root killing of apple and cherry stocks in relation to soil moisture and soil covers. Nebr. Agr. Expt. Sta. Bul. 79:26-32. ENGLISH, H. 1961. Effect of certain soil treatments on development of bacterial canker in peach trees. Phytopathology 5 1 5 5 (Abstr.). ENGLISH, H. and J.R. DAVIS. 1969. Effect of temperature and growth state on the susceptibility of Prunus spp. to Pseudomonas syringae. Phytopathology 59:1025 (Abstr.). ENGLISH, H. and J.E. DE VAY. 1964. Influence of soil fumigation on growth and canker resistance of young fruit trees in California. Down to Earth 20:68. ENGLISH, H., J.E. DE VAY, 0. LILLELAND, and J.R. DAVIS. 1961. Effect of certain soil treatments on the development of bacterial canker in peach trees. Phytopathology 51:65. FERGUSON, R.B., R. A. RYKER, and E.D. BALLARD. 1975. Portable oscilloscope technique for detecting dormancy in nursery stock. USDA Forest Serv. Gen. Tech. Rpt. INT-26. FILEWICZ, W. 1931. The frost injuries of fruit trees in Poland in 1928-29 with special reference to influence of the stock and scion upon the resistance of apple trees against frost. Proc. 9th Intern. Hort. Congr., p. 312-320.
94
HORTICIJLTURAL REVIEWS
FILEWICZ, W. and I. MODLIBOWSKA. 1941. The influence of a scion variety on the resistance of the roots against frost. Proc. Amer. Soc. Hort. Sci. 38 :348-3 52. FILINGER, G.A. and A.B. CARDWELL. 1941. A rapid method of determining when a plant is killed by extreme temp. Proc. Amer. Soc. Hort. Sci. 39:85-86. FLINT, H.L., B.R. BOYCE, and D.J. BEATTIE. 1967. Index of injury-A useful expression of freezing injury to plant tissue as determined by the electrolytic method. Can. J. P l a n t Sci. 47:229-230. FOGLE, H.W. 1975. Trends in the peach industry. p. 495-500. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. FOS, A. 1976. Preliminary entomological observations on cherry decline in Tarn-et-Garonne. Rev. Zool. Agr. Pathol. Veg. 75:134-140. FOSTER, H.H. 1960. Identification and pre-plant control of parasitic nematodes attacking peach trees in South Carolina. Phytopathology 50:575. FOSTER, H.H. and D.F. COHOON. 1958. Post-plant fumigation for the control of root-knot nematode in South Carolina. Phytopathology 48:342. FOSTER, H.H., C.E. GAMBRELL, and W.H. RHODES. 1965. Effects of pre-plant nematicides and rootstocks on the growth and fruit production of peach trees in Meloidogyne-infested soil. Nematologica 11:38 (Abstr.). FOSTER, H.H., C.E. GAMBRELL, JR., W.H. RHODES, and W.P. BYRD. 1972. Effect of pre-plant nematicides and resistant rootstocks on growth and fruit production of peach trees in Meloidogyne spp.-infested soil of South Carolina. P l a n t Dis. Rptr. 56:169-171. FRENCH, W.J. and J.W. MILLER. 1974. Bacterial canker of peach in Florida. Proc. Fla. State Hort. Soc. 86:310-311. FRENYO, V. and T. BUBAN. 1976. Possible precursors of apricot apoplexy in leaves. Bot. Kozlemen. 63:131-137. FIJCHIGAMI, L.H., D.R. EVERT, and C.J. WEISER. 1971. A translocatable cold hardiness promoter. P l a n t Physiol. 47:164-167. GALLAHER, R.N., H.F. PERKINS, and J.B. JONES, JR. 1975. Calcium concentration and distribution in healthy and decline peach tree tissue. HortScim ce 10 :134 - 13 7. GARDAN, L., J . LUISETTI, J.P. PRUNIER, and A. VIGOUROUX. 1975. Quick decline of peach (English translation). Ann. Phytopathol. 7:185-187. GARDAN, L., J.P. PRUNIER, J. LUISETTI, and J.J. BEZELGUES. 1973. Study on bacterial diseases of fruit trees. VII. Responsibility of various P.seudomonas in the bacterial decline of apricot trees in France. Rev. Zool. Agr. Pathol. Veg. 72:112-120. GARDNER, J.M., R.P. SCHEFFER, and N. HIGINBOTHAM. 1974. Effect of host-specific toxins on electropotentials of plant cells. P l a n t Physiol. 54: 246-249.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
95
GERBER, J.F., J.D. MARTSOLF, and J.F. BARTHOLIC. 1974. The climate of trees and vines. HortScience 9:569-572. GIDDENS, J., H.F. PERKINS, J.B. JONES, JR., and J. TAYLOR. 1972. Effect of peach root residue, lime, and supplemental nitrogen on survival and yield of peach trees in a decline area. Comm. Soil Sci. Plant Anal. 3:253-259. GILMORE, A.E. 1949. The peach replant problem. Calif. Fruit & Grape Grower 36:19-21. GILMORE, A.E. 1959. Growth of replanted peach trees. Proc. Amer. SOC. Hort. Sci. 73:99-111. GILMORE, A.E. 1963. Pot experiment related to the peach replant problem. Hilgard ia 34 :63-78. GOLUS, B.M. 1935. Changes of plasma permeability induced by temperature effects. Compt. Rend. Acad. Sci. 2:305-306. GOOD, J.M. 1960. Control of nematodes in peach orchards. Ga. Coastal Plain Expt. Sta. Mimeo Ser. N. S. 104. GRANETT, A.L. and R.M. GILMER. 1971. Mycoplasmas associated with Xdisease in various Prunus species. Phytopathology 61:1036-1037. GREENHAM, C.G. and D.J. COLE. 1950. Studies on the determination of dead and diseased tissues. I. Investigations on dead plant tissues. Austral. J. Agr. Res. 1:103-117. HAMMOND, M.W. and S.D. SEELEY. 1977. Cold acclimation of apple tree bark in response to photoperiod, temperature, and abscisic acid. HortScience 12:421 (Abstr.). HAMPSON, M.C. and W.A. SINCLAIR. 1973. Xylem dysfunction in peach caused by Cytospora leucostoma. Phytopathology 63:676-681. HAMPSON, M.C. and W.A. SINCLAIR. 1974. Leucostoma canker of peach: Symptoms in relation to water supply. Plant Dis. Rptr. 58:971-973. HANSEN, C.J. 1955. Influence of the rootstock on injury from excess boron in Nonpareil almond and Elberta peach. Proc. Amer. SOC. Hort. Sci. 65:128-132. HANSEN, C.J., B.F. LOWNSBERY, and C.O. HESSE. 1956. Nematode resistance in peaches. Calif. Agr. 10(9):5-11. HARE, W.W. 1965. The inheritance of resistance to nematodes. PhytopathOlogy 55 :1162 - 1167. HARRISON, T.B. 1958. Replanting peach trees. Amer. Fruit Grower 78:29. HARVEY, R.B. 1923. Cambial temperature of trees in winter and their relation to sun scald. Ecology 4:261-265. HAVIS, A.L. 1962. Some effects of old peach soil treatments on young peach trees in the greenhouse. Proc. Amer. SOC. Hort. Sci. 81:147-152. HAVIS, L. and A.L. GILKESON. 1947. Toxicity of peach roots. Proc. Amer. SOC. Hort. Sci. 50:203-205. HAVIS, A.L., H.F. MORRIS, R. MANNING, and T.E. DENMAN. 1958. Responses of replanted peach trees to soil treatments in field tests in Texas. Proc. Amer. SOC.Hort. Sci. 71:67-76.
96
HORTICULTURAL REVIEWS
HAYDEN, R.A., E.F. SAVAGE, and V.E. PRINCE. 1968. Growth of young peach trees as affected by pre-plant fumigant treatment. Proc. Amer. SOC. Hort. Sci. 93:119-127. HEIMANN, M. 1968. New investigation on factors causing gummosis in apricots. Acta Hort. 11:529-536. HEINICKE, A.J. 1932. The effect of submerging the roots of apple trees a t different seasons of the year. Proc. Amer. SOC. Hort. Sci. 29:205-207. HELTON, A.W. 1961. Low temp injury as a contributing factor in Cytospora invasion of plum trees. P l a n t Dis. Rptr. 45:591-597. HELTON, A.W. and H. RANDALL. 1975. Cambial gummosis in P r u n u s domestica infected with Cytospora cincta. P l a n t Dis. Rptr. 59:340-344. HELTON, A.W. and K.G. ROHRBACH. 1967. Chemotherapy of Cytospora canker disease in peach trees. Phytopathology 57:442-446. HENDERSCHOTT, C.H. and L.F. BAILEY. 1955. Growth-inhibiting substances in extracts of dormant flower buds of peach. Proc. Amer. SOC. Hort. Sci. 65:85-92. HENDERSCHOTT, C.H. and D.R. WALKER. 1959. Seasonal fluctuations in quantity of growth substances in resting peach flower buds. Proc. Amer. SOC. Hort. Sci. 74:121-129. HENDRIX, F.F., JR. and W.M. POWELL. 1969. Control of peach tree decline in established orchards. Down to Earth 24:14-16. HENDRIX, F.F., JR. and W.M. POWELL. 1970a. Control of root pathogens in peach tree decline sites. Phytopathology 60:16-19. HENDRIX, F.F., JR. and W.M. POWELL. 1970b. Role of soil-borne fungi in peach tree decline. Uniu. Ga. Expt. Sta. Res. Bul. 77:7-16. HENDRIX, F.F., JR., W.M. POWELL, and J.H. OWEN. 1966. Relation of root necrosis caused by Pythium species to peach tree decline. PhytopathOlogy 5 6 :1229- 12 32. HEUSER, C.W. 1972. Response of callus cultures of Prunuspersica, P. tomentosa, and P. besseyi to cyanide. Can. J. Bot. 50:2149-2152. HEWETSON, F.N. 1953. Reestablishing the peach orchard. Pa. Agr. Expt. Sta. Prog. Rpt. 106. HEWETSON, F.N. 1957. Reestablishing the peach orchard: The influence of various nutrient solutions and fertilizers on the growth and development of one-year peach trees. Proc. Amer. SOC. Hort. Sci. 69:122-125. HIBBARD, A.D. 1948. The effect of severity of pruning on the performance of young Elberta peach trees. Proc. Amer. SOC.Hort. Sci. 52:131-136. HIBINO, H., G.H. KALOOSTIAN, and H. SCHNEIDER. 1971. Mycoplasmalike bodies in the pear psylla vector of pear decline. Virology 43:34-40. HIBINO, H. and H. SCHNEIDER. 1970. Mycoplasma-like bodies in seive tubes of pear trees affected with pear decline. Phytopathology 60:499-501. HICKEY, K.D. 1962. Peach cankers affect production life of trees. Wayne County (N. Y ) Farm & Home News 46:4.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
97
HIGGINS, B.B., G.P. WALTON, and J.J. SKINNER. 1943. The effect of nitrogen fertilization on cold injury of peach trees. Ga. Agr. Expt. Sta. Bul. 266. HILBORN, M.T. and J.H. WARING. 1946. A summary of investigations on use of hardy trunk-forming stocks in Maine. Proc. Amer. SOC.Hort. Sci. 48: 151-165. HILDEBRAND, E.M. 1947. Perennial peach canker and the canker complex in New York, with methods of control. Cornell Agr. Expt. Sta. Mem. 276. HILDRETH, A.C. 1926. Determination of hardiness in apple varieties and the relation of some factors to cold resistance. Minn. Agr. Expt. Sta. Bul. 42. HINE, R.B. 1961a. The role of amygdalin breakdown in the peach replant problem. Phytopa thology 51 :lo-13. HINE, R.B. 1961b. The role of fungi in the peach replant problem. Plant Dis. Rptr. 45:462-465. HODGSON, F.R. 1923. Observations on the rest period of deciduous fruit trees in a mild climate. Proc. Amer. SOC.Hort. Sci. 20:151-155. HOESTRA, H. 1961. The role of nematodes in the orchard replant problem. 6 t h Intern. Nematol. Symp., p. 62-63. HOESTRA, H. 1965. Thielauiopsis basicola, a factor in the cherry replant problem in the Netherlands. Neth. J. Plant Pathol. 71:180-182. HOESTRA, H. 1967. Specific apple replant disease: prospects and problems. Meded. Ryksfaculteit Landb.-Wet. Gent. 32:427-432. HOESTRA, H. 1968. Replant diseases of apple in the Netherlands. Mededelingen Landbouwhog. Wagen., Nederland, 68-13, p. 1-105. HOLUBOWICZ, T. 1976. Modification of winter hardiness of fruit plants by different environmental conditions and growth substances. A n n . Rpt. Acad. Agr., Inst. Hort. Prod., Poznan, Poland 1:l-60. HOLUBOWICZ, T. and A.A. BOE. 1969. Development of cold hardiness in apple seedlings treated with GA and ABA. J. Amer. SOC. Hort. Sci. 94:661-664. HOLUBOWICZ, T. and A.A. BOE. 1970. Correlation between hardiness and free amino acid content of apple seedlings treated with GA and ABA. J. Amer. SOC.Hort. Sci. 95:85-88. HOWARD, R.F. 1924. The relation of low temperatures to root injury of the apple. Nebr. Agr. Expt. Sta. Bul. 199. HOWELL, G.S. and C.J. WEISER. 1970. The environmental control of cold acclimation in apple. Plant Physiol. 45:390-394. HUNG, C.P. and W.R. JENKINS. 1969. Criconemoides curuatum and the peach tree decline problem. J. Nematol. 1:12 (Abstr.). HUTCHINS, L.M. 1933. Identification and control of the phony disease of the peach. Ga. Sta. Dept. Entomol. Bul. 78. HUTCHINS, L.M. 1936. Nematode resistant peach rootstocks of superior vigour. Proc. Amer. SOC. Hort. Sci. 35:330-338.
98
HORTICULTURAL REVIEWS
HUTCHINSON, A. and O.A. BRADT. 1968. Clonal plum and peach seedling rootstocks for peaches on a clay loam a t Vineland. Hort. Res. Inst. Ont. Rpt., 1962-1968. p. 16-22. ILIEV, J. 1968. “Apoplexy” of the apricot tree in connection with the height and type of the trunk. Acta Hort. 11:329-335. IRVING, R.M. and F.O. LANPHEAR. 1967. Environmental control of cold hardiness in woody plants. Plant Physiol. 42:1191-1196. ISRAEL, D.W., J.E. GIDDENS, and W.W. POWELL. 1973. The toxicity of peach tree roots. Plant & Soil 39:103-112. JACKSON, J.E. 1973. Effects of soil fumigation on the growth of apple and cherry rootstocks on land previously cropped with apples. A n n . Appl. Biol. 74:99-104. JACOBSEN, J.V. 1977. Regulation of ribonucleic acid metabolism by plant hormones. Annu. Rev. Plant Physiol. 28:537-564. JENSEN, D.D. 1971. Herbaceous host plants of Western X-disease agent. Phytopa t hology 6 1:1465- 1470. JENSEN, R.E., E.F. SAVAGE, and R.A. HAYDEN. 1970. The effect of certain environmental factors on cambium temperatures of peach trees. J.Amer. SOC. Hort. Sci. 95:286-292. JOHANSON, F.D. 1950. A preliminary report on the incidence of two types of plant parasitic nematodes on peaches in Connecticut. Storrs Agr. Expt. Sta. Univ. Conn. Info. 10. JOHNSON, J. 1965. The use of certain soil fumigants and nematicides as preand post-plant treatments on peach and plum trees. Phytopathology 55:499. JOHNSON, P.W., V.A. DIRKS, and R.E.C. LAYNE. 1978. Population studies of Pratylenchus penetrans and its effects on peach seedling rootstocks. J. Amer. SOC. Hort. Sci. 103:169-172. JOHNSTONE, G.R. and W.D. BOUCHER. 1973. Interaction of rootstock, scion variety, and virus complement on apple tree growth. J. Hort. Sci. 48:175179. JONES, A.L. 1971a. Bacterial canker of sweet cherry in Michigan. Plant Dis. Rptr. 55:961-965. JONES, A.L. 1971b. Diseases of tree fruits in Michigan. Ext. Bul. E-714, Coop. Ext. Serv., Mich. State Univ., East Lansing, p. 1-31. JONES, M.B. and J.V. ENGIE. 1961. Identification of a cyanogenetic growthinhibiting substance in extracts of peach flower buds. Science 134:284. JONES, M.B., J.W. FLEMING, and L.F. BAILEY. 1957. Cyanide as a growthinhibiting substance in extracts of peach leaves, bark, and flower buds. Proc. Amer. SOC. Hort. Sci. 69:152-157. KAMINSKA, M. 1973a. Course of infection in young apple trees with proliferation disease (English translation). Acta Agrobot. 26:103-113. KAMINSKA, M. 1973b. The effect of apple proliferation disease on chlorophyll, free amino acid, and amide contents in the leaves of infected trees. Phytopa thol. Zeit. 76:142-148.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
99
KAMINSKA, M. and B. ZAWADZKA. 1973. Studies on apple proliferation in Poland. 111. Observations on the disappearance of apple proliferation symptoms (English translation). Acta Agrobot. 26:97-101. KAMINSKA, M., B. ZAWADZKA, and D.F. MILLIKAN. 1971. Some physiological changes associated with the proliferation disease in apple. Phytopathol. Zeit. 72:86-91. KEGLER, H., H.M. MULLER, H. KLEINHEMPEL, and T.D. VERDEREVSKAJA. 1973. Investigations on cherry decline and bilberry witches’ broom (English translation). Nachricht. Pflanzenschutz. DDR 27:5-8. KENIS, J.D. and M.O. EDELMAN. 1976. Some biochemical aspects of dormancy and its interruption in flower buds of the peach, Prunus persica cv. Dixie Red. I. Changes in RNAse and proteinase activity and composition of polyphenoloxidases and peroxidases and modifications in the concentration of RNA, soluble proteins, and total nitrogen. Phyton 34:133-142. KENKNIGHT, G. 1958. Thermal stability of peach rosette virus. Phytopathology 48 :33 1- 33 5. KENNARD, W.C. 1949. Defoliation of Montmorency sour cherry trees in relation to winter hardiness. Proc. Amer. SOC. Hort. Sci. 53:129-133. KETCHIE, D.O. 1966. Fatty acids in the bark of Halehaven peach as associated with hardiness. Proc. Amer. SOC. Hort. Sci. 88:204-207. KETCHIE, D.O. and C.H. BEEMAN. 1973. Cold acclimation in Red Delicious apple trees under natural conditions during four winters. J. Amer. SOC. Hort. Sci. 98:257-261. KETCHIE, D.O., C.H. BEEMAN, and A.L. BALLARD. 1972. Relationship of EC to cold injury and acclimation in fruit trees. J. Amer. SOC. Hort. Sci. 97: 403-406. KETCHIE, D.O. and C. MURREN. 1972. Effect of glycerol on the survival of apple trees. Cryobiology 9:315 (Abstr.). KETCHIE, D.O. and C. MURREN. 1976. Use of cryoprotectants on apple and pear trees. J. Amer. SOC. Hort. Sci. 101:57-59. KIRKPATRICK, H.C., S.K. LOWE, and G. NYLAND. 1975a. Peach rosette: The morphology of an associated mycoplasma-like organism and the chemotherapy of the disease. Phytopathology 652364-870. KIRKPATRICK, H.C., J.M. THOMPSON, and J.H. EDWARDS. 1975b. Effects of aluminum concentration on growth and chemical composition of peach seedlings. HortScience 10:132-134. KLEMENT, Z., D.S. ROZSNYAY, and M. ARSENIJEVIC. 1974. Apoplexy of apricots. 111. Relationship of winter frost and the bacterial canker and dieback of apricots. Acta Phytopathol. Acad. Sci. Hung. 9:35-45. KLEMENT, Z., D.S. ROZSNYAY, and E. VISNYOBSZKY. 1972. Apoplexy of apricots. I. Bacterial die-back and the development of the disease. Acta Phytopathol. Acad. Sci. Hung. 7:3-12. KNECHT, G.N. and E.R. ORTON, JR. 1970. Stomate density in relation to winter hardiness of Ilex opaca Ait. J. Amer. SOC. Hort. Sci. 95:341-345.
100
HORTICULTURAL REVIEWS
KNOWLTON, H.E. 1936. Experiments on the hardiness of peach and apple fruit buds. Proc. Amer. SOC.Hort. Sci. 34:238-241. KOCH, L.W. 1955. The peach replant problem in Ontario. I. Symptomology and distribution. Can. J Bot. 33:450-460. KOCHBA, J. and R.M. SAMISH. 1971. Effect of kinetin and NAA on rootknot nematodes in resistant and susceptible peach rootstocks. J. Amer. SOC. Hort. Sci. 96:458-461. KOCHBA, J. and R.M. SAMISH. 1972a. Level of endogenous cytokinins and auxins in roots of nematode resistant and susceptible peach rootstocks. J . Amer. SOC.Hort. Sci. 97:115-119. KOCHBA, J . and R.M. SAMISH. 1972b. Effect of growth inhibitors on rootknot nematodes in peach roots. J. Amer. SOC.Hort. Sci. 97:178-180. KOCHBA, J., P. SPIEGEL-ROY, and R.M. SAMISH. 1972. Response of ‘Bonita’ and ‘Ventura’ peach cvs. on various peach and apricot seedling rootstocks in an arid environment. Israeli J. Agr. Res. 22:189-200. KOLOMIETS, LA., E.V. TEPLITSKAYA, and T.M. PARFENOVA. 1970. On the role of growth inhibitors in winter dormancy and frost resistance of apple and peach trees. Fiziol. Biokhim. Rasten. 2:410-415. KOUYEAS, H. 1971. On the apoplexy of stone fruit trees caused by Phytophthora spp. Ann. Inst. Phytopathol. Benaki N. S. 1,0:163-170. KRUPASAGAR, V. and K.R. BARKER. 1966. Increased cytokinin concentrations in tobacco infected with root-knot nematode Meloidogyne incognita. Phytopathology 56:885 (Abstr.). KUNZE, L. 1972. Investigations on determining proliferation disease of apple in serial tests (English translation). Mitteil. Biol. Rundesanst. Land-Forstwirt. Berlin-Dahlem 144:35-46. LADD, J.N., P.G. BRISBANE, J.H.A. BUTLER, and M. AMATO. 1976. Studies on soil fumigation. 111. Effect on enzyme activities, bacterial number, and ninhydrin-reactive compounds. Soil Biol. Biochem. 8:255-260. LAMMERTS, W.E. 1941. An evaluation of peach and nectarine varieties in terms of winter chilling requirements and breeding possibilities. Proc. Amer. SOC.Hort. Sci. 39:205-211. LANGRIDGE, J. 1963. Biochemical aspects of temperature response. Ann. Rev. Plant Physiol. 14:441-462. LANTZ, H.L. and B.S. PICKETT. 1942. Apple breeding: Variation within and between progenies of Delicious with respect to freezing injury due to the November freeze of 1940. Proc. Amer. SOC. Hort. Sci. 40:237-240. LAPINS, K. 1961. Artificial freezing of 1-year-old shoots of apple varieties. Can. J . Plant Sci. 41:381-393. LAPINS, K. 1962. Artificial freezing as a routine test of cold hardiness of young apple seedlings. Proc. Amer. SOC.Hort. Sci. 81:26-34. LARSEN, F.E. 1967. Stimulation of leaf abscission of woody plants by potassium iodide and alanine. HortScience 2:19-20.
SHORT LIFE. REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
101
LASHEEN, A.M. and C.E. CHAPLIN. 1971. Biochemical comparison of seasonal variations in three peach cultivars differing in cold hardiness. J.Amer. SOC. Hort. Sci. 96:154-159. LASHEEN, A.M., C.E. CHAPLIN, and R.N. HARMON. 1970. Biochemical comparison of fruit buds in five peach cultivars of varying degree of cold hardiness. J. Amer. SOC.Hort. Sci. 95:177-181. LAYNE, R.E.C. 1974. Breeding peach rootstocks for Canada and the Northern U S . HortScience 9:364-366. LAYNE, R.E.C. 1975. New developments in peach varieties and rootstocks. Compact Fruit Tree 8:69-77. LAYNE, R.E.C. 1976a. Influence of peach seedling rootstocks on perennial canker of peach. HortScience 11:509-511. LAYNE, R.E.C. 1976b. Peach rootstock breeding, rootstock hardiness, and rootstock influence on scion cultivars. Riu. Ortoflorofrutt. Ital. 60:113-119. LAYNE, R.E.C., H.O. JACKSON, and F.D. STROUD. 1973. Influence of peach seedling rootstock on growth, yield, and cold hardiness of peach scion cultivars. HortScience 8:267 (Abstr.). LAYNE, R.E.C., H.O. JACKSON, and F.D. STROUD. 1977. Influence of peach seedling rootstock on defoliation and cold hardiness of peach cultivars. J . Amer. SOC.Hort. Sci. 102:89-92. LAYNE, R.E.C. and G.M. WARD. 1978. Rootstock and seasonal influences on carbohydrate levels and cold hardiness of ‘Redhaven’ peach. J . Amer. SOC. Hort. Sci. 103:408-413. LAYNE, R.E.C., G.M. WEAVER, H.O. JACKSON, and F.D. STROUD. 1976. Influence of peach seedling rootstock on growth, yield, and survival of peach scion cultivars. J . Amer. SOC. Hort. Sci. 101:568-572. LEBEDEV, S.I. and P.A. KOMARNITSKII. 1971. Physiological-biochemical changes in Mazzard cherry buds and their frost resistance during ontogenesis. Soviet Plant Physiol. 18:151-156. LEPIDI, A.A., N.P. NUTI, and U. CITERNESI. 1974. Microbiological aspects of the peach replant disease: The rhizophere effect in peach replanted in normal and diseasing conditions. A n n . Phytopathol. 6~35-44. LESLEY, J.W. 1944. Peach breeding in relation to winter chilling requirements. Proc. Amer. SOC. Hort. Sci. 45:243-250. LESLEY, J.W. 1957. A genetic study of inbreeding and crossing inbred lines Hort. Sci. 70:93-103. of peaches. Proc. Amer. SOC. LEVENGOOD, W.C. 1973. Bioelectric currents and oxidants levels in plant systems. J. Expt. Bot. 24:626-639. LEVITT, J. 1951. Frost, drought, and heat resistance. A n n . Rev. Plant Physiol. 2:245-268. LEVITT, J. 1959. Effect of artificial increase in sugar content on frost hardiness. Plant Physiol. 34:401-402. LEVITT, J. 1966. Winter hardiness in plants. p. 495-563. I n H.L. Meryman I
102
HORTICULTIJRAL REVIEWS
(ed.). Cryobiology. Academic Press, New York. LIPE, W.N. and J.C. CRANE. 1966. Dormancy regulation in peach seed. Science 153:541-542. LOWNSBERY, B.F. 1959. Studies of the nematodes, Criconemoides xenoplax on peach. Plant Dis. Rptr. 43:913-917. LOWNSBERY, B.F. 1961. Factors affecting populations of Criconemoides xenoplax. Phytopa thology 5 1:101-103. LOWNSBERY, B.F., H. ENGLISH, E.H. MOODY, and F.J. SCHICK. 1973. Criconemoides xenoplax experimentally associated with a disease of peach. Phytopathology 63:994-998. LOWNSBERY, B.F., J.T. MITCHELL, W.H. HART, F.M. CHARLES, M.H. GERDTS, and A.S. GREATHEAD. 1968. Responses to post-planting and pre-planting soil fumigation in California peach, walnut, and prune orchards. Plant Dis. Rptr. 525390-894. LOWNSBERY, B.F. and I.J. THOMASON. 1959. Progress in nematology related to horticulture, a review. Proc. Amer. SOC. Hort. Sci. 74:730-746. LUEPSCHEN, N.S. 1976. Use of benomyl sprays for suppressing Cytospora canker on artificially inoculated peach trees. Plant Dis. Rptr. 60:477-479. LUEPSCHEN, N.S. and K.G. ROHRBACH. 1969. Cytospora canker of peach trees: Spore availability and wound susceptibility. Plant Dis. Rptr. 53:869872. LUEPSCHEN, N.S., K.G. ROHRBACH, A.C. JONES, and L.E. DICKENS. 1975. Susceptibility of peach cultivars to Cytospora canker under Colorado orchard conditions. HortScience 10:76-77. LUISETTI, J., L. GARDAN, and J.P. PRUNIER. 1973. Studies on bacterial diseases of fruit trees. VI. Study on pathogenicity of Pseudomonas morsprunorum f.sp. persicae. Effect of inoculum concentration. A n n . Phytopath01. 5:347-353. LUISETTI, J. and J.P. PAULIN. 1972. Studies on bacterial diseases of fruit trees. 111. Investigations of Pseudomonas syringae (van Hall) on the surface of aerial parts of the pear tree and a study of its quantitative variations. A n n . Phytopathol. 4:215-227. LUKENS, R.J., P.M. MILLER, G.S. WALTON, and S.W. HITCHCOCK. 1971. Incidence of X-disease of peach and eradication of chokecherry. Plant Dis. Rptr. 55:645-647. LYONS, J.M. 1973. Chilling injury in plants. A n n u . Rev. Plant Physiol. 24: 445-466. LYSKANOWSKA, M.K. 1976. Bacterial canker of sweet cherry ( P r u n u s auium) in Poland. I. Symptoms, disease development, and economic importance. Plant Dis. Rptr. 60:465-469. MAI, W.F. and K.G. PARKER. 1967. Root diseases of fruit trees in New York State. I. Population of Pratylenchus penetrans and growth of cherry in response to soil treatment with nematicides. Plant Dis.Rptr. 51:398-401.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
103
MALO, S.E. 1967. Nature of resistance of Okinawa and Nemaguard peach to root-knot nematode M. jaoanica. Proc. Amer. SOC. Hort. Sci. 90:39-46. MARTH, P.C. and F.E. GARDNER. 1939. Evaluations of variety peach seedHort. Sci. 37: ling stocks with respect to ‘wet-feet’tolerance. Proc. Amer. SOC. 335-337. MARTSOLF, J.D., C.M. RITTER, and A.H. HATCH. 1975. Effect of white latex paint on temperature of stone fruit tree trunks in winter. J. Amer. SOC. Hort. Sci. 100:122-129. MAZUR, P. 1969. Freezing injury in plants. Annu. Rev. Plant Physiol. 20: 419-448. MCBETH, C.W. 1954. Some practical aspects of soil fumigation. Plant Dis. Rp tr. 2 27:95- 9 7. MCBETH, C.W. and A.L. TAYLOR. 1944. Immune and resistant cover crops valuable in root-knot infested peach orchards. Proc. Amer. SOC. Hort. Sci. 45: 158-166. MCCLUNG, A.C. 1953. Magnesium deficiency in North Carolina peach orchards. Proc. Amer. SOC. Hort. Sci. 62:123-130. MCCOWN, B.H., G.E. BECK, and T.C. HALL. 1969. The hardening response of three clones of Dianthus and the corresponding complement of peroxidase iso-enzymes. J. Amer. SOC. Hort. Sci. 94:691-693. MCCUE, C.A. 1915. Effect of certain mineral fertilizers upon strength of wood in the peach tree. Proc. Amer. SOC. Hort. Sci. 12:113-118. MCGLOHON, H.E. and M.E. FERREE. 1976. Control peach tree short life. Fruit South 1:6-8. MCKEE, M.W., J.H. FRIDRICH, and C.G. FORSHEY. 1972. Some effects of eastern X-disease on the nitrogen metabolism of peach leaves. HortScience 7:393-394. MEADOR, E.M. and M.A. BLAKE. 1943. Seasonal trend of fruit bud hardiness in peaches. Proc. Amer. SOC. Hort. Sci. 43:91-98. MILLER, R.W. and W.M. DOWLER. 1973. Report from research work group studying peach tree short life. Coop. Ext. Serv. Clemson Univ. 4. MINZ, G. and E. COHN. 1962. Susceptibility of peach rootstocks to root-knot nematodes. Plant Dis. Rptr. 46:531-534. MIRCETICH, S.M. 1971. The role of Pythium in feeder roots of deceased and symptomless peach trees and in the orchard soils in peach tree decline. Phytopathology 6 1:357 - 360. MIRCETICH, S. M. and H.W. FOGLE. 1969. Stem pitting in Prunus species other than peach. Plant Dis. Rptr. 53:5-11. MIRCETICH, S.M. and H.L. KEIL. 1970. Phytophthora cinnemoni root rot and stem canker of peach trees. Phytopathology 60:1376-1382. MIRCETICH, S.M. and M.E. MATHERON. 1976. Phytophthora root and crown rot of cherry trees. Phytopathology 66:549-558.
104
HORTICULTURAL REVIEWS
MIRCETICH, S.M., W.J. MOLLER, and G. NYLAND. 1977. Prunus stem pitting in sweet cherry and other stone fruit trees in California. Plant Dis. Rptr. 6 1:93 1-935. MIZUTANI, F., A. SUGIURA, and T. TOMANA. 1977. Studies on the soil sickness problem for peach trees. 1. Cyanogenesis in the relationship between root sensitivity to water-logging and soil sickness. J. Japan. SOC. Hort. Sci. 46: 9-17. MOJTAHEDI, H., B.F. LOWNSBERY, and E.H. MOODY. 1975. Ring nematodes increase development of bacterial cankers in plums. Phytopathology 65:556-559. MOUNTAIN, W.B. and H.R. BOYCE. 1957. Parasitic nematodes in relation to the peach replant problem in Ontario. Phytopathology 47:313. MOUNTAIN, W.B. and H.R. BOYCE. 1958a. The peach replant problem in Ontario. V. The relation of parasitic nematodes to regional differences in severity of peach replant failure. Can. J. Bot. 36:125-134. MOUNTAIN, W.B. and H.R. BOYCE. 1958b. The peach replant problem in Ontario. VI. The relation of Pratylenchuspenetrans to the growth of young peach trees. Can. J. Bot. 36:135-151. MOUNTAIN, W.B. and Z.A. PATRICK. 1959. The peach replant problem in Ontario. VII. The pathogenicity of Pratylenchus penetrans (Cobb. 1917) Filip. and Stek. 1941. Can. J. Bot. 37:459-470. MOWRY, J.B. 1960. Factors in productivity of peach varieties. Trans. Ill. State Hort. SOC.94:llO-119. NESMITH, W.C. and W.M. DOWLER. 1973. Cold hardiness of peach trees as affected by certain cultural practices. HortScience 8:267 (Abstr.). NESMITH, W.C. and W.M. DOWLER. 1975. Soil fumigation and fall pruning related to peach tree short life. Phytopathology 65:277-280. NESMITH, W.C. and W.M. DOWLER. 1976. Cultural practices affect cold hardiness and peach tree short life. J. Amer. Sac. Hort. Sci. 101:116-119. NYLAND, G . and W.J. MOLLER. 1973. Control of pear decline with a tetracycline. Plant Dis. Rptr. 57:634-637. OBERLE, G.D. 1957. Breeding peaches and nectarines resistant to spring frosts. Proc. Amer. SOC. Hort. Sci. 70:85-92. OH, S.D. and R.F. CARLSON. 1976. Water soluble extracts from peach plant parts and their effect on growth of seedlings of peach, apple, and bean. J. Amer. Sac. Hort. Sci. 101:54-57. OLIEN, C.R. 1967. Freezing stresses and survival. Annu. Rev. Plant Physiol. 18:387-408. ORION, D. and D. ZUTRA. 1971. The effect of the root-knot nematode on the penetration of crown gall bacteria into almond roots. Israeli J. Agr. Res. 21: 27-29. ORMROD, D.P. and R.E.C. LAYNE. 1974. Temperature and photoperiod effects on cold hardiness of peach scion-rootstock combinations. HortScience 9: 451-453.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
105
ORMROD, D.P. and R.E.C. LAYNE. 1977. Scion and rootstock influence on winter survival of peach trees. Fruit Var. J. 31:30-33. OSTERHOUT, W.J.V. 1922. Injury, recovery, and death in relation to conductivity and permeability. J.B. Lippincott Co., Philadelphia. OTTO, G. 1972a. Investigations on the cause of replant disease in fruit trees. I. Experiments on the transmission of replant disease through roots. Zentra 1b. Ba k teriol., Parasi ten k. I n f e k tions kra n k. Hygiene 127 :2 79 - 289. OTTO, G. 1972b. Investigations on the cause of replant disease in fruit trees. 11. Experiments on the transmission of replant disease by rootless diseased soil. Zentral b. Ba kteriol., Parasiten k. In fektionskran k. Hygiene 127:601611. OTTO, G. 1972c. Investigations on the cause of replant disease in fruit trees. 111. Experiments to remove replant disease by soil steaming a t various temperatures. Zentral b. Ba kteriol., Parasiten k. I n fektionskran k. Hygiene 127: 777-782. OTTO, G 1972d. Investigations on the cause of replant disease in fruit trees. V. Effect of different steaming temperatures on the microflora of diseased soil. Zentral b. Ba kteriol., Parasiten k. I n fektionskran k. Hygiene 128:377382. OVERCASH, J.P. and J.A. CAMPBELL. 1955. The effect of intermittent warm and cold periods on breaking the rest period of peach leaf buds. Proc. Amer. SOC. Hort. Sci. 66237-92. OWEN, J.H., W.M. POWELL, and F.F. HENDRIX, JR. 1965. Occurrence of peach tree decline in Georgia in 1965. Plant Dis. Rptr. 492359-860. OWENS, L.D. 1969. Toxins in plant disease: Structure and mode of action. Science 165:18-25. PACLT, J. 1972. Fundamental observations on the divergence of views on the origin and nature of premature dieback of apricot. Pol’nohodarstvo 18:824833. PANAGOPOULOS, C.G. and J.E. CROSSE. 1964. Frost injury as a predisposing factor in blossom blight of pear caused by Pseudomonas syringae van Hall. Nature 202:1352. PARKER, J. 1963. Cold resistance in woody plants. Bot. Rev. 29:123-201. PARKER, K.G. and W.F. MAI. 1956. Damage to tree fruits in New York by root lesion nematodes. Plant Dis. Rptr. 40:694-699. PARKER, K.G., W.F. MAI, G.H. OBERLY, K.D. BRASE, and K.D. HICKEY. 1966. Combating replant problems in orchards. Cornell Ext. Bul. 1169:l-19. PATRICK, Z.A. 1955. The peach replant problem in Ontario. 11. Toxic substances from microbial decomposition products of peach root residues. Can. J. Bot. 33:461-486. PAULECHOVA, K. and D. RAKUS. 1971. Study on the damaging effect of apple proliferation (English translation). Ochr. Rost. 7:39-46. PELLETT, H. 1971. Comparison of cold hardiness levels on root and stem tissues. Can. J. Plant Sci. 51:193-195.
106
HORTICULTURAL REVIEWS
PELLETT, N.E. 1973. Influence of nitrogen and phosphorus fertility on cold acclimation of roots and stems of two woody plants. J. Amer. SOC. Hort. Sci. 98:82-86. PEPIN, H.S., G.W.F. SEWELL, and J.F. WILSON. 1975. Soil populations of Thielaviopsis basicola associated with cherry rootstocks in relation to effects of the pathogen on their growth. Ann. Appl. Bid. 79:171-176. PETERSEN, D.H. 1961. The pathogenic relationship of Clitocybe tabescens to peach trees. Phytopathology 515319-823. PETERSEN, D.H. 1975. Bacterial canker of peach. p. 360-362. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. PETERSEN, D.H. and W.M. DOWLER. 1965. Bacterial canker of stone fruits in the southeastern states. Plant Dis. Rptr. 49:701-702. PIRINGER, A.A. and R.J. DOWNS. 1959. Responses of apple and peach trees to various photoperiods. Proc. Amer. SOC. Hort. Sci. 73:9-15. PITCHER, R.S., D.W. WAY, and B.M. SAVORY. 1966. Specific replant diseases of apple and cherry and their control by soil fuigation. J. Hort. Sci. 41:379-396. PLICH, M. 1976. Influence of growth regulators on the development of collar rot disease caused by the fungus Phytophthora cactorum in apple trees. Fruit Sci. Rpts. 3:33-42. POLLOCK, B.M. 1962. Temperature control of physiological dwarfing in peach seedlings. Plant Physiol. 37:190-197. POSNETTE, A.F. and R. CROPLEY. 1970. Decline and other effects of five virus infections on three varieties of plum (Prunus domestica L.). Ann. Appl. Bid. 65:lll-114. POTTER, J.F. 1924. Experiments on resistance of apple roots to low temperatures. New Hampshire Agr. Expt. Sta. Tech. Bul. 27. POWELL, W.M., J.H. OWEN, and W.A. CAMPBELL. 1965. Association of phycomycetous fungi with peach tree decline in Georgia. Plant Dis. Rptr. 49: 279-281. PRINCE, V.E. 1966. Winter injury to peach trees in central Georgia. Proc. Amer. SOC. Hort. Sci. 88:190-196. PRINCE, V.E., L. HAVIS, and L.E. SCOTT. 1955. Effect of soil treatments in a greenhouse study of the peach replant problem. Proc. Amer. SOC. Hort. Sci. 65:139-148. PRINCE, V.E. and B.D. HORTON. 1972. Influence of pruning a t various dates on peach tree mortality. J. Amer. SOC. Hort. Sci. 97:303-305. PROEBSTING, E.L. 1950. A case history of a “Peach Replant” situation. Proc. Amer. SOC. Hort. Sci. 56:46-48. PROEBSTING, E.L. and A.E. GILMORE. 1941. The relation of peach root toxicity to the re-establishing of peach orchards. Proc. Amer. SOC. Hort. Sci. 38:21-26.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
107
PROEBSTING, E.L., JR. 1961. Cold hardiness of Elberta peach fruit buds as influenced by nitrogen level and cover crops. Proc. Amer. Soc. Hort. Sci. 77:97-106. PROEBSTING, E.L., JR. 1963. The role of air temperature and bud development in determining cold hardiness of dormant peach fruit buds. Proc. Amer. Soc. Hort. Sci. 83:259-269. PROEBSTING, E.L., JR. 1970. Relation of fall and winter temperatures to flower bud behavior and wood hardiness of deciduous fruit trees. HortScience 5:422-424. PROEBSTING, E.L., JR. and H.H. MILLS. 1961. Loss of hardiness by peach fruit buds as related to their morphological development during the pre-bloom and bloom period. Proc. Amer. Soc. Hort. Sci. 78:104-110. PROEBSTING, E.L., JR. and H.H. MILLS. 1969. Effect of growth regulators on fruit bud hardiness in Prunus. HortScience 4:254-255. PROEBSTING, E.L., JR. and H.H. MILLS. 1974. Time of GA application determines hardiness response of ‘Bing’ cherry buds and wood. J. Amer. Soc. Hort. Sci. 99:464-466. PROEBSTING, E.L., JR., H.H. MILLS, and T.S. RUSSELL. 1966. A standardized temperature-survival curve for dormant Elberta peach fruit buds. Proc. Amer. Soc. Hort. Sci. 89:85-90. PRUNIER, J.P., L. GARDAN, and J. LUISETTI. 1970. Role of a bacterial flora in some forms of apricot decline (English translation). Ann. Phytopathol. 2:775. PRUNIER, J.P., J. LUISETTI, and L. GARDAN. 1970. Studies on bacterial diseases of fruit trees. I. A new bacterial disease of peach: Description, aetiology, development of the parasite (English translation). Ann. PhytopathoL 2:155-179. PRUNIER, J.P., J. LUISETTI, and L. GARDAN. 1973a. Studies on bacterial diseases of fruit trees. V. A study on pathogenicity of Pseudomonas mors-prunorum fsp. persicae, agent of bacterial decline of peach. Methodology: First results on the effect of inoculation date. (English translation). Ann. Phy topa thoI. 5 :327- 346. PRUNIER, J.P., J. LUISETTI, and L. GARDAN. 1973b. Studies on bacterial diseases of fruit trees. Chemical trials against bacterial decline of peach trees in France. Phytiatrie-Phytopharmacie 23:71-87. PSALLIDAS, P.G. and C.G. PANAGOPOULOS. 1975. A new bacteriosis of almond caused by Pseudomonas amygdali sp. nov. Ann. Inst. Phytopathol. Benaki 11:94-108. QUAMME, H.A., R.E.C. LAYNE, H.O. JACKSON, and G.A. SPEARMAN. 1975. An improved exotherm method for measuring cold hardiness of peach flower buds. HortScience 10:521-523. QUAMME, H.A., C.J. WEISER, and C. STUSHNOFF. 1973. The mechanism of freezing injury in xylem of winter apple twigs. Plant Physiol. 51973-277.
108
HORTICULTURAL REVIEWS
RAESE, ,J.T. 1977. Induction of cold hardiness in apple tree shoots with ethaphon, NAA, and growth retardants. J Amer. SOC.Hort. Sci. 102:789-792. RAESE, tJ.T., M.W. WILLIAMS, and H.D. BILLINGSLEY. 1977. Sorbitol and other carbohydrates in dormant apple shoots as influenced by controlled temperatures. Cryobiology 14:373-378. RALLO, L. 1973. Pear decline in plantations in the Valle del Ebro (English translation). Ann. Inst. Nacional Inuestig. Agrarias, Protec. Veget. 3:147205. RAWL, E.H. 1935. Peach tree abnormalities developing from applications of Hort. Sci. nitrogen fertilizers alone. A preliminary report. Proc. Amer. SOC. 33:293-298. REFATTI, E. 1970a. On the problem of apple decline in Valtellina (English translation). Rass. Econ. Prou. Sondrio 1970 (3/4):1-8. REFATTI, E. 1970b. Apple decline in Valtellina. 11. Study of the epidemiology and spread of the disease (English translation). Riu. Patol. Veg., Pauia Ser. IV 6:255-267. RHOADS, AS. 1954. Clitocybe root rot found widespread and destructive in Georgia and South Carolina peach orchards. P l a n t Dis. Rptr. 38:42-46. ROHDE, R.A. 1965. The nature of resistance in plants to nematodes. Phytopa t hol ogy 5 5 :1159 - 1162. ROHRBACH, K.G. and N.S. LUEPSCHEN. 1968. Seasonal changes in sugar alcohols and sugars in peach bark: A possible relationship to Cytospora canker susceptibility. Proc. Arner. Soc. Hort. Sci. 93:135-140. ROLLINS, H.A., F. HOWLETT, and F. EMMERT. 1962. Factors affecting apple hardiness and methods of measuring resistance of tissue to low temperature injury. Ohio State Dept. Agr. Res. Bul. 901. ROSENBERGER, D.A. and A.L. JONES. 1977. Seasonal variation in infectivity of inoculum from X-diseased peach and chokecherry plants. P l a n t Dis. Rp tr. 6 1:102 2 - 1024. ROSIK, J., J. KUBALA, M. STANOVA, and P. LACOK. 1971. Structural properties of apricot gum polysaccharides. IV. Observation on their changes during the vegetative cycle after gummosis evoked by pathogens. Bid. Bratisl. Ser. A 26:13-18. ROSS, R.G. and A.D. CROWE. 1973. Replant disease in apple orchard soil. Can. P l a n t Dis. Suru. 53:144-146. ROSS, R.G. and A.D. CROWE. 1976. Further studies on replant disease of apple in Nova Scotia. Can. P l a n t Dis. Suru. 56:88-92. ROWE, R.N. and D.V. BEARDSELL. 1973. Waterlogging of fruit trees. A review. Comrnonw. Bur. Hort. & Plant. Crops, Hort. Abstr. 43:533-548. ROWE, R.N. and P.B. CATLIN. 1971. Differential sensitivity to waterlogging and cyanogenesis by peach, apricot, and plum roots. J. Arner. SOC.Hort. Sci. 96 :305- 308. ROZSNYAY, D.S. and B. BARNA. 1974. Apoplexy of apricots. IV. Studies on the toxin production of Cytospora (Valsa) cincta Sacc. Acta Phytopathol. Acad. Sci. Hung. 9:301-310.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
109
ROZSNYAY, D.S. and Z. KLEMENT. 1973. Apoplexy of apricots. 11. Cytosporal die-back and the simultaneous infection of Pseudomonas syringae and Cytospora cincta on apricots. Acta Phytopathol. Acad. Sci. Hung. 8:57-69. RUBINSTEIN, B. and A. C. LEOPOLD. 1962. Effects of amino acids on bean leaf abscission. Plant Physiol. 37:398-401. RYAN, C.K.J. 1975a. Specific replant disease in Hawke’s Bay Part 111: Apple rootstock evaluation for replant sites. Orchardist New Zealand 48: 191- 193. RYAN, C.K.J. 1975b. Specific replant disease in Hawke’s Bay Part IV: Control methods including fumigation technique. Orchardist New Zealand 48:194195. SAKAI, A. 1961. Effect of polyhydric alcohols on frost hardiness in plants. Nu t u re 189 :416 - 4 17. SAKAI, A. 1966. Seasonal variation in the amounts of polyhydric alcohol and sugar in fruit trees. J. Hort. Sci. 41207-213. SAMISH, R.M. 1954. Dormancy in woody plants. Annu. Rev. P l a n t Physiol. 5:183-204. SAMISH, R.M. and S. LAVEE. 1962. The chilling requirement of fruit trees. Proc. 16th Intern. Hort. Congr., p. 372-388. SAMISH, R.M., S. LAVEE, and A. EREZ. 1967. A concept of dormancy of woody plants with special reference to the peach. Proc. 17th Intern. Hort. Congr. 3:397 -408. SANDS, D.C. and D.A. KOLLAS. 1974. Pear blast in Connecticut. P l a n t Dis. Rptr. 58:40-41. SANDS, D.C. and G.S. WALTON. 1975. Injections control peach diseases. Frontiers P1a n t Sci. 27:5 -6. SARASOLA, A.A. and C.A.S. DE BUSTAMANTE. 1970. New studies on pear decline and apple collar rot (English translation). Reuta Inuestnes Agrop Ser. 5, 7:47-75. SAUNIER, R. 1966. A method of determining the resistance of some fruit tree rootstocks to root asphyxiation (English translation). Ann. Amelior. Plant. 16:367-384. SAVAGE, E.F. 1970. Cold injury as related to cultural management and possible protective devices for dormant peach trees. HortScience 5:425-428. SAVAGE, E.F. 1972. Calcium deficiency-a factor in peach tree short life. Natl. Peach Counc. Proc. 31:109-112. SAVAGE, E.F. and F.F. COWART. 1942a. Factors affecting peach tree longevity in Georgia. Ga. Agr. Expt. Sta. Bul. 219. SAVAGE, E.F. and F.F. COWART. 1942b. The effects of pruning upon the root distribution of peach trees. Proc. Amer. SOC.Hort. Sci. 41:67-70. SAVAGE, E.F. and F.F. COWART. 1954. Factors affecting peach tree longevity in Georgia. Proc. Amer. Soc. Hort. Sci. 64:81-86. SAVAGE, E.F., R.A. HAYDEN, and W.E. WARD. 1968. The effect of subsoiling on the growth and yield of peach trees. Ga. Agr. Expt. Sta. Res. Bul. 30.
110
HORTIClJLTURAL REVIEWS
SAVAGE, E.F., J.H. WEINBERGER, E.S. LUTTRELL, and AS. RHOADS. 1953. Clitocybe root rot-a disease of economic importance in Georgia peach orchards. Plant Dis. Rptr. 37:269-270. SAVORY, B.M. 1966. Specific replant diseases, causing root necrosis and growth depression in perennial fruit and plantation crops. Research Rev. 1. Commonw. Bur. Hort. Plant. Crops, East Malling, Maidstone, Kent, England. SAVORY, B.M. 1967. Specific replant diseases of apple and cherry. Rpt. East Malling Res. Sta. (1966) p. 205-208. East Malling, England. SCARTH, G.W. 1944. Cell physiological studies of frost resistance. A review. New Phytologist 43:l- 12. SCHMID, G. 1974. Pear decline. Schweizer. Zeit. Obst-Weinbau 110:297301. SCHNEIDER, G.W. and A.C. MCCLUNG. 1957. Interrelationships of pruning, nitrogen rate, and time of N application in Halehaven peach. Proc. Amer. SOC. Hart. Sci. 69:141-147. SCOTT0 LA MASSESE, C., C. MARENAUD, and J. DUNEZ. 1973. Analysis of a decline phenomenon of peach trees in the Eyrieux valley (English translation). Compt. Rend. Sean. Acad. Agr. France 59:327-339. SEEMULLER, E. and L. KUNZE. 1972. Investigations on pear decline in southwestern Germany (English translation). Mitteil. Biol. Bundesan. L a n d Forstwirt. Berlin-Dahlem 144:47-70. SETLIFE, E.C. and E.K. WADE. 1973. Stereum purpureum associated with decline and death of apple trees in Wisconsin. Plant Dis. Rptr. 57:473-474. SEWELL, G.W.F. and J.F. WILSON. 1975. The role of Thielauiopsis basicola in the specific replant disorders of cherry and plum. Ann. Appl. Biol. 79:149169. SHANDILYA, T.R. 1974. A new canker and die-back disease of apple from Himachal Pradesh. Indian J. Mycol. Plant Puthol. 4:969-971. SHANNON, L.M. and E.G. CHRIST. 1954. Replanting peaches. Amer. Fruit Grower 74:5,14-15. SHARPE, R.H. 1974. Breeding peach rootstock for the southeastern United States. HortScience 9:362-363. SHARPE, R.H., C.O. HESSE, B.F. LOWNSBERY, V.G. PERRY, and C.J. HANSEN. 1969. Breeding peaches for root-knot nematode resistance. J. Amer. SOC.Hort. Sci. 94:209-212. SIMINOVITCH, D., B. RHEAUME, and R. SACHAR. 1967. Seasonal increase in protoplasm and metabolic capacity in tree cells during adaptation to freezing. Mol. Mech. Temp. Adapt., Amer. Assoc. Adu. Sci. Publ. 84:3-40. SIMINOVITCH, D., J. SINGH, and I.A. DE LE ROCHE. 1975. Studies on membranes in plant cells resistant to extreme freezing. I. Augmentation of phospholipids and membrane substance without changes in unsaturation of fatty acids during hardening of black locust bark. Cryobiology 12:144-153.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
111
SIMONS, R.K. 1970. Phloem tissue development in response to freeze injury to trunks of apple trees. J . Amer. SOC. Hort. Sci. 95:182-190. SITEPU, D. and H.R. WALLACE. 1974. Diagnosis of retarded growth in an apple orchard. Austral. J. Expt. Agr. & Animal Husb. 14:577-584. SLATER, C.H.W. and J.P. RUXTON. 1954. The effect of soil compaction on incidence of frost. (E 430) East Mall. Rpt. p. 88-91. East Malling, England. SMITH, P.R. and T.F. NEALES. 1977. The growth of young peach trees following infection by the viruses of peach rosette and decline diseases. Austral. J. Agr. Res. 28:441-444. SMITH, P.R., L.L. STUBBS, and D.I. CHALLEN. 1977a. Studies on the epidemiology of peach rosette and decline disease in Victoria. Austral. J . Agr. Res. 28:103-113. SMITH, P.R., L.L. STUBBS, and D.I. CHALLEN. 1977b. The detection of prune dwarf virus in peach trees affected with peach rosette and decline with Golden Queen peach as an indicator, and the distribution of the virus in affected trees. Austral. J . Agr. Res. 28:115-123. SMITH, S.H. and R.F. STOUFFER. 1975. Prunus stem pitting. p. 387-396. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. SMITH, S.H., R.F. STOUFFER, and D.M. SOULEN. 1973. Induction of stem pitting in peaches by mechanical inoculation with tomato ringspot virus. Phytopathology 63:1404-1406. SMITH, W.W. 1954. Occurrence of ‘stem pitting’ and necrosis in some body stocks for apple trees. Proc. Amer. SOC. Hort. Sci. 63:lOl-113. SOBERS, E.K. and C.P. SEYMOUR. 1967. Cylindrocladium floridanum spm. associated with decline of peach trees in Florida. Phytopathology 57:389393. SOMA, K. and H. SCHNEIDER. 1971. Developmental anatomy of major lateral leaf veins of healthy and of pear-decline diseased pear trees. Hilgardia 40:471-504. SPIVEY, C.D. and N.F. MCGLOHON. 1973. Peach tree decline. Coop. Ent. Serv., Univ. Ga. Agr. Coll., Athens, Ga. Bul. 714. ST. JOHN, J.B. and M.N. CHRISTIANSEN. 1976. Inhibition of linolenic acid synthesis and modification of chilling resistance in cotton seedlings. Plant Physiol. 57 :257 -259. STADELMANN, E.J. 1969. Permeability of the plant cell. Annu. Rev. Plant Physiol. 20:585-606. STANOVA, M. 1977. On the physiology and pathology of Cytospora cincta Sacc. Act. Inst. Bot., Acad. Sci. Slou., R e j 2. Biol. 203:217-227. STEINMETZ, F.H. and M.T. HILBORN. 1938. A histological evaluation of low temperature injury to apple trees. Maine Agr. Expt. Sta. Bul. 388. STENE, A.E. 1937. Pruning of winter injured peach trees. Proc. Amer. SOC. Hort. Sci. 35:147-150.
112
HORTICULTURAL REVIEWS
STEPONKUS, P.L. and F.O. LANPHEAR. 1967a. Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol. 42:1423-1426. STEPONKUS, P.L. and F.O. LANPHEAR. 1967b. Light stimulation of cold acclimation: Production of a translocatable promoter. Plant Physiol. 42: 1673-1679. STERGIOS, B.G. and G.S. HOWELL, JR. 1973. Evaluation of viability tests for cold stressed plants. J. Amer. SOC. Hort. Sci. 98:325-330. STOUFFER, R.F., K.D. HICKEY, and M.F. WELSH. 1977. Apple union necrosis and decline. Plant Dis. Rptr. 61:20-24. STROBEL, G.A. 1974. Phytotoxins produced by plant parasites. Annu. Reu. Plant Physiol. 25:541-566. STUART, N.W. 1937. Cold hardiness of some apple understocks and the reciprocal influence of stock and scion on hardiness. Proc. Amer. SOC. Hort. Sci. 35:386-389. STUART, N.W. 1939. Comparative cold hardiness of scion roots from fifty apple varieties. Proc. Amer. SOC. Hort. Sci. 37:330-334. STUART, N.W. 1941. Cold hardiness of Malling apple rootstock types as determined by freezing tests. Proc. Amer. SOC. Hort. Sci. 38:311-314. STUBBS, L.L. and P.R. SMITH. 1971. The association of Prunus necrotic ringspot, prune dwarf, and green sunken mottle viruses in the rosetting and decline disease of peach. Austral. J. Agr. Res. 22:771-785. STUSHNOFF, C. 1972. Breeding and selection methods for cold hardiness in deciduous fruit crops. HortScience 7:lO-13. STUSHNOFF, C. 1973. Breeding for cold hardiness. Horticulture 51:30-32. SUDDS, R.H. and R.S. MARSH. 1943. Winter injury to trunks of young apple trees in West Virginia following a fall application of nitrate of soda. Proc. Amer. SOC. Hort. Sci. 42:293-297. SWINGLE, C.F. 1932. The exosmosis method of determining injury as applied Hort. Sci. 29:380-383. to apple rootstock hardiness studies. Proc. Amer. SOC. TAYLOR, J. 1972. Contributions to the control of peach decline in Georgia orchards. Ga. Agr. Res. 14:3-7. TAYLOR, J., J.A. BIESBROCK, F.F. HENDRIX, JR., W.M. POWELL, J.W. DANIELL, and F.L. CROSBY. 1970. Peach tree decline in Georgia. Ga. Agr. Expt. Sta. Res. Bul. 77:l-45. TAYLORSON, R.B. and S.B. HENDRICKS. 1976. Aspects of dormancy in vascular plants. BioScience 26:95-101. THOMAS, F.B. and D.G. WHITE. 1950. Foliar analysis of four varieties of peach rootstocks grown a t high and low potassium levels. Proc. Amer. SOC. Hort. Sci. 55:56-60. THOMPSON, W.K., F.L. JONES, and D.G. NICHOLS. 1975. Effect of dormancy factors on the growth of vegetative buds of young apple trees. Austral. J. Agr. Res. 26:989-996.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
113
TSITSILASHVILI, O.K. 1977. Effect of K on the content of amino and organic acids in grape and on their liberation by the roots. Soviet Plant Physiol. 24:335-337. TUFTS, W.P. and L.H. DAY. 1934. Nematode resistance of certain deciduous fruit tree seedlings. Proc. Amer. Soc. Hort. Sci. 31:75-82. TUKEY, H.B., JR. 1970. The leaching of substances from plants. Annu. Reu. Plant Physiol. 21:305-324. UPSHALL, W.H. and G.N. RUHNKE. 1935. Growth of fruit tree stocks as influenced by a previous crop of peach trees. Sci. Agr. 16:16-20. VAN GUNDY, S.D., L.H. STOLZY, T.E. SZUSZKIEWICZ, and R.L. RACKHAM. 1962. Influence of oxygen supply on plant parasitic nematodes in soil. Phytopa thology 5 2 :6 28 -632. VEGIS, A. 1964. Dormancy in higher plants. Annu. Rev. Plant Physiol. 15: 185-224. VIGLIERCHIO, D.R. 1971. Nematodes and other pathogens in auxin-related plant-growth disorders. Bot. Rev. 37:l-19. VIGOUROUX, A., M. CONUS, and R. OLIVIER. 1972. Behavior of peach varieties to bacterial decline under conditions favourable for the disease (Pseudomonas mors-prunorum f s p . persicae) (English translation). Compt. Rend. Sean. Acad. Agr. France 58:1387-1391. WALKER, D.R. 1970. Growth substances in dormant fruit buds and seeds. HortScience 5:414-416. WALKER, D.R. and C.W. DONOHO, JR. 1959. Further studies of the effects of GA on breaking the rest period of young peach and apple trees. Proc. Amer. SOC. Hort. Sci. 74:87-92. WALTMAN, C.S. 1937. The effects of fall nitrogen fertilization on soluble nitrogen and phosphate phosphorus content of dormant peach twigs. Proc. Amer. Soc. Hort. Sci. 35:273-278. WARCUP, J.H. 1976. Studies on soil fumigation. IV. Effects on fungi. Soil Biol. Biochem. 8:261-266. WARD, G.M. and A.B. DURKEE. 1956. The peach replant problem in Ontario. 111. Amygdalin content of peach tree tissues. Can. J.Bot. 34:419-422. WAREING, P.F. and P.F. SAUNDERS. 1971. Hormones and dormancy. A n nu. Rev. Plant Physiol. 22:261-288. WAY, R.D. 1954. The effect of some cultural practices and of size of crop on the subsequent winter hardiness of apple trees. Proc. Amer. Soc. Hort. Sci. 63:163-166. WEAVER, D.J. 1971. Association of two Cylindrocladium species with “short life” of peach trees in Georgia. Phytopathology 61:1095-1096. WEAVER, D.J. 1974a. Effect of root injury on the invasion of peach roots by isolates of Clitocybe tabescens. Mycopathol. Mycol. Appl. 52:313-317. WEAVER, D.J. 1974b. A gummosis disease of peach trees caused by Botryosphaeria do thidea. Phytopa thology 65:1429- 1432.
114
HORTICULTLJRAL REVIEWS
WEAVER, D.J. and E.J. WEHUNT. 1975. Effect of soil p H on susceptibility of peach to Pseudomonas syringae. Phytopathology 65:984-989. WEAVER, D.J., E.J. WEHUNT, and W.M. DOWLER. 1974. Association of tree site, Pseudomonas syringae, Criconemoides xenoplax, and pruning date with short life of peach trees in Georgia. P l a n t Dis. Rptr. 58:76-79. WEAVER, G.M. 1963. Influence of rootstocks on susceptibility of peach to peach canker. Fruit Var. & Hort. Dig 17:43-44. WEHUNT, E.J. and .J.M. GOOD. 1975. Nematodes on peaches. p. 377-387. In N.F. Childers (ed.) The peach. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. WEINBERGER, J.H. 1949. Field notes on cold injury taken a t the USDA Hort. Field Station, Fort Valley, Ga. (unpublished). WEINBERGER, J.H. 1950a. Chilling requirement of peach varieties. Proc. Amer. Soc. Hort. Sci. 56:122-128. WEINBERGER, J.H. 1950b. Prolonged dormancy of peaches. Proc. Amer. SOC. Hort. Sci. 56:129-133. WEINBERGER, J.H. 1952. Winter injury to peach trees on Yunnan stock. P l a n t Dis. Rptr. 361307-308. WEINBERGER, J.H. 1967. Some temperature relations in natural breaking of the rest of peach flower buds in the San Joaquin Valley, California. Proc. Hort. Sci. 91534-89. Amer. SOC. WEINBERGER, J.H. 1969. The stimulation of dormant peach buds by a cytokinin. HortScience 4:125-126. WELSH, M.F. and L.P.S. SPANGELO. 1971. Necrotic stem pitting and decline, two bud-transmissable diseases affecting Malus robusta No. 5 apple rootstocks in British Columbia but not in Eastern Canada. Phytoprotection 52:58-67. WENSLEY, R.N. 1956. The peach replant problem in Ontario. IV. Fungi associated with replant failure and their importance in fumigated and nonfumigated soils. Can. J. Bot. 34:967-981. WENSLEY, R.N. 1966. Rate of healing and its relation to canker of peach. Can. J . P l a n t Sci. 46:251-264. WENSLEY, R.N. 1970. Innate resistance of peach to perennial canker. Can. J. P l a n t Sci. 50:339-343. WESTWOOD, M.N. 1970. Rootstock-scion relationships in hardiness of deciduous fruit trees. HortScience 5:418-421. WESTWOOD, M.N. 1976. Inheritance of pear decline resistance. Fruit Var. J. 30:63-64. WESTWOOD, M.N. and H.R. CAMERON. 1978. Environment-induced remission of pear decline symptoms. P l a n t Dis. Rptr. 62:176-179. WESTWOOD, M.N., H.R. CAMERON, P.B. LOMBARD, and C.B. CORDY. 1971. Effect of trunk and rootstock on decline, growth, and performance of Hort. Sci. 96:147-150. pear. J. Amer. SOC.
SHORT LIFE, REPLANT PROBLEMS OF DECIDUOUS FRUIT TREES
115
WESTWOOD, M.N., M.H. CHAPLIN, and A.N. ROBERTS. 1973. Effects of rootstock on growth, bloom, yield, maturity, and fruit quality of prune ( P r u n u s domestica L.). J Amer. Soc. Hort. Sci. 98:352-357. WESTWOOD, M.N. and P.B. LOMBARD. 1977. Pear rootstock and Pyrus research in Oregon. Acta Hort. 69:117-122. WHEELER, H. and H.H. LUKE. 1963. Microbial toxins in plant diseases. Annu. Reu. Microbiol. 17:223-242. WIEST, S.C., G.L. GOOD, and P.L. STEPONKUS. 1976. Evaluation of root viability following freezing by the release of ninhydrin-reactive compounds. HortScience 11:197-199. WILBUR, W., D.E. MUNNECKE, and E.F. DARLEY. 1972. Seasonal development of Armillaria root rot of peach as influenced by fungal isolates. Phytopa t hol ogy 62 :567-570. WILCOX, A.N. 1936. Material for the breeding of winter hardy pears. Proc. Amer. Soc. Hort. Sci. 34:13-15. WILDUNG, D.K., H.M. PELLETT, and C.J. WEISER. 1972a. The relationship of soil temperature and moisture to the hardening of apple roots. HortScience 7:335 (Abstr.). WILDUNG, D.K., H.M. PELLETT, and C.J. WEISER. 1972b. Factors influencing the cold hardiness of clonal apple rootstock. HortScience 7:335 (Abstr.). WILDUNG, D.K., C.J. WEISER, and H.M. PELLETT. 1973. Temperature and moisture effects on hardening of apple roots. HortScience 8:53-55. WILLIAMS, M.W. and J.T. RAESE. 1974. Sorbitol in tracheal sap of apple as related to temperature. Physiol. Plant. 30:49-52. WILNER, J. 1959. Note on an electrolytic procedure for differentiating between frost injury of roots and shoots in woody plants. Can. J. P l a n t Sci. 39:512-513. WILNER, J. 1960. Relative and absolute electrolytic conductance tests for frost hardiness of apple varieties. Can. J. P l a n t Sci. 40:630-637. WILNER, J. 1961. Relationship between certain methods and procedures of testing for winter injury of outdoor exposed shoots and roots of apple trees. Can. J P l a n t Sci. 41:309-315. WILNER, J. 1965. The influence of maternal parent on frost-hardiness of apple progenies. Can. J. P l a n t Sci. 45:67-71. WILNER, J., W. KALBFLEISH, and W.J. MASON. 1960. Note on two electrolytic methods and procedures of testing for winter injury of outdoor shoots and roots of apple trees. Can. J. P l a n t Sci. 40:563-565. WINKLEPLECK, R.L. and J.A. MCCLINTOCK. 1939. The relative cold resistance of some species of P r u n u s used as rootstocks. Proc. Amer. SOC. Hort. Sci. 3 7 :324-326. WINKLER, H. and G. OTTO. 1972. Investigations on the cause of replant disease in fruit trees. IV. Effect of various steaming temperatures on motile
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forms of nematodes in replant diseased soil. Zentralb. Bakteriol. Parasitenk., Infektionskrank. Hygiene 127:783-788. WOODBRIDGE, C.G. and A.M. LASHEEN. 1960. The nutrient status of normal and decline Bartlett pear trees in Yakima Valley in Washington. Proc. Amer. SOC.Hort. Sci. 75:93-99. YABLONSKII, E.A. 1975. Dynamics of phosphorus-containing substances and winter hardiness of amygdalaceous fruit cultures. Soviet Plant Physiol. 22: 88 1-886. YADAVA, U.L. and S.L. DOUD. 1977. Effect of exogenous phytohormones and rootstocks on budbreak and growth of peach ( P r u n u s persica (L.) Batsch). Proc. 4th Annu. Mtg. Plant Growth Reg. Work. Grp., Hot Springs, Ark., Aug. 9-11, 1977, p. 252-257. Plant Growth Regulator Working Group, Longmont, Colo. YADAVA, U.L. and S.L. DOUD. 1978a. Effect of peach seedling rootstocks and orchard sites on cold hardiness and survival of peach. J. Amer. SOC. Hort. Sci. 103:321-323. YADAVA, U.L. and S.L. DOUD. 1978b. Effect of rootstock on the bark thickness of peach scions. HortScience 13:538-539. YADAVA, U.L., S.L. DOUD, and D.J. WEAVER. 1978. Evaluation of different methods to assess cold hardiness of peach trees. J. Amer. SOC.Hort. Sci. 103 :3 18-3 2 1. YADAVA, U.L., S.L. DOUD, D.J. WEAVER, and J.H. EDWARDS. 1979. Evaluation of laboratory and field methods to assess cold hardiness and survival of peach trees under natural freezing conditions. J. Amer. SOC. Hort. Sci. (in press). YELENOSKY, G. 1975. Cold hardening in citrus stems. Plant Physiol. 56: 540-543. YOSHIDA, S . and A. SAKAI. 1974. Phospholipid degradation in frozen plant cells associated with freezing injury. Plant Physiol. 53:509-511. YOUNGSON, C.R., C.A.I. GORING, and R.L. NOVEROSKE. 1967. Laboratory and greenhouse studies on the application of fumazone in water to soil for control of nematodes. Down to Earth 23:27-32. ZEHR, E.I., R.W. MILLER, and F.H. SMITH. 1976. Soil fumigation and peach rootstocks for protection against peach tree short life. Phytopathology 6 6 :6 89 - 6 9 4.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
2 Seed Viability During Long-Term Storage L. N. Bass USDA-SEA-AR National Seed Storage Laboratory, Fort Collins, Colorado 80523 I. 11. 111. IV. V. VI.
Introduction 117 118 Effects of Species and Cultivar Effects of Production Conditions 119 Effects of Seed Maturity 119 Effects of Harvesting and Processing 123 Effects of Storage Environment 124 A. Seed Moisture Content 125 B. Temperature 132 C. Controlled Atmosphere Storage 134 VII. Changes During Storage 135 A. Biochemical Changes 135 B. Cytological Changes 135 VIII. Summary 136 IX. Literature Cited 137
I. INTRODUCTION The need to store seeds for long periods of time arose with the development of improved agricultural practices and plant breeding programs. In recent years, much research has been devoted to the storage requirements of various kinds of seeds. Justice and Bass (1978) reviewed in depth the research that had been conducted prior to 1973. Other recent reviews on seed storage include those by Bass (1973a1, Harrington (1972), and Roberts (1972). Therefore, this paper deals principally with more recent literature. For commercial purposes, seeds usually are not stored for more than one or two years, but even for such a short period special conditions are required to maintain viability in some climatic 117
118
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regions. For plant breeding purposes, small samples of many kinds of seeds must be preserved indefinitely, and maintaining viability requires a good knowledge of the storage requirements for each kind. 11. EFFECTS OF SPECIES AND CULTIVAR
Variations in seed longevity among species have been extensively documented. Harrington (1972) summarized the data available for species with (a) short-lived seeds and (b) seed longevity of ten years or more. Among the former are various aquatic, nut tree, and tropical species, and seed longevity varies widely. Some seeds may remain viable for only a few days or weeks, but others may remain viable for a few years. Many short-lived seeds cannot be dried to a low moisture content or be subjected to temperatures below freezing. Consequently, longevity of such seeds cannot be increased by conventional storage methods. However, seeds of some species which are short-lived under natural conditions can be stored for several years when carefully dried and stored under a low temperature and relative humidity or in a sealed moistureproof container . Long-lived seeds survive best under low temperature and low moisture storage conditions or in the soil under conditions unfavorable for germination. Seeds of some species have a long life under both conditions. Seeds of most temperate zone crops can be stored for more than ten years under conditions of low temperature and low relative humidity. Most seeds recorded as having survived for more than 100 years are of species which develop hard seeds. Because their seedcoats are impermeable to water, hard seeds do not fluctuate in moisture content with changes in atmospheric relative humidity as do seeds with permeable coats. Seeds of the following genera are known to have survived for 100 years or more (Harrington 1972): Albizia 147 years (Ramsbottom 1942), Cassia 158 years (Becquerel 1934), Goodia 105 years (Ewart 1908), and Trifoliurn 100 years (Youngman 1952). Seeds known to have survived for over 500 years are hard seeded. Examples include Canna (Anon. 19681, Lotus (Ohga 1923; Arnold and Libby 1951; Chaney 1951; Wester 1973), and Lupinus (Porsild et al. 1967). All have high percentages of hard seeds. Although barley does not have hard seeds, a sample survived 123 years of storage in a sealed glass tube at uncontrolled temperatures (Aufhammer and Simon 1957). Documentation of differences in seed longevity among cultivars of the same species is limited. ‘Oderbrucker’ barley seeds retained their viability during storage better than did seeds of other cultivars (Shands et al. 1967). Seeds of ‘Black Valentine’ bean stored better than did seeds of ‘Brittle Wax’ (Toole and Toole 1954).
SEED VIABILITY DURING LONG-TERM STORAGE
119
Seed longevity differed significantly among cultivars of bean, tomato, cucumber, pea, sweet corn, watermelon, and papaya (James et al. 1967; Bass 197313) (Table 2.1). Seeds of 27 muskmelon cultivars varied in their keeping quality within and among storage conditions over a 12-year period. Seeds of some genera retain their viability much longer than others during storage, and because of variations in keeping quality among cultivars (Table 2.1) germination of stored seeds must be monitored regularly. 111. EFFECTS OF PRODUCTION CONDITIONS Austin (1972) found no literature that related preharvest factors to the longevity of stored seeds. Weather probably is the most important production factor affecting seed quality. Rains just before harvest can cause wheat to sprout in the head (Moss et al. 1972) and cause delays in harvesting which create problems with seedborne fungi. Damp weather promotes the growth of fungi on seeds in the field. We have observed that seeds with a heavy mold population lose viability more rapidly during storage than seeds that are mold-free. Extremely dry conditions before harvest can cause seeds to be too dry, making them more susceptible to mechanical damage. Damaged seeds deteriorate more rapidly in storage than do undamaged seeds (Moore 1972). However, irrigation regime during production had little effect on bean seed longevity (Table 2.2). IV. EFFECTS OF SEED MATURITY
Seed maturity is the point in development a t which maximum dry weight is attained (Harrington 1972; Roberts 1972). Most plants flower and produce seeds over several days, weeks, or months; consequently, not all seeds on a plant mature a t the same time. Commercial seeds are harvested when the greatest yield of mature seeds can be obtained. Thus, each lot will contain both immature and mature seeds. Immature seeds usually do not store as well as mature seeds, and the viability of seeds left for some time on the plant before harvest may decline, depending upon weather conditions preceding harvest. Harvesting too soon results in excessive quantities of immature seeds, and harvesting too late results in decreased yield caused by shattering. Very few studies have addressed the question, “HOWwell do immature seeds store?” Most studies involving seed maturity have considered either yield or seedling vigor, not longevity in storage. Eguchi and Yamada (1958) harvested cabbage, carrot, Chinese cabbage, cucumber, edible burdock, eggplant, Japanese radish, pumpkin, tomato, watermel-
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TABLE 2.1. PERCENTAGE OF GERMINATION OF BEANS, PEAS, SWEET CORN, CUCUMBER, WATERMELON, TOMATO, AND PAPAYA SEEDS WHEN STORED AND AFTER 8 OR 9 YEARS' STORAGE AT 10°C AND 50% RH
Germination ("lo) Cultivar Tomato Bonny Best Break O'Day Clarks Special Early Crack Proof Dwarf Champion Earliana Garden State Improved GrothensGlobeStrain 2 Homestead 2 Indiana Baltimore Livingston's Globe Marglobe Moscow Oxheart Pearson Improved Pinkshipper Purdue 1361 Rutgers San Marzano Sioux Small Fruited Red Cherry Stone Sunray Urbana Valiant Wisconsin 55 ~
Bean Alabama 1 Black Valentine Blue Lake Blue Ribbon Pak Brittle Wax Contender Corneli 14 Commodore Imp. Dwarf Horticultural Ex tender Genuine Cornfield Golden Wax Topnotch Kentucky Wonder Kinghorn Wax Lazy Wife McCaslin Seminole Slendergreen Sulfur Tendergreen Tendergreen Improved Tennessee Green Pod Top Crop White Half Runner White Kentucky Wonder 191
Initial
9 Year
93 95 94 95 84 92 94 90 88 76 92 89 96 88 90 84 87 96 95
90 97 89
81 89 96 94 90 78 95 95 94 89 .~ 90 82 87 90 96
88 90 94
84 85 92
91 ._
Meanchange Range of change 99 94 79 94 85 99 84 90 93 99 97 75 97 98 80 96 89 98 91 96 98 97 90 96 89
98 90 74 97 79 99 79 78 91 93 94 86 95 92 79 70 93 89 77 91 90 94 80 93 77
Meanchange Range of change
Change % -3 +2 -5 -4 -3 -3 +2 +4 +2 +2 +3 +6 -2 +1 0 -2 0 -6 0 -2 -4 +1 -1 -5 -5 -2 -0.9 +6 to -6
-1 -4 -5 +3 -6 0 -5 -12 -2 -6 -3 +11 -2 -6 -1 -26
+4
-9 -14 -5 -8 -3 -10 -3 -12
-5 t11 to-26
SEED VIABILITY DURING LONG-TERM STORAGE
121
TABLE 2.1. (Continued)
Germination ("lo) Cultivar Peas Alaska Alderman Ameer American Wonder Bliss Everbearing Creole Dwarf Alderman Dwarf Grey Sugar Early Perfection First and Best Garden Alaska Glacier Gradus Improved Hundred Fold Laxton Progress Lincoln Little Marvel Laxtons Superb New Era Perfection Premier Pride ~ ~
.
~
Thomas Laxton Wando
.
Initial
9 Year
98 88 87 84 93 97 83 99 96 77 98 88 91 96 89 95 89 81 91 91 88 96 96 97
98 85 81 81 81 92 68 99 91 74 93 77 71 92 85 95 90 79 86 90 84 95 91 99
Mean change Range of change Sweet corn Calumet Country Gentleman Country Gentleman H brid Golden Bantam (8row7 Golden Cross Golden Early Market Golden Cross Bantam Goldrush Iochief Keystone Evergreen Hybrid Seneca Chief Spancross Superchief Sweetangold Tempo Barbecue
98 81 93 95 94 98 99 93 99 96 82 99 94 95 96 81
99 78 95 93 93 96 99 93 99 96 67 99 98 90 96 91
Mean change Range of change
Cucumber A&C Ashley Black Diamond Chinese Snake Crystal Apple Cubit Early Cluster Early Fortune
96 93 94
99 ..
95 93 99 94
95 91 92 95 83 95 97 91 ~~
Change % 0 -3 -6 -3 -12 -5 -15 0 -5 -3 -5 -11 -20 -4 -4 0 +1 -2 -5 -1 -4 -1 -5 +2 -4.6 +2 to -20 +1 -3 +2 -2 -1 -2 0 0
0 0 -15 0 +4 -5 0 +10 -0.7 +10 to-15 -1 -2 -2 -4 -12 +2 -2 -3
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TABLE 2.1. (Confinued)
Germination ( ( k ) Cultivar Improved Long Green Improved Long Green Special Long Japanese Climbing Lemon Marketer Model Niagra Ohio M.R. 17 Palomar Staysgreen Stone Straight Eight Vaughan West Indian Gerkin White Wonder Wisconsin SMR 12
Initial
9 Year
95 99 99 99 98 95 98 96 99 89 99 97 90 97 97 98
96 95 93 95 98 95 96 93 98 77 97 99 89 94 95 96
Mean change Range of change Watermelon Black Diamond Blacklee WR Blackstone Calhoun Sweet Charleston Grey Congo Dixie Queen Florida Giant Garrisonian Golden Honey Harris’ Earliest Irish Grey Kleckley’s Sweet 6 Klondike Striped 11 New Hampshire Midget Peacock WR-50 Purdue Hawkesbury Striped Klondike Blue Ribbon Sugar Baby Summit Tendersweet Tom Watson White Hope Chilean Black Seeded
94 95 84 99 86 93 87 90 82 89 93 95 97 92 56 89 95 95 98 96 92 96 96 91
94 90 75 92 84 90 86 82 85 81 94 91 93 96 51 81 95 89 98 84 91 94 89 90
Mean change Range of change Papaya PR 6-65 PR 7-65 PR 8-65 P R 9-65 PR 10-65 S 64
78 71 89 48 55 66
44 46 36 50 26 70
Mean change Range of change
Chanae % +1 -4 -6 -4 0 0 -2 -3 -1 -12 -2 +2 -1 -3 -2 -2
-2.6 +2to-12 0 -5 -9 -7 -2 -3 -1 -8 +3 -8 +1 -4 -4 +4 -5 -8 0 -6 0 -12 -1 -2 -7 -1 -3.5 +4 to -12 -34 -25 -53 +2 -29 +4 -23.5 4-4 to -53
SEED VIABILITY DURING LONG-TERM STORAGE
123
TABLE 2.2. PERCENTAGE OF GERMINATION OF WADE AND TOP CROP BEAN SEEDS PRODUCED UNDER FOUR IRRIGATION REGIMES, WHEN STORED AND AFTER 15 YEARS AT 5°C AND 40% RH
Germination (%I
Cultivar Wade
TopCrop
Irrigation Regime Wet Wet Wet Dry Dry Wet Dry Dry Wet Wet Dry Dry
Wet Dry Wet Dry
When Stored 93 93 93 93
After 15 Years 92 89 89 93 Mean change Range of change
94 94 93 93
92 92 92 90 Mean change Range of change
56 Change -1 -4
-4 0 -2 0 to -4 -2 -2
-1
-3 -2 - 1 to -3
on, and Welsh onion seeds a t three- to seven-day intervals, giving four to six stages of maturity over two or three years. For all kinds except Chinese cabbage, pumpkin, and tomato, mature seeds retained viability better than did immature seeds. The same was true for Kentucky bluegrass when both immature and mature seeds were stored under the same conditions (Bass 1965). After 93 months a t 2°C and 70% relative humidity (RH), mature seeds germinated 53%, immature seeds only 15%; a t 32°C and 15% RH, mature seeds germinated 81%and immature seeds 59%. When fruits of butternut squash were stored for several months, germination improved with time of storage of the fruits (Young 1949; Holmes 1953). However, the seeds were not stored after removal from the fruits. Van Staden (1978a) found that Protea neriifolia L. seeds were mature about seven months after fertilization. At that time, germination was 93%. Leaving the seeds in the influorescences longer resulted in decreased viability. Germination was 86% and 40% when harvested 1 and 5 months after maturity. For best quality, seeds generally should be harvested as soon as they reach full maturity. Because of the lack of uniform maturity within a field, seeds must be harvested when the best germination and yield can be obtained. Such seed should have the maximum storage potential under any given storage conditions. Austin (1972) discussed seed maturity and seed size jointly, as such seeds have the same problems in storage. V. EFFECTS OF HARVESTING AND PROCESSING
Harvesting practices can cause seeds to lose viability and vigor. Damage to seeds during harvest is influenced by factors such as seed size and
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HORTICULTURAL REVIEWS
shape, firmness of the seedcoat, difficulty of extraction from the head or pod, and seed moisture content. Seeds of grasses which are harvested with the glumes still surrounding the caryopsis or grain usually are not as subject to damage as are seeds with the glumes removed. Damage to seeds like peas and beans increases or decreases as seed and pod moisture increases or decreases. Very dry seeds damage easily. Some kinds of seeds such as corn are harvested a t a moisture content too high for safe storage and are promptly and carefully dried to a safe moisture content. Drying too slowly can permit heat accumulation, resulting in decreased viability. Drying too rapidly or a t too high a temperature can damage seeds and reduce storage life. Most horticultural seeds should not be dried a t a temperature above 38°C. Adequate movement of air through the seeds is essential whether drying is done by heated or unheated air (Justice and Bass 1978). Small samples of seeds can be dried by storage with CaClz or CaCo. Seed lots directly from the field usually contain varying amounts of extraneous materials such as pieces of leaves and stems, broken seeds, immature seeds, insect parts, and other materials which may have a high moisture content or moisture holding capacity. For longest seed life, such extraneous materials must be removed before storage (Justice and Bass 1978). Dry seeds damage easily with rough handling (Dorrell and Adams 1969). Therefore, cleaning equipment and handling procedures must be properly adjusted for each kind of seed.
VI. EFFECTS OF STORAGE ENVIRONMENT The effects of environmental factors on seed longevity are interrelated, and therefore difficult to discuss separately. Seed moisture content and storage temperature are the major environmental factors affecting the preservation of stored seed, with seed moisture content usually more critical than temperature (Owen 1956; Barton 1961; James 1967; Bass 1973a; Justice and Bass 1978). For most seeds that can be dried to a low moisture content without damage, the lower the moisture content and storage temperature, the longer the viability. The third major factor in seed survival is oxygen partial pressure. Literature on the effect of partial pressure of oxygen is not extensive, and data from some of the earlier work (Owen 1956; Roberts 1961; Touzard 1961) were contradictory. But later work (Roberts et al. 1967; Roberts and Abdalla 1968) has shown that the higher the oxygen concentration, the shorter the life span of seeds of most species studied.
SEED VIABILITY DURING LONG-TERM STORAGE
125
A. Seed Moisture Content Because earlier work has been thoroughly reviewed (Owen 1956; Barton 1961; James 1967; Kozlowski 1972; Roberts 1972; Heydecker 1973; Bass 1973a; Justice and Bass 1978), discussions here will be confined to more recent work. Some kinds of seeds cannot be dried to a low moisture content without loss of viability; others can be dried with a desiccant or by natural means but not with heated air; still others can be dried very rapidly without loss of viability. Most common crop seeds can be rapidly dried with heated air (Justice and Bass 1978). To illustrate the effect of drying method on seed viability, Japanese pear seeds dried to 3 to 5% moisture content in air or by silica gel showed no loss in germination as a result of drying; but vacuum dried seeds lost viability rapidly (Omura et al. 1978). Seed moisture content can be controlled by controlling the relative humidity of the storage area or by drying the seeds to the desired moisture content and storing them in sealed moistureproof containers (Harrington 1972; Bass 1973a; Justice and Bass 1978). Each kind of seed attains a moisture content in equilibrium with the relative humidity of the surrounding atmosphere. Seed equilibrium moisture content varies with both relative humidity and temperature (Table 2.3). Humidity control methods, drying methods, and protective packaging were reviewed by Justice and Bass (1978). Relative humidity in a seed storage facility is usually controlled by either a refrigeration-type or a desiccant-type dehumidifier. The refrigeration-type system takes the moisture out of the air as it passes over the cooling coil. With this type of system, the air is cooled to a temperature colder than that desired, then rewarmed, thereby reducing the RH. The desiccant-type humidity control system utilizes a liquid or solid desiccant to absorb moisture vapor from the air and later eject it from the room. Desiccant dehumidifiers usually use dry chemicals for small TABLE 2.3. EQUILIBRIUM MOISTURE CONTENT OF CRIMSON CLOVER SEEDS AT VARIOUS TEMPERATURES AND RELATIVE HUMIDITIES
Tem erature
RH
10
50
FC)
21
32
(%I ~~
70 90 50 I0 90 50 I0
Equilibrium Moisture (%)
9.4
12.5 14.0 8.7 14.1 17.6
1.7
9.4
126
HORTICULTURAL REVIEWS
systems and salt solutions for large systems. The dehumidifier incorporates one or two beds of granular silica gel or activated alumina. In a two-bed system, the air is circulated through one bed while the other is being dried out. In a rotary one-bed system, the air passes through part of the bed while the other part is being dried out (Justice and Bass 1978). Hermetically sealed metal cans and glass jars are impervious to moisture vapor and gases, as are containers made of some flexible materials. Studies carried out in our laboratory to determine the protective value of various heat-sealable materials indicated that only those materials which included a foil layer at least 0.35 mil thick provided moisture protection equivalent to that provided by a hermetically sealed metal can. For storage either in a moistureproof heat-sealable container (Bass and Clark 1974; Clark and Bass 1975) or a sealed metal can (Basset al. 1962, 1963a,b; Bass 1978; Bass and Stanwood 1978) seed moisture content must be low enough to be safe a t the highest temperature to which the seeds might be exposed. For example, 4% moisture content lettuce seeds which initially germinated 97%, germinated 85% after 19 years a t 21°C but declined to 0% at 32°C. In fact, seeds held a t 32°C germinated only 36% after just 8 years of storage. Seeds which contained 7% and 10% moisture lost all viability in less than one year a t 32°C but germinated 94% and 96%, respectively, after 19 years a t -12°C (Table 2.4). Not all seeds require the same moisture content a t a given temperature. Germination of 10% moisture content sorghum seeds was 91% when sealed. Germination was 43% after 5 years' and 0% after 8 years' storage a t 32"C, but was 59% after 16 years' storage a t 21°C (Bass and Stanwood 1978). Other kinds of seeds showed different responses. Therefore, one must know the maximum temperature to which the seeds will be exposed during storage and also the anticipated length of storage. Although there are lot and species differences in safe moisture content for sealed storage, most kinds of seeds which can be dried will retain their viability well for a t least 5 years a t temperatures as high as 21"C, provided their moisture content does not exceed 4 or 5%. Woodstock et al. (1976) found that freeze-dried onion, pepper, and parsley seeds retained their viability better than did seeds that were not freeze-dried when stored a t 40°C and 50°C. At 50°C, non freeze-dried seeds of onion, pepper, and parsley lost their viability in less than 3 to 6 months. Freeze-dried seeds of onion and parsley germinated 61% and 74%, respectively, after 12 months a t 50°C. Freeze-dried pepper seeds produced 77% abnormal seedlings and no normal seedlings. For seeds stored a t 21" to 25"C, only freeze-dried pepper seeds germinated significantly better than control seeds after 12 months' storage. Length of freeze-drying (one, two, or four days) had little effect on germination. However, moisture content when freezedried may have a significant effect on response. Seed moisture content
SEED VIABILITY DURING LONG-TERM STORAGE
127
TABLE 2.4. PERCENTAGE OF GERMINATION OF LETTUCE SEEDS STORED AT APPROXIMATELY 4, 7, AND 10% MOISTURE CONTENT AT FIVE TEMPERATURES IN SEALED METAL CANS
Temperature ("C) - 12 - 1
10
21 32
Seed Moisture (96) 4 7 10 4 7 10 4 7 10 4 7 10 4 7 10
Initial Germination (96) 97 97 95 97 97 95 97 97 95 97 97 95 97 97 95
Germination (%I Years in Storage
1 96 94 92 97 92 92 95 ~~
9.1 ..
91 94 94 11 92 0
0
4 96 95 93 94 97 94 93 94 .. 21 89 4 0 90 0 0 ~~
8 96 98 ~. 94 90 76 91 90 9.1 ..
0 90 0 0 36 0 0
19 93 94 96 93 1 18 90 0 0 85 0 0 0 0 0 ~~
may need to be reduced to 8 or 9% by conventional drying before seeds can be freeze-dried safely (Woodstock et al. 1976). Seeds from the study reported by Woodstock et al. (1976) were stored in the National Seed Storage Laboratory a t 21", -12", and -70°C with only minor differences in germination of the freeze-dried and the non freeze-dried seeds after 6 years in storage (unpublished data). Seeds of Cheiranthus cheiri L. (wallflower), Vinca rosea L., and Salvia splendens F. Sellow ex Roem. and Schult. (scarlet sage) retained viability best a t a high relative humidity and low temperature and lost it most rapidly a t a low relative humidity (Nakamura 1975). Resistance to excessive drying varied among species. In vegetables, pea (Pisum sativum LJ, garden bean (Phaseolus uulgaris LJ, and broad bean (Vicia faba L.), and in flowers, pansy (Viola tricolor LJ, California poppy (Eschscholzia California Cham.), and Mexican firebush (Euphorbia heterophylla L.) showed least resistance to excess drying (Nakamura 1975). Perilla (Perilla acymaides L. var. crispa Benth) seeds, known to be short-lived, lost viability very rapidly when dried to 2.1% moisture content. Both controlled seed moisture content and a low temperature were required for maximum storage life of perilla seeds. Wallflower seeds stored open a t 5°C had 20% higher germination after 6 years' storage than seeds stored a t 5°C and room temperature (20" to 30°C summer and 3" to 8°C winter) sealed with CaClz and 60% higher than seeds sealed with CaO a t room temperature. Germination of Vinca rosea L. seeds stored 6 years open a t 5°C was 17% higher than for seeds sealed over CaClz and 13% and 81%
128
HORTICULTURAL REVIEWS
higher than for seeds a t room temperature sealed over CaC12 and CaO, respectively (Nakamura 1975). Germination of scarlet sage seeds stored 6 years open a t 5°C was 19% higher than that of seeds sealed over CaClz.Seeds sealed over CaO germinated 4% after 2 years a t room temperature (Nakamura 1975). Lettuce seeds stored a t room temperature sealed over CaClz (6.3% moisture content) germinated 91% after 9 years, but only 2.5% after 15 years; but seeds sealed over CaO (2.5% moisture content) germinated over 40% after 20 years. The difference in longevity between lettuce seeds sealed over CaClz and CaO apparently resulted from the difference in seed moisture content (Nakamura 1975). At room temperature, edible burdock (Arctiurn lappa L.) seeds sealed over CaClz and CaO germinated about the same percentage after 9 years; but after 15 years, the seeds over CaO germinated 26% and those over CaC12 germinated 6%. Welsh onion seeds stored 15 years a t room temperature sealed over CaO had 2.6 to 3.1% moisture content and germinated 52 to 54%, whereas seeds sealed over CaClz had 5.9 to 6.9% moisture content and germinated 1%(Nakamura 1975). Carrot, Chinese cabbage, cucumber, spinach, and eggplant seeds stored a t room temperature retained their viability longer when sealed over CaC12 than when sealed over CaO. Carrot seeds sealed over CaO lost viability in less than 10 years, but seeds sealed over CaClz lost only about half their initial viability during 2 1 years' storage a t room temperature. When stored a t room temperature sealed over CaClz, Chinese cabbage seeds had declined from 92.5 to 39.5% after 17 years, but seeds sealed over CaO failed to germinate after 17 years (Nakamura 1975). At room temperature, cucumber seeds sealed over CaClz declined 6% in viability after 2 1 years, but seeds sealed over CaO declined 86%. Spinach seeds declined from 82.5 to 56% germination during 17 years' storage a t room temperature, but viability of seeds sealed over CaO declined from 82.5 to 4%. Eggplant seeds stored 21 years a t room temperature declined in viability only 11%when sealed over CaClz but declined 81% when sealed over CaO. Radish, pepper, and squash seeds retained their viability better when sealed over CaClz than when sealed over CaO and stored a t room temperature (Nakamura 1975). Powell and Mathews (1976) reported that pea seeds stored under both warm, humid (25"C/93% RH) and cool, extremely dry (lO"C/l% RH) conditions showed deteriorative changes after 6 weeks, although little or no loss of viability had occurred. At 25°C and 93% RH, viability began to decline after 6 weeks, but a t 45°C and 94% RH, viability began to decline after 2 days. Rate of loss of viability was closely associated with seed moisture content. Moisture content of seeds a t 25°C and 93% RH increased from 10.4 to 22.7% in 15 weeks, but that of seeds a t 10°C and 1%
SEED VIABILITY DURING LONG-TERM STORAGE
129
R H decreased from 10.4 to 5.7% during the same period. The high moisture content seeds lost viability rapidly, while the low moisture content seeds retained their viability . Arumugam and Shanmugavelu (1977) reported that the germination of papaya seeds declined during storage when sealed in glass bottles with either CaO or silica gel, but 9.5 to 10.1% moisture content seeds retained good viability for 9 months when sealed in glass bottles without a desiccant. The reductions in viability observed for seeds sealed with the desiccants apparently resulted from excessive drying. Bass (1975) found that papaya seeds retained their viability well when seed moisture content was in equilibrium with 10°C and 50% RH whether stored a t 10°C and 50% R H or sealed in containers made of a heat-sealable material with a good foil layer in the lamination and stored a t 5°C. After 6 years of storage, seeds at 5°C in the heat-sealable containers germinated 3% higher than the seeds stored a t 10°C and 50% RH. Van Staden (197813) reported that 98.7% of Protea neriifolia seeds harvested a t 8%moisture content germinated in 20 days. Germination of seeds stored 3 years in cloth bags a t 20°C and 26°C (7.54% and 6.89% moisture) was 54.3% and 38.7%, respectively. Seeds stored 3 years under nitrogen in sealed glass containers a t 20°C (6.1% moisture) germinated 96.3%. Seeds in plastic bags a t 5°C and -10°C contained 6% and 8% moisture and germinated 97.7% and 96.3%, respectively. Days from planting to start of germination increased with increased storage in cloth bags a t 20°C and 26°C. No delay in germination was observed for seeds stored a t 5°C and -10°C and a t 20°C in nitrogen. The delay in start of germination was accompanied by a decrease in germination percentage. Honjo and Nakagawa (1978) found that seeds of Citrus grandis (L.) Osbeck, C. otachibana Hort. ex Y Tanaka, C. sulcata Hort. ex Takahashi, C. natsudaidai Hayata, C. iyo Hort. ex Tanaka, and C. tamurana Hort. ex Tanaka remained fully viable a t seed moisture contents above 20%. Seeds of trifoliate orange (Poncirus trifoliata [L.] Rafin.) fluctuated in germination a t seed moisture contents above 20%, but no seeds with less than 20% moisture content germinated. To evaluate the tolerance of citrus seeds to cold temperatures, seeds of C. natsudaidai with 54%, 31%, 23%, and 17% moisture content were stored a t 4", l o ,- lo , -3", and -5°C. Seeds with 31% and 54% moisture content retained good viability for 3 years a t 4°C. At l o , -lo, -3", and -5"C, a t all seed moistures, and a t 4°C and 23% and 17% moisture content, the rate of viability decline was variable. In a second storage experiment, seeds a t 29%, 39%, and 54% moisture content retained good viability for 2 years a t 4°C. Seeds a t 1°C and -1°C and with 34% and 23% moisture content showed variable rates of deterioration. It was concluded that for long storage C. natsudaidai seeds should have a moisture content above 30% and be held a t 4°C.
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According to Kotobuki (1978), seeds of Japanese persimmon (Diospyros kaki L.f.) do not tolerate drying. Regardless of the rapidity or the method of drying, seeds with the same moisture content showed the same germination percentage. At seed moisture contents above 30% germination was above 90%, but as seed moisture was reduced to below 30%, germination declined, until a t about 10% seed moisture few seeds germinated. Japanese persimmon seeds with 42.7% and 51% moisture content retained their initial viability for 18 months when stored a t 0°C. Seeds with 31.9% moisture showed a sharp decline in germination during the first 6 months of storage a t 0°C with little additional decline in viability during the next 12 months. Storage of seeds a t relative humidities between 65% and 90% provides seed moisture contents favorable for the growth of storage fungimainly a few group species of Aspergillus and Penicillium (Justice and Bass 1978). Some authorities on seed storage and seed health question whether storage fungi are ever the primary cause of loss of viability of seeds. However, Christensen (1973) reported that seeds of pea, barley, corn, and wheat stored a t moisture contents and temperatures favorable for the growth of storage fungi germinated 95% or higher after several months of storage if kept free of fungi; but germination of seeds inoculated with storage fungi was reduced to near zero during the same period. For many kinds of seeds, seed moisture contents in equilibrium with various relative humidities have not been determined, and consequently moisture contents a t which seeds are likely to be invaded by storage fungi are not known. Christensen (1973) has reviewed the literature on the effects of fungi on stored seeds. Storage fungi can be controlled best by storing seeds under conditions unfavorable for the growth of such fungi. T h e optimum temperature for growth of most storage fungi is about 30" to 33"C, the maximum about 50" to 55"C, and the minimum 0" to 5°C. A few Penicillium species found on seeds can grow a t temperatures as low as -5°C. For best control of storage fungi, seeds should not be stored a t temperatures above 30°C and relative humidities above 65%. Respiration of insects may cause accumulations of moisture which could encourage the growth of fungi, transmit fungi from seed to seed, and generate enough heat to affect seed viability (Howe 1973). Insects can be controlled by chemicals or by storage in insect-proof containers. Insecticides do not damage dry seeds, but some damage moist seeds. For long-term storage of germplasm, insects are no problem when seeds are stored a t subfreezing temperatures. Seed lots of a given kind, variety, chronological age, and germination do not all maintain their viability equally well in storage under identical conditions. Delouche and Baskin (1973), in an attempt to predict dif-
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ferences in seed storage life, developed the accelerated aging test, which measures physiological differences among seed lots which are not evident from the results of standard germination tests. Seeds were stored for short periods (2 to 8 days) under conditions known to promote deterioration-40" to 45°C and 100% R H for most species, but for some species 30°C and 75% RH was better. Seed lots which declined in viability most rapidly under these conditions had the poorest storage potential. Use of the accelerated aging test is beneficial to the seedsman in determining which seed lots can be carried over to the next planting season and which seed lots should be sold first. Delouche et al. (1973) reported that high quality bean, lettuce, onion, radish, and watermelon seeds showed little or no deterioration during 2Y2 years' storage a t 45% R H and 7°C. Similar seeds stored a t 75% R H and 30°C lost their viability in less than one year. At ambient conditions (Mississippi State, Mississippi) radish, bean, and watermelon seeds germinated 9596, 90%, and 86%, respectively, after 2% years, lettuce 68% after 1%years, and onion 42% after one year of storage. Delouche et al. (1973) reviewed the literature on storage of seeds in tropical and subtropical regions. They noted that for short-term storage (1 to 9 months) seeds should be stored a t 30°C and 50% RH, 20°C and 60% RH, or comparable conditions. For storage up to 18 months, they recommended a 10% decrease in the relative humidities listed above and other comparable temperature/RH combinations, such as 10°C and 60% RH. For long-term storage, R H should be 45% a t 10°Cand 30 to 40% a t 0" to -5°C. Most research has been on the storage of dry seeds, but Villiers (1974) studied storage of fully imbibed seeds as well as dry seeds. Fully imbibed lettuce and Fraxinus americana (L.) seeds retained good viability a t 30°C and 22"C, respectively, while the rate of viability loss in dry stored seeds increased with increased seed moisture content and storage time. Villiers and Edgcumbe (1975) stored seeds of lettuce cultivars 'Big Boston', 'Arctic King', and 'Grand Rapids' a t a range of moisture contents and fully imbibed in contact with liquid water. As the moisture content of the seeds not in contact with the liquid water increased, storage life decreased. Fully imbibed seeds held a t 30°C lost no viability in 1 2 months as long as they remained in contact with liquid water. Increased numbers of seedling abnormalities, including stunted roots and shoots, distorted cotyledons with necrotic areas, subdivided first leaves, swollen roots, and necrotic radicle meristems, were observed with increased time in dry storage. Plants from seeds stored fully imbibed a t 30°C for over 18 months appeared normal, grew vigorously, and produced normal, high-germinating seeds which produced a second generation crop of normal, vigorous seeds.
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Seeds of ‘Oswego’, ‘Fulton’, ‘Imperial 44’, ‘Imperial 846’, and ‘Imperial 847’ lettuce retained viability well a t -12°C and 70% R H for 1 4 years, but a t 5°C and 40% RH produced almost no normal seedlings after the same period of storage (Bass, unpublished data).
B. Temperature Storage temperature is the second most important factor in determining seed longevity. At temperatures above freezing, seed storage life decreases as temperature increases. The response of seeds to temperatures below freezing has not been fully documented. Owen (1956), Barton (1961); Roberts (19721, Harrington (1972), Bass (1973a), and Justice and Bass (1978) reviewed the literature on effects of storage temperature on seed longevity. Temperatures between 5°C and -29°C were reported to be satisfactory for medium to long-term seed storage with temperatures below -5°C preferable. Kretschmer (1976) found that after 4 years’ storage a t 10” to 3OoC, 5°C or -18°C lettuce seeds germinated over 90%. He concluded that for best results lettuce seeds should be stored with a low water content in water vapor-tight polyethylene bags. Temperatures near -18°C and 5% moisture content are recommended for long-term storage of seeds for germplasm preservation. (IBPGR 1976). In recent years, considerable emphasis has been placed on storage of seeds a t subfreezing temperatures, especially -196°C. Sakai and Noshiro (1975) investigated factors contributing to the survival of seeds cooled to the temperature of liquid nitrogen. They found that as a safe, general practice, seeds should be dried to 8 to 15% moisture content, be enclosed in an aluminum foil or an aluminum or plastic vessel with a screw cap, and the container be immersed directly into LN2. After storage, the containers should be rewarmed at 0°C or room temperature. Onion seeds a t 4% and 16% moisture content in sealed glass vials showed no decline in germination or yield after 3.75 years of storage a t -196°C and -20°C (Harrison and Carpenter 1977). Seeds of Anemone coronaria L., Antirrhinum majus L., Asparagus officinalis L., Lactuca sativa L., Pastinaca sativa L., Phaseolus vulgaris L., Pisum sativum L., Primula sinensis Sab. ex Lindl., Raphanus sativus L., and Zea mays L. also showed no reduction in viability after a few months’ storage a t -196°C. Stanwood and Bass (1978) reported that a t moisture contents below 13% (wet-weight) seeds of 42 commonly cultivated species showed no decline in viability after cooling to -196°C. In studies with seeds below 8% moisture content, no damage was observed from cooling to -196°C and rewarming, except for soybean, for which optimum moisture content
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for slow rewarming was 14.6% and for fast rewarming was 15.8% (Sakai and Noshiro 1975). Lettuce seeds with 5 to 13% moisture content were not injured by cooling to -196"C, but seeds with 13 to 16% moisture content were injured when cooled below -40°C (Stanwood et al. 1978). Cassava seeds with 6.34% moisture showed no detrimental effects of freezing in the vapor above LN2, but freezing in LN2 resulted in decreased germination. Seeds with 2% moisture frozen in LN2 shattered upon thawing (Mumford and Grout 1978). Junttila and Stushnoff (1978), Stushnoff and Junttila (1978), and Mumford and Grout (1978) found that hydrated lettuce seeds avoid injury by super-cooling. Super-cooling as an avoidance mechanism depends upon the intact structure of the endosperm. Th; degree of resistance to low temperature was related to the degree of hydration in the 20 to 40% moisture range, and the killing point was detectable by differential thermal analysis. No exotherms were detected for seeds with less than 16% moisture, but 2 types of exotherms were found in seeds containing more than 20% moisture. The first exotherm, which appeared as a single peak a t -10" f 2"C, was not related to the injury of intact seeds, but the second exotherm, which was linearly correlated with seed moisture content within the limits of 20 to 40%, represented the killing point of individual seeds. For seeds between 40% and 50% moisture content, the exotherm was -16 f 2°C. When the endosperm was disrupted the secondary isotherm disappeared, and the first isotherm represented the killing temperature. Extremely rapid freezing rates of 80", 110", and 240°C per hour shifted the free water peak slightly but did not change the secondary peaks (Stushnoff and Junttila 1978). Lettuce seeds with seed moisture levels up to 28.3% survived a freezing rate of 4°C per hour but not 40°C per hour prior to storage at -20°C for 28 days. At 21.8% moisture, freezing rate was not a factor, and high survival also occurred a t 40°C per hour. Lettuce seeds with 47.3% moisture did not tolerate one day a t -20°C (Stushnoff and Junttila 1978). Stanwood et al. (1978) reported that no freeze damage was observed in seeds with 13.9% moisture or lower when cooled to 5", -lo,-18", -70", or -196°C. Damage was observed in 19.7% moisture seeds cooled to -70" or -196°C. Japanese pear seeds slowly dried to less than 10% moisture content showed no loss of germination when subjected to temperatures of 0", -lo", -25", and -196°C for 48 hours. Seeds a t 55% moisture content lost viability a t temperatures lower than 0°C. Seeds at 11.7% moisture lost all viability in less than one year a t room temperature, but seeds a t 4.3% moisture retained their full initial viability for 3 years. Both 11.7% and 4.3% moisture content seeds stored a t -20°C and -196°C showed no loss
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of viability during 3 years' storage. Several months of low temperature stratification were required for germination of dried stored seeds (Omura et al. 1978). Storage of cucumber seeds a t -196°C for 2 years did not decrease viability, but storage a t -20°C reduced viability somewhat (Fedosenko and Yuldasheva 1976).
C. Controlled Atmosphere Storage Bass (1973a) and Justice and Bass (1978) comprehensively reviewed the literature on controlled atmosphere storage of seeds. They found the reported results to be variable and in some instances contradictory, probably because of widely divergent test procedures. Some workers controlled either storage temperature or seed moisture content, and others controlled neither. Some workers used air-dry seeds and room temperature, which provided very little information about the conditions actually used. Air-dry moisture content and room temperature vary with the kind of seed, time of year, geographic location, and kind of building. To accurately assess the value of either a partial vacuum or a gas in prolonging seed storage life, all environmental conditions must be considered. Under certain circumstances, some kinds of seeds are benefited by storage under a partial vacuum or gas such as COz or N,. But what are those circumstances? In an effort to understand more fully the interrelationships involved, we initiated a study to evaluate the effects of seed moisture content, storage temperature, and surrounding atmosphere on seed longevity. Seeds of crimson clover, lettuce, safflower, sesame, and sorghum were conditioned to 4, 7, or 10% moisture content and sealed in metal cans with atmospheres of air, carbon dioxide, nitrogen, helium, argon, or a partial vacuum (51 f 1 mm mercury) and stored a t temperatures of -12", -lo, lo", 21", or 32°C (Bass et al. 1962, 1963a,b). After 16 years' storage there were no significant differences in germination among the atmospheres for sorghum seeds a t the respective moistures and temperatures (Bass and Stanwood 1978). Similar results were obtained for crimson clover (Bass 1978), lettuce, safflower, and sesame seeds (unpublished data) except that lettuce seeds with 7% moisture content sealed in air a t temperatures of -1°C and warmer lost viability more rapidly than did the seeds in the other atmospheres or a partial vacuum. After 1 9 years' storage, 7% moisture content lettuce seeds sealed in air germinated 1% compared to 96%, 94%, 89%, 92%, and 94% for seeds sealed in a partial vacuum, carbon dioxide, nitrogen, helium, and argon, respectively (Bass, unpublished data). Even with these comprehensive studies we still do not know the ultimate value of controlled atmosphere storage of seeds. The benefits of such storage, if any, may be for very long storage, and then only for
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certain kinds of seeds stored at specific seed moistures and storage temperatures. For most situations, the added expense of using an atmosphere other than air appears to be unnecessary. VII. CHANGES DURING STORAGE A. Biochemical Changes Seed storage begins when seeds reach full maturity, regardless of where or how they are held. Biochemical changes occur in all parts of the seed both during and after maturation. Although much has been written about biochemical changes associated with deterioration, our knowledge of these processes is still incomplete. Abdul-Baki and Anderson (1972) and Roberts (1972) have thoroughly reviewed the literature. Attempts have been made to correlate such factors as increased fat acidity, increased enzyme activity, depletion of food reserves, and changes in membrane permeability with deterioration. Villiers (1973, 1974) and Villiers and Edgcumbe (1975) proposed that deterioration in dry-stored seeds results from the lack of operable systems to repair and replace organelles. When lettuce seeds were stored fully imbibed in contact with liquid water a t temperatures which promote rapid deterioration of dry seeds, no deterioration occurred. The number of abnormal seedlings in dry-stored seeds increased with increased time in storage. When dry seeds which showed considerable deterioration were imbibed and stored in liquid water, no further deterioration occurred. This suggests that repair mechanisms are operable in fully imbibed seeds and not in dry seeds. Consequently, any repair in dry-stored seeds must occur after the seeds are imbibed during the germination process.
B. Cytological Changes Cytological changes in the form of chromosomal aberrations occur in seeds of numerous crop and native plants, such as Antirrhinum, Crepis, Datura, Nicotiana, Hordeum, Vicia, Zea, Allium, Pisum, Secale, Beta, and Triticum spp. Kolotenkov (1974) reported that the frequency of mutations in Pisum sativum seeds was doubled while the frequency of chlorophyll mutations was increased from 0.5 to 5.8% by soaking the seeds in water for 6 to 12 hours, followed by thorough drying before planting. Seeds soaked and planted immediately were not affected. Villiers (1974) and Villiers and Edgcumbe (1975) found that an increase in moisture content of seeds of Lactuca sativa L. and Fraxinus americana L. in dry storage caused an increase in the rate of accumula-
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tion of chromosome aberrations. Storage of fully imbibed seeds in water allowed a very low incidence of chromosome aberrations to be maintained. Seedlings grown from dry-stored seeds showed increased morphological abnormalities with increased time in storage, while those from imbibed stored seeds appeared normal. Villiers and Edgcumbe (1975) found that radiation damage in irradiated lettuce seeds decreased with time when stored fully imbibed, but increased when stored dry. Floris and Anguillesi (1974) found that when the embryos and endosperms of wheat seeds were aged separately, each produced mutagenic substances which induced nuclear damage in the radicle meristem. The nuclear damage observed in isolated embryos did not differ from that observed in intact seeds. Isolated aged endosperm induced some chromosome damage in young embryos but did not increase the aberrations in isolated aged embryos. Orlova and Nikitina (1972) studied the timing of the appearance of chromosome aberrations during storage of Welsh onion seeds. With the passage of time in storage under room conditions and a t 50°C and 75% RH the number of single bridges and fragments decreased as did the total number of all types of rearrangements. They concluded that chromosome changes in fresh seeds occur a t the moment of germination and can be partially removed by the action of a protective substance. In aged seeds, part of the chromosome damage occurred in dormant seeds and appeared to be irreversible. In later studies (Orlova et al. 1976) a decrease in the mitotic potential of Welsh onion seeds was observed during aging. Orlova and Ezhova (1976) reported that when a DNA inhibitor was applied to young and old Welsh onion seeds, an equivalent increase in chromosome aberrations occurred. They concluded that automutagens capable of inducing potential chromosome changes accumulated during aging of the seeds. In aged pea seeds, the occurrence of first mitosis was delayed with increased time in storage and occurred when root length was about 4 mm in seeds stored 4 days and 4.8 mm in seeds stored 14 days a t 38°C with 18% moisture content. Disturbance of cell divisions by seed aging appears to be a factor in the induction of chromosomal aberrations (Roos, unpublished data).
VIII. SUMMARY Within families and genera, differences in seed longevity have been demonstrated among species and among cultivars. Production conditions, maturity a t harvest, and harvesting and processing conditions affect seed longevity. The more critical factors affecting seed longevity are seed moisture content and storage temperature. For maximum longevity seeds must be
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stored dry a t a low temperature. Many kinds of seeds can be dried by heated air but some cannot. Storage with CaC12 or CaO also extends storage life; however, some kinds of seeds live longer with CaClz than with CaO, and others live longer stored with CaO than with CaClZ.Most seeds that can be dried live longer a t subfreezing temperatures than a t above-freezing temperatures. A temperature of 10°Cor lower will prolong seed life. Within limits, the lower the temperature and seed moisture content, the longer seeds will remain viable. Hermetic storage can increase seed storage life provided seed moisture content is sufficiently low when the seeds are sealed. Storage in an a t mosphere other than air offers no advantage except for very long storage of a few kinds of seeds. Results of recent investigations suggest that cryogenic (-196°C) storage may extend the longevity of seeds more than conventional storage does. Cryogenic storage, through stoppage of all metabolic activity and biochemical changes, may also prevent the development of chromosomal aberrations which have been shown to occur during storage by conventional methods. IX. LITERATURE CITED ABDUL-BAKI, A.A. and J.D. ANDERSON. 1972. Physiological and biochemical deterioration of seeds. p. 283-315. In T.T. Kozlowski (ed.) Seed biology, vol. 2. Academic Press, New York. ANON. 1968. 550-year old seed sprouts. Sci. News 94:367. ARNOLD, J.R. and W.F. LIBBY. 1951. Radiocarbon dates. Science 113:lll120. ARUMUGAM, S. and K.G. SHANMUGAVELU. 1977. Studies on the viability of papaya seeds under different environments. Seed Res. 5(1):23-31. AUFHAMMER, G. and U. SIMON. 1957. Die samen landwirtshaftlicher kulturpflanzen im grundstein des chamaligen nurnberger stadttheaters und ihre keimfahigkeit. Ztschr. f. Acker- u. Pflanzenbau. 103:454-472. AUSTIN, R.B. 1972. Effects of environment before harvesting on viability. p. 114-149. I n E. H. Roberts (ed.) Viability of seeds. Chapman and Hall, London. BARTON, L.V. 1961. Seed preservation and longevity. Leonard Hill, London. BASS, L.N. 1965. Effect of maturity, drying rate, and storage conditions on longevity of Kentucky bluegrass seed. Assoc. Off. Seed Anal. Proc. 55:43-46. BASS, L.N. 1973a. Controlled atmosphere and seed storage. Seed Sci. & Technol. 1:463-492. BASS, L.N. 1973b. Response of seeds of 27 Cucumis melo cultivars to three storage conditions. Assoc. Off. Seed Anal. Proc. 63:83-87. BASS, L.N. 1975. Seed storage of Carica papaya L. HortScience 10:232-233.
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BASS, L.N. 1978. Sealed storage of crimson clover seed. Seed Sci.& Technol. 6:1017-1024.
BASS, L.N. and D.C. CLARK. 1974. Effects of storage conditions, packaging materials, and seed moisture content on longevity of safflower seeds. Assoc. Off. Seed Anal. Proc. 64:120-128. BASS, L.N., D.C. CLARK, and E. JAMES. 1962. Vacuum and inert-gas storage of lettuce seed. Assoc. Off. Seed Anal. Proc. 52:116-122. BASS, L.N., D.C. CLARK, and E. JAMES. 1963a. Vacuum and inert-gas storage of crimson clover and sorghum seeds. Crop Sci. 3:425-428. BASS, L.N., D.C. CLARK, and E. JAMES. 1963b. Vacuum and inert-gas storage of safflower and sesame seeds. Crop Sci.3:237-240. BASS, L.N. and P.C. STANWOOD. 1978. Long-term preservation of sorghum seed as affected by seed moisture, temperature, and atmospheric environment. Crop Sci. 18:575-577. BECQUEREL, P. 1934. La longevite des graines macrobiotiques. Acad. des. Sci. Compt. Rend. 199:1662-1664. CHANEY, R.W. 1951. How old are the Manchurian lotus seeds? Gard. J. (N.Y. Bot. Gard.) 1:137-139. CHRISTENSEN, C.M. 1973. Loss of viability in storage: Microflora. Seed Sci. & Technol. 1:547-562. CLARK, D.C. and L.N. BASS. 1975. Effects of storage conditions, packaging materials, and moisture content on longevity of crimson clover seeds. Crop Sci. 15:577-580.
DELOUCHE, J.C. and C.C. BASKIN. 1973. Accelerated aging techniques for predicting the relative storability of seed lots. Seed Sci.& Technol. 1:427-452. DELOUCHE, J.C., R.K. MATHES, G.M. DOUGHERTY, and A.H. BOYD. 1973. Storage of seed in sub-tropical and tropical regions. Seed Sci.& Technol. 1:671-700. DORRELL, D.G. and M.W. ADAMS. 1969. Effect of some seed characteristics on mechanically induced seedcoat damage in navy beans (Phaseolus vulgaris L.). Agron. J. 61:672-673. EGUCHI, T. and H. YAMADA. 1958. Studies on the effect of maturity on longevity in vegetable seeds (in Japanese. English summary). Natl. Inst. Agr. Sci. Bul., Ser. E, Hort. 7:145-165. EWART, A. J. 1908. On the longevity of seeds. Roy. SOC. Victoria, Proc. 21: 2-210.
FEDOSENKO, V.A. and L.M. YULDASHEVA. 1976. The preservation of C u cumis sativus seeds at extremely low temperatures (in Russian). Vsesoyuznogo Ordena Lenina Instituta Rastenievodstva imeni N. I. Vavilova 64:60-62. VIR, Leningrad, USSR. FLORIS, C. and M.C. ANGUILLESI. 1974. Aging of isolated embryos and endosperms of durum wheat: An analysis of chromosome damage. Mutation Res. 22:133-138.
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HARRINGTON, J.F. 1972. Seed storage and longevity. p. 145-245. I n T. T. Kozlowski (ed.) Seed biology, vol. 3. Academic Press, New York. HARRISON, B.J. and R. CARPENTER. 1977. Storage of Allium cepa seed a t low temperatures. Seed Sci. & Technol. 5:699-702. HEYDECKER, W. 1973. Seed ecology. Pennsylvania State University Press, University Park, Pa. HOLMES, A.D. 1953. Germination of seeds removed from mature and immature butternut squashes after seven months of storage. Proc. Amer. SOC. Hort. Sci. 62:433-436. HONJO, H. and Y. NAKAGAWA. 1978. Suitable temperature and seed moisture content for maintaining the germinability of citrus seed for long term storage. p. 31-35. I n T. Akihama and K. Nakajima (eds.) Long term preservation of favorable germ plasm in arboreal crops. The Fruit Tree Research Station of the Ministry of Agriculture and Forestry, Japan [Kokusai Print Service, Tokyo]. HOWE, R.W. 1973. Loss of viability of seed in storage attributable to infestations of insects and mites. Seed Sci. & Technol. 1:563-586. IBPGR. 1976. Report of IBPGR working group on engineering, design, and cost aspects of long-term seed storage facilities. International Board for Plant Genetic Resources, Rome. JAMES, E. 1967. Preservation of seed stocks. Adu. Agron. 19237-106. JAMES, E., L.N. BASS, and D.C. CLARK. 1967. Varietal differences in longevity of vegetable seeds and their response to various storage conditions. Proc. Amer. SOC.Hort. Sci. 91:521-528. JUNTTILA, 0. and C. STUSHNOFF. 1978. Freezing avoidance by deep su-per-cooling in hydrated lettuce seeds. Nature 269:325-327. JUSTICE, O.L. and L.N. BASS. 1978. Principles and practices of seed storage. USDA Agr. Handb. 506. KOLOTENKOV, P.V. 1974. The mutagenic influence of drying on pea seeds. Soviet Genetics 10:924-925. KOTOBUKI, K. 1978. Seed storage of Japanese persimmon, Diospyros kaki. p. 36-42. I n T. Akihama and K. Nakajima (eds.) Long-term preservation of favorable plant germ plasm in arboreal crops. The Fruit Tree Research Station of the Ministry of Agriculture and Forestry, Japan [Kokusai Print Service, Tokyo]. KOZLOWSKI, T.T. (ed.). 1972. Seed biology, vol. 3. Academic Press, New York. KRETSCHMER, M. 1976. Mehrjahrige Lagerung von Lactuca sativa L. - bei unterschiedlichen Temperaturen 1. Veranderungen der Temperature-toleranz im Dunkeln und bei Licht. Gartenbauwissenschaft 41:S.229-235. MOORE, R.P. 1972. Effects of mechanical injuries on viability. p. 94-113. In E. H. Roberts (ed.) Viability of seeds. Chapman and Hall, London.
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MOSS, H.J., N.F. DERERA, and L.N. BALAAM. 1972. Effect of pre-harvest rain on germination in the ear and a-amylase activity of Australian wheat. Austral. J. Agr. 23:769-777. MUMFORD, P.M. and B.W.W. GROUT. 1978. Germination and liquid nitrogen storage of cassava seed. Ann. Bot. 42:255-257. NAKAMURA, S. 1975. The most appropriate moisture content of seeds for their long life span. Seed Sci. & Technol. 3:747-759. OHGA, I. 1923. On the longevity of seeds of Nelumbo nucife. Bot. Mag. (Tokyo) 37:87-95. OMURA, M., Y. SATO, and K. SEIKE. 1978. Long-term preservation of Japanese pear seeds under extra low temperatures. p. 26-30. In T. Akihama and K. Nakajima (eds.) Long term preservation of favorable germ plasm in arboreal crops. The Fruit Tree Research Station of the Ministry of Agriculture and Forestry, Japan [Kokusai Print Service, Tokyo]. ORLOVA, N.N. and T.A. EZHOVA. 1976. Effect of the DNA synthesis inhibitor 5-aminouracil on the appearance of chromosomal aberrations in Allium fistulosum seeds of various ages. Soviet Genetics 10:1476-1481. ORLOVA, N.N. and V.I. NIKITINA. 1972. The moment of appearance of chromosome aberrations during the aging of seeds. Soviet Genetics 4:11531158. ORLOVA, N.N., N.P. ROGATYKH, and G.A. KHARTINA. 1976. Decrease in the mitotic potential of cells in dormant seeds of Welsh onion during storage. Soviet Plant Physiol. 22:629-635. OWEN, E.G. 1956. The storage of seeds for maintenance of viability. Commonw. Agr. Bur. Pastures and Field Crops Bul. 43. POLLOCK, B.M. 1961. The effects of production practices on seed quality. Seed World 89(5):6, 8 , 10. PORSILD, A.E., C.R. HARINGTON, and G.A. MULLIGAN. 1967. Lupinus arcticus Wats. grown from seeds of Pleistocene Age. Science 158:113-114. POWELL, A.A. and S. MATHEWS. 1976. Deteriorative changes in pea seeds (Pisum sativum L.). J. Expt. Bot. 28:225-234. RAMSBOTTOM, J. 1942. Duration of viability in seeds. Gard. Chron. 111: 234. ROBBINS, M.L. and W.N. WHITWOOD. 1973. Deep-cold treatment of seeds: Effect on germination and on callus production from excised cotyledons. Hort. Res. 13:137- 141. ROBERTS, E.H. 1961. The viability of rice seed in relation to temperature, moisture content, and gaseous environment. Ann. Bot. 25:381-390. ROBERTS, E.H. (ed.). 1972. Viability of seeds. Chapman and Hall, London. ROBERTS, E.H. and F.H. ABDALLA. 1968. The influence of temperature, moisture, and oxygen on period of seed viability in barley, broad beans, and peas. Ann. Bot. (N.S.) 32:97-117. ROBERTS, E.H., F.H. ABDALLA, and R.J. OWEN, JR. 1967. Nuclear damage and the ageing of seeds with a model for seed survival curves. Symp. SOC. Expt. Biol. 21:65-100.
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SAKAI, A. and M. NOSHIRO. 1975. Some factors contributing to the survival of crop seeds cooled to the temperature of liquid nitrogen. p. 317-326. In 0. H. Frankel and J. G. Hawkes (eds.) Crop genetic resources for today and tomorrow. International Biological Programs, Vol. 2. Cambridge University Press, New York. SHANDS, H.L., D.C. JANISCH, and A.D. DICKSON. 1967. Germination response of barley following different harvesting conditions and storage treatments. Crop Sci. 7:444-446. STANWOOD, P.C. and L.N. BASS. 1978. Ultracold preservation of seed germplasm. p. 361-371. I n P.H. Li and A. Sakai (eds.) Plant cold hardiness and freezing stress. Academic Press, New York. STANWOOD, P.C., M.W. BROWN, and E.E. ROOS. 1978. Freezing damage of high moisture lettuce seeds. Newsletter Assoc. Off. Seed Anal. 52:38-39. STUSHNOFF, C. and 0. JUNTTILA. 1978. Resistance to low temperature injury in hydrated lettuce seed by supercooling. p. 241-247. I n P.H. Li and A. Sakai (eds.) Plant cold hardiness and freezing stress. Academic Press, New York. TOOLE, E.H. and V.K. TOOLE. 1954. Relation of storage conditions to germination and to abnormal seedlings of bean. Proc. Intern. Seed Testing Assoc. 18:123-129. TOUZARD, J. 1961. Influences de diverses conditions constantes de temperature et d’humidite sur la longevite des graines de quelques especes cultivees. Adv. hort. sci. and their applications. Proc. 15th Intern. Hort. Congr., Nice, I, 339-347, Pergamon, Oxford. VAN STADEN, J. 1978a. Seed viability in Protea neriifolia. I. The effects of time of harvesting and seed viability. Agroplantae 10:65-67. VAN STADEN, J. 1978b. Seed viability in Protea neriifolia. 11. The effects of different storage conditions on seed longevity. Agroplantae 10:69-72. VILLIERS, T.A. 1973. Aging and the longevity of seeds in field conditions. p. 265-288. I n W. Heydecker (ed.) Seed ecology. Pennsylvania State University Press, University Park, Pa. VILLIERS, T.A. 1974. Seed aging: Chromosome stability and extended viability of seeds stored fully imbibed. Plant Physiol. 53:875-878. VILLIERS, T.A. and D.J. EDGCUMBE. 1975. On the cause of seed deterioration in dry storage. Seed Sci. & Technol. 3:761-774. WESTER, H.V. 1973. Further evidence of age of ancient viable lotus seeds from Pulan tien deposit, Manchuria. HortScience 8:37 1-377. WOODSTOCK, L.W., J. SIMKIN, and E. SCHROEDER. 1976. Freeze drying to improve seed storability. Seed Sci. & Technol. 4:301-311. YOUNG, R.E. 1949. The effect of maturity and storage on germination of butternut squash seed. Proc. Amer. SOC. Hort. Sci. 53:345-346. YOUNGMAN, B.J. 1952. Germination of old seeds. Kew Bul. 6:423-426.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
3 Nutritional Ranges in Deciduous Tree Fruits and Nuts C. B. Shear and M. Faust Fruit Laboratory, Horticultural Research Institute, Science and Education Administration, U. S. Department of Agriculture, Beltsville, Maryland 20705 I. Introduction 143 11. Deficiency and Toxicity Symptoms A. Nitrogen (N) 145 1.Deficiency 145 2. Toxicity 145 B. Phosphorus (PI 145 1.Deficiency 145 2.Toxicity 146 C. Potassium (K) 146 1.Deficiency 146 2. Toxicity 147 D. Magnesium (Mg) 147 1.Deficiency 147 2. Toxicity 147 E. Calcium (Ca) 147 1.Deficiency 147 F. Iron (Fe) 149 1.Deficiency 149 2. Toxicity 149 G. Manganese (Mn) 149 1.Deficiency 149 2. Toxicity 149 H. Zinc (Zn) 150 1.Deficiency 150 2. Toxicity 150 I. Boron (B) 150 1.Deficiency 150 2. Toxicity 151
142
144
NlJTRITION RANGE I N DECIDUOUS F R U I T S & N U T S 143
J. Copper (Cu) 152 1. Deficiency 152 2. Toxicity 152 K. Chlorine (C1) 152 1.Deficiency 152 2. Toxicity 152 L. Sodium (Na) 152 1. Toxicity 152 M. Sulfur (S) 153 1. Deficiency 153 N. Arsenic (As) 153 1. Toxicity 153 0.Aluminum (Al) 153 1. Toxicity 153 111. Nutrient Concentration in Plant Tissues in Relation to Nutritional Disorders 153 IV. Literature Cited 161
I. INTRODUCTION Although all plants require the same minerals to complete their life cycles, the quantities and balances necessary for optimum growth and production of high yields of quality produce vary greatly among species. The nutrition of large woody trees including fruit trees differs in many ways from that of annual herbaceous plants. Fruit nutrition has been studied since the turn of the century and its history has been reviewed (Faust 1979). Several specific aspects of tree nutrition also have been reviewed (Ballinger et al. 1966; Benson and Linder 1966; Bould 1966, 1970; Boynton and Oberly 1966a,b; Cain and Shear 1964; Chapman 1966; Hansen and Proebsting 1949; Kenworthy and Martin 1966; Proebsting 1966; Shear 1966; Wallace 1961; Westwood and Wann 1966), and the nutritional ranges a t which fruit trees grow best or manifest nutritional deficiencies have been assembled (Kenworthy and Martin 1966). As time has passed and more data have become available, slight modifications have been made in absolute values a t which plant performance could be defined. All available lists giving ranges of nutrient requirements are out of print. Yet this information is needed because of newly developing orchards introducing scientific nutritional methods. Therefore, publishing an up-to-date list of ranges of nutrient requirements for deciduous trees is necessary. In fruit crops, perhaps more than in any other group of economic plants, nutrient imbalances may manifest themselves in quality characteristics of the fruit of otherwise normal appearing trees. Therefore, in considering the adequacy of nutrition for fruit and nut trees we must be aware
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not only of the level of nutrients sufficient to prevent abnormal growth, or leaf symptoms, but also of those necessary to prevent abnormal fruit color, texture, or keeping quality, or in nuts, to prevent reduced filling or oil content. Although each nutrient element usually enters into a number of metabolic processes in the plant, specific symptoms associated with failure of its dominant function are usually the first to appear when an element is in deficient supply. However, since nutrients are not taken up by plants entirely independently of one another, symptoms of deficiencies and excesses may not always be easily distinguished and a knowledge of nutrient interactions is essential for accurate diagnosis. Soil and climatic factors also greatly influence the uptake and function of nutrients. Therefore, the appearance of a symptom characteristic of the deficiency of a certain element may not indicate a lack of that element in the nutrient medium, or even in the plant. The uptake of the nutrient element may have been inhibited by a lack or excess of soil moisture or by an excess of some other element or, once within the plant, it may have been converted into a metabolically inactive form. For these reasons, identification of the deficiency characterized by specific symptoms may not provide the information necessary to correct the disorder. Symptoms are very useful in identifying nutritional disorders, but to diagnose the imbalance responsible for the occurrence of a specific symptom, a knowledge of the nutrient content of one or more portions of the plant is often necessary. The diagnostician must be aware of the many factors other than nutritional that may be responsible for reducing tree growth or inducing symptoms that can be confused with those of nutrient deficiency or excess (Woodbridge 1976). Drought, heat, cold, mechanical injury, insects, nematodes, pathogenic diseases, herbicides, and pesticides may produce symptoms almost indistinguishable from those of malnutrition. In fact, true symptoms of malnutrition may result from some of these agents, particularly from herbicides and virus diseases. Successful diagnosis of the cause of any nutritional disorder requires all available information on cultural and climatic conditions as well as a knowledge of symptomology and tissue composition. 11. DEFICIENCY AND TOXICITY SYMPTOMS Symptoms vary among species included in this section. Where possible, symptoms are described in such a way as to apply to as many of the species as possible. Characteristics unique to individual species are emphasized where necessary.
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A. Nitrogen (N) 1. Deficiency.-Nitrogen deficiency is common in fruit and nut trees. Reduced top growth with short, upright spindly shoots with pale, yellowish green leaves are the first symptoms. Symptoms are usually fairly uniform over the entire plant. The symptoms may develop a t any time during the growing season depending on weather conditions and level of available N. Unless additional N is made available, symptoms become more severe as the season advances. Thus, the best time to judge N deficiency is late in the season. In severely deficient trees, basal shoot leaves may develop extreme symptoms. These leaves may develop necrotic areas along their margins in tung, and in pecans and walnuts leaflets may drop from the rachis. In fruit trees, fall coloring may be brighter on N deficient trees. Leaf color differences are less marked on cherry, peach, and pear trees, whereas in apple and plum marked color reduction may appear by mid season. Fruits are usually smaller and earlier in maturing, especially on the stone fruits, and peach fruit is astringent and stringy. Nuts may be poorly filled. Fruit bud differentiation may be decreased and fruit set the following year may be greatly reduced.
2. Toxicity.-Though much less spectacular, the effects of excessive levels of N can be as economically disastrous as N deficiency. Symptoms of over-fertilization with N may manifest themselves in many ways depending on the species, the balance of N with other nutrients, the form of N (ammonium, nitrate, or urea) available to the roots, and the time of application. Nitrogen is a major factor in both growth and flowering, and effects of too much may be most readily recognized as excessive stimulation of shoot elongation and development of abnormally dark green leaves. Its most detrimental effects, however, are on fruit maturity and quality. As N supply increases above the optimum, fruit color is reduced in both stone and pome fruits; area and intensity of red color on red cultivars of apples is reduced, as is yellow on yellow cultivars. Maturity is delayed in both fruits and nuts. In pome fruits, flavor may be diminished, storage life shortened, and susceptibility to many physiological disorders increased, both on the tree and in storage. Though most of these disorders are associated primarily with Ca deficiency (see below) they are all aggravated by a high level of N. In the oil-producing nuts, high N, especially a high ratio of N to K not only delays maturity but lowers the oil content of fruit.
B. Phosphorus (P) 1. Deficiency.-Phosphorus deficiency severe enough to produce recognizable foliar symptoms is rare in fruit or nut trees in the orchard.
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Symptoms on all fruit and nut crops show up first as limited and slender growth. Young expanding leaves are abnormally dark green and the lower sides of the young leaves, especially along the margins and main veins, frequently show purplish discoloration. The leaves may have a leathery texture and form abnormally acute angles with the stem. Since the first symptom of P deficiency is an inhibition of active vegetative growth, the leaf symptoms frequently become less marked in late summer after active vegetative growth is complete and the P uptake by the roots is able to catch up with the reduced demands of the slowly growing plant. Lateral buds may remain dormant or die, and a s a result few lateral shoots appear. Blossoming and fruiting are reduced and bud opening in the spring may be delayed. Deficient stone fruits ripen early, have a greenish ground color, and may be highly flushed with a soft, puffy acid flesh of poor eating quality. 2. Toxicity.-Effects of excess P are expressed usually as a n antagonism of P and one or more of the essential heavy metals such a s Zn, Cu, Fe, or Mn. Since symptoms of deficiencies of these elements may be induced by excesses of other elements as well a s by a n insufficient supply of the metals themselves, the complex interactions responsible for their appearance cannot be interpreted from visual symptoms but require knowledge of plant composition and the soil factors responsible for th a t composition.
C. Potassium (K) 1. Deficiency.-"Scorching" of the margins of older leaves is the outstanding symptom of advanced K deficiency in all fruit and nut crops. In the stone fruits an upward lateral curling a n d chlorosis of the leaves is evident before the scorch appears. In most species of nut trees chlorosis may precede the scorching. Often, even before chlorosis develops, leaf petioles recurve and the leaves roll and droop, giving the tree the appearance of wilting even though the leaves are completely turgid. In apple, scorch may be preceded by a greyish green discoloration of the upper surface of the margins which later turns a reddish brown and works inward, mostly interveinally. Young leaves generally show less severe symptoms although they may be smaller than normal. A heavy fruit crop usually accentuates the symptoms. Nuts, especially those with high oil content, make a high demand on available K and even young leaves on K deficient trees may fall prematurely. In tung, fruit still clinging to leafless shoots is a typical symptom of severe potassium deficiency. Poor filling and low oil content of kernels also result from inadequate K.
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2. Toxicity.-Symptoms specific for excessive accumulation of K in fruit or nut trees are unknown. High concentrations of K in the soil, however, may affect the uptake of other cations and induce symptoms of deficiencies of these elements. The one most commonly observed is Mg deficiency, but the heavy metals Mn and Zn also may be reduced to deficiency levels by excess K.
D. Magnesium (Mg) 1. Deficiency.-Magnesium deficiency in its severest stages may cause marginal scorching similar to K deficiency, but its pattern of development is very distinctive. Its earliest appearance is a fading of the green color a t the terminals of older leaves or leaflet terminals in pinnateleaved species. The fading, followed by chlorosis, progresses interveinally towards the base and midrib giving the very typical “herringbone” appearance to the leaves. In pear, the symptoms can be very spectacular. Dark purplish islands surrounded by chlorotic bands may develop in the interveinal tissue on both sides of the midrib while the leaf margin maintains a more-or-less normal green color. Such leaves have a “Christmas tree” appearance. In some cases the whole leaf may turn yellow before falling. As the season advances, symptoms develop on progressively younger leaves and the older leaves are abscised. Heavily fruiting trees and branches are the most severely affected. Developing fruit has a high demand for Mg and will draw it from neighboring leaves, thus inducing severe symptoms and early defoliation. In extremely severe cases fruit may fail to mature and may drop early. In most fruit and nut crops certain stages of Mg and K deficiencies may be difficult to distinguish visually by even an experienced diagnostician. In such cases leaf analyses may be necessary for absolute identification.
2. Toxicity.-Symptoms of excessive concentrations of Mg are not specific but usually appear as a deficiency of either K or Ca, depending on the balance of cations available to the tree.
E. Calcium (Ca) 1. Deficiency.-Since Ca affects the supply of other nutrients in so many ways, indirect influences of insufficient Ca may confound the recognition of visible foliar symptoms of direct Ca deficiency. Specific foliar symptoms of Ca deficiency have been developed on many fruit and nut crops in artificial cultures, and these symptoms have sometimes, though rarely, been observed on orchard trees.
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The first indication of Ca deficiency on apple foliage is the upward cupping of the margins of the youngest leaves. On actively growing terminals the expanding leaves develop a uniform veinal and interveinal chlorosis. The very youngest leaves may become entirely chlorotic and terminal growth stops. Margins of older affected leaves may become necrotic and shatter. In severe cases, terminals die back. Various symptoms have been described as associated with low levels of soil Ca or low soil pH but these cannot definitely be ascribed to a deficiency of Caper se since, under these conditions, toxic levels of such elements as Na, Al, Mn, Zn, B, and perhaps H may become available. The fruit of many deciduous fruit trees often shows symptoms associated with a low level of Ca, even when the Ca level in the rest of the plant is sufficient for normal growth. Symptoms may be expressed in many different ways depending on species and cultivar. A common though not always distinctive (see boron deficiency) response to low Ca is cracking of the fruit, especially stone fruits and apples. Cracking usually occurs immediately after periods of heavy rainfall and/or high relative humidity. In extreme cases peaches are small, green, and hard. Pome fruits are especially sensitive to low levels of Ca and may exhibit one or more of the following disorders. Bitter pit appears as slight indentations in the skin, usually toward the calyx end of the fruit. These areas turn brown, and soft dessicated tissue develops in the flesh immediately beneath the spots. Bitter pit may develop while the fruit is still on the tree, but usually develops in storage or after fruit is taken from storage and kept for a few days a t room temperature. Cork spot may appear early in the development of the fruit, first as small blushed areas on the skin above hard brown spots in the flesh. These spots consist of hard compressed tissue caused by cell proliferation after normal cell division has ceased. Calcium-deficient fruit are also more susceptible to sunburn, which appears as large, depressed dehydrated areas on the exposed surface. Lenticel breakdown appears first as pale areas around the lenticels. White halos develop around the lenticels and later turn brown or black. These prominent lenticels may be the only symptom of Ca deficiency to develop on mildly deficient fruit. A number of other fruit disorders-watercore, internal breakdown, and low temperature breakdown-also are associated with inadequate Ca in the fruit. A bark symptom of apples called “measles” or internal bark necrosis results from a complex involving low Ca, high Mn, and sometimes low B. This symptom is described under B deficiency and Mn toxicity.
A. Nitrogen deficiency. Left to right-severe to none.
E. Manganese deficiency.
B. Potassium deficiency. Left to r severe to none.
F. Zinc deficiency. Le severe to none.
FIGURE 3.2. NUTRITIONAL DEFICIENCY SYMPTOMS II
C. Calcium deficiency.
right-
ACH
0. Iron deficiency. Left to rightsevere to none.
0. Manganese deficiency.
H. Copper deficiency. Left to rlght-severe to none.
1. Zinc deficiency on the tree.
M. Sulfur deficiency.
FIGURE 3.2 (Continued)
J. Zinc deficiency in sand culture.
N. Magnesium deficiency.
ciency on the tree.
0. Magnesium deficiency.
L. Boron deficiency on the tree.
P. Arsenic toxicity.
Photographs I.J.K.L. and M are courtesy 01 N. F. Childers. Rutgers University
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149
F. Iron (Fe) 1. Deficiency.-Iron deficiency symptoms are one of the most commonly observed on fruit and nut trees. This is true because of the many conditions other than an actual deficiency of Fe that can induce the symptoms. T h e initial symptom is the loss of green color in the very youngest leaves. While the interveinal tissue becomes pale green, yellow, or even white, the veins remain dark green. New leaves may unfold completely devoid of color but the veins usually turn green later. In acute cases, dieback of shoots and branches may occur.
2. Toxicity.-Though rare under field conditions, Fe toxicity usually results in Mn deficiency.
G . Manganese (Mn) I. Deficiency.-Chlorosis between the main veins starting near the margin of the leaf and extending toward the midrib is the typical symptom of Mn deficiency. Manganese deficiency symptoms are similar to those of both Fe and Mg. Unlike Fe deficiency, chlorosis does not appear on the very youngest newly expanding leaves nor do the finest veins remain green. Unlike Mg, Mn deficiency seldom develops so far as to produce interveinal necrosis. Whereas Mg deficiency is usually confined to the older leaves, Mn deficiency symptoms develop on the younger leaves shortly after they have fully expanded and persist with little change. In peach, terminal growth may become stunted. Symptoms observed on walnut are similar to those already described, but in severe cases some interveinal bronzing and necrosis may occur. Unlike the necrosis resulting from B excess, the necrotic areas are usually angular rather than rounded or blotchy. A disorder of pecans called “mouse-ear’’ has been attributed to Mn deficiency, though there is some question as to its cause. “Mouse-ear” is characterized by a shortening of the mid-vein of the leaflets which causes the leaflets to become rounded and wrinkled and to cup upward. T h e entire leaf may be smaller than normal. 2. Toxicity.-A disorder known as “measles” that occurs on apples, particularly on the cultivars ‘Delicious’ and ‘Jonathan’, is in part caused by an excess of Mn or, more specifically, an excess of Mn accompanied by low Ca in the bark. A part of the syndrome is an expression of B deficiency and will be described under that element. Manganese-related measles is characterized by the eruption of pimples on the bark of 2-year-old shoots. As the symptoms progress from year to year the pimples enlarge and erupt, producing sunken areas surrounded by callus.
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These areas coalesce and the bark becomes rough, cracked, and scaly. In severe cases, whole branches may die. H. Zinc (Zn) 1. Deficiency.-Zinc deficiency symptoms are variously described as “rosette,” “yellows,” “little leaf,” and “bronzing” in different fruit and nut trees. In all cases, however, the initial mild symptom is an interveinal leaf chlorosis difficult to distinguish from Mn deficiency. With Zn deficiency, however, more extensive symptoms usually develop. Newly developing leaves are smaller than normal, and reduced shoot elongation brings them close together giving rise to the popular names “little leaf” and “rosette.” In severe cases, older leaves may fall, leaving tufts or “rosettes” of leaves near the terminals of branches. In pecans, walnuts, and almonds, reddish brown areas or perforations may develop between the veins. In tung, the leaf margins become wavy, one side of the blade may fail to develop, and the leaf will curl towards the small side into a sickle shape. In very severe cases this uneven growth affects the whole tree, giving it a one-sided appearance. The lower surface of leaves may take on a purplish-bronze cast from which the name “bronzing” is taken. In severe cases, necrotic areas may develop a t random over the leaf surface and later disintegrate, giving the leaf a ragged appearance. In stone fruits, irregular chlorotic areas develop along the margins and later coalesce to form continuous yellow bands extending from midrib to margins. Red to purple blotches may develop within the chlorotic areas and later dry up and fall out, producing a shot-hole effect. Crinkling, cupping, and curving of the leaves are also common. Small crops of small misshapen fruit are produced. Deficient peach and plum fruits may be more flattened than normal while apricot fruits may be less flattened than usual. Nuts from deficient oil-producing nut species are usually poorly filled and low in oil content. 2. Toxicity.-As with most heavy metals, an excess of Zn usually appears as Fe chlorosis.
I. Boron (B) 1. Deficiency.-Boron deficiency shows up in many different ways, depending on the crop and the extent of the deficiency. In most fruit crops, symptoms usually appear on the fruit before vegetative parts are affected. Fruit symptoms in apples and pears are quite similar. Fruits do not develop normally and take on a gnarled misshapen appearance
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caused by depressions usually underlaid by hard corky tissue which rapidly browns when exposed to the air. The color of the surface of these areas is usually darker green than the surrounding tissue. If the deficiency does not become severe until late in their development, the main fruit symptom may be internal cork formation scattered throughout the entire apple from peel to core. This type of B deficiency often has been confused with cork spot (see Ca deficiency). Some apple cultivars’ fruit may crack, particularly if both B and Ca are low. In mild cases, the whole surface of the fruit may be covered with small cracks that have callused over, producing a russeted appearance. In plums, the symptom appears as brown sunken areas in the flesh of the fruit, ranging in size from small spots to almost the whole fruit. The firm flesh beneath these sunken areas may extend to the pit. Affected fruit usually colors earlier than normal, and falls. Gum pockets may be formed also in the flesh of the fruit, especially of almond. In peaches, the fruit develops brown, dry corky areas in the flesh adjacent to the pit, and some fruits may crack along the suture. The most typical vegetative symptom in all tree crops is the failure of apical meristems to develop and eventual death of shoot tips followed by forcing of new weak shoots below the dead tips. Boron-deficient leaves are darker green, thick, and brittle, and are abscised early, starting at the shoot tips. Boron deficiency may be part of the symptom complex of “apple measles”-the appearance of purplish pimples on young twigs progressing to rough cracked bark on older twigs. Lenticel proliferation, corky callus development, and bark splitting occurs on B deficient peach and tung also. Reproductive organs are particularly sensitive to lack of B and such incipient symptoms as failure to set fruit or even the wilting and dying of blossoms as in “blossom blast” of pears may be the only indication of B deficiency. 2. Toxicity.-Fruit, shoot, and bark symptoms are the most typical of B injury in the stone fruits, almond, apricot, cherry, peach, plum, and prune, and the pome fruits, apple, pear, and quince. Dieback of twigs, greatly enlarged nodes on one- and two-year-old twigs, gumming of the twigs and larger branches, splitting, early maturity, corking, and dropping of the fruit are typical responses of the stone fruits. Early maturity and shortened storage life are characteristic of toxicity in apples. Foliage symptoms on stone and pome fruits usually are yellowing along the midrib and large lateral veins, often followed by abscission. In contrast, most nut crops show a tip burning followed by marginal and interveinal necrosis. Older leaves are the first to be affected.
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J. Copper (Cu) 1. Deficiency.-Copper deficiency is occasionally seen on fruit and nut trees in the orchard. On almond, bark on the trunk and older branches becomes rough and in late winter there may be some gum exudation from these areas. On most species leaves become chlorotic and various degrees of mottling develop. In peach, new leaves may be narrow and elongated with wavy margins. Terminals are most severely affected, and wilting and defoliation occur in severe cases. In walnut and tung, marginal and interveinal necroses precede defoliation, and in all species death of the terminals is followed by growth of laterals, giving a bushy appearance to the trees. Copper and Zn deficiencies are often associated, producing a confusing symptom picture.
Toxicity.-Copper toxicity is practically unknown under orchard conditions. When induced under artificial culture conditions the symptom is usually that of Fe chlorosis, the severity being related to the level of c u . 2.
K. Chlorine (Cl) 1. Deficiency.-Although C1 is an essential nutrient element, specific symptoms attributable to a lack of C1 have not been observed on fruit or nut trees. 2. Toxicity.-Most stone fruits are known to be injured by excess chloride in the soil. Stunting without specific leaf symptoms may result from moderate salt concentrations. At higher levels apricot leaves cup upward and roll along margins and tip. Margins later scorch. In cherry, small pale leaves with marginal scorch develop and drop early. Almond, plum, and prune show tip and marginal leaf scorch. Symptoms on peach are similar to those on cherry.
L. Sodium (Na) Sodium has not been determined to be an essential nutrient for any deciduous fruit or nut tree species, nor has it been shown to be substitutable for any portion of the K requirement as is the case with some plants. 1. Toxicity.-In “alkali” soils where Na constitutes 15% or more of the exchangeable cations, or under saline conditions where Na is a major component of the soluble salts, Na may be toxic. Although some chlorosis may precede the appearance of burning, the most typical symptoms of excess Na on most fruits and nuts are tip
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burning and marginal scorch. In apple, leaves may turn yellow and drop in a few days.
M. Sulfur (S) 1. Deficiency.-Sulfur deficiency occasionally occurs in apple, apricot, cherry, peach, plum, and pear orchards. Symptoms are a general yellowing of the younger leaves somewhat similar to N deficiency. In peach, the much smaller chlorotic leaves develop marginal necrosis. Rosettes of small laterals with small pale leaves may develop near terminals. In severe cases, large necrotic areas that result in leaf distortion occur in older leaves. In apple, some interveinal chlorosis occurs.
N. Arsenic (As) 1. Toxicity.-Arsenic toxicity may occur on stone fruit trees growing on old apple orchard sites where large amounts of arsenate spray residues have accumulated in the soil. Peaches, apricots, and almonds are very susceptible to injury. Prunes and cherry are moderately sensitive. Plums, pears, and apples are more resistant. Symptoms appear first on older leaves as a brown to red coloration along the leaf margins followed by a similar discoloration scattered between the veins. The tissue in many of these spots dies and drops out, giving a shot-hole appearance. In severe cases, complete defoliation may occur or young terminal leaves may remain normal. Yield is usually reduced and fruit is astringent.
0. Aluminum (Al) 1. Toxicity.-Aluminum is not considered to be an essential nutrient element, although in very low concentrations it may have stimulatory effects on plant growth. Aluminum, however, is very toxic in small concentrations, especially below pH 4.7. Root malformation, malfunction, and ultimate death are the usual responses to toxic levels of Al. Resulting leaf symptoms are not specific for A1 toxicity, but usually appear as those of Ca deficiency.
111. NUTRIENT CONCENTRATION IN PLANT TISSUES IN RELATION TO NUTRITIONAL DISORDERS The absence of deficiency or toxicity symptoms does not necessarily indicate an optimum plant nutrient status. Incipient nutrient imbalances that may seriously reduce crop yield and quality may exist even in the '
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absence of noticeable growth reduction. Diagnosis of such conditions can be done accurately, rapidly, and economically by chemical analysis of appropriate plant tissues. Leaves are the most commonly used tissue for analysis, but because of the peculiarities of distribution of certain elements within the plant, feeding roots, petioles, fruit, or certain fruit parts may be used for some elements. Leaf analyses, to be of diagnostic value, must be based on standardized sampling methods and the results must be compared only with standard values obtained by those same procedures. Such values are given in Table 3.1. When available, these values refer to concentrations in leaves from the mid-portion of terminal shoots sampled a t about the cessation of terminal growth. This sampling would be during July or August in the North-Temperate Zone, the exact time depending on species and cultivar. For species having pinnate leaves, leaflets from the mid-section of the rachis of mid-shoot leaves should be sampled. If possible, leaves showing symptoms, especially those with necrotic tissue, should not be sampled. If it is impossible to collect leaf samples a t the proper time, or if other than mid-shoot leaves must be sampled, the direction of changes in concentration of the different elements with time and position on the shoot must be taken into consideration in comparing them with standard values. Any statement regarding the change in element concentration with time or position must be qualified. Calcium, Mn, Fe, and Na generally increase in concentration with time if they are continuously available for uptake by the roots. Nitrogen, P, K, Mg, and Zn generally decrease, while others are variable. Change in concentration of some elements from basal to terminal leaves on the shoot will vary, depending upon which side of the level of adequacy the concentrations fall. Nitrogen and P are usually higher in terminal than in basal leaves, whereas Ca is consistently higher in basal leaves. Potassium, Mg, Mn, Fe, Cu, and Zn shift their gradient on each side of the normal range. When these elements are in the deficiency range, retranslocation from the older to the younger leaves produces a lower concentration in the basal leaves. If a n excess of these elements is present, the concentration is usually higher in the older leaves. Boron, Al, and S are variable in this respect. It must be pointed out, however, that if changes in availability occur during the growing season a s a result of deficient or excess moisture, for example, these patterns may vary. Fruit analysis, particularly of pome fruits, has been found to be the most satisfactory means of diagnosing Ca and B deficiencies. As mentioned earlier, the fruit are the first to show symptoms of deficiencies and a number of physiological disorders occurring on the tree or in
Species
Element
NE
Leaf Leaf
July
Leaf Leaf Leaf Leaf Fruit flesh Fruit peel Leaf Leaf l-yearold bark Leaf Leaf
<5
NE NE 40-500 (?) 20-60 2
<20
NE NE NE NE NE NE > 150'
NE
Toxicity Range > 2.6 NE NE NE NE NE NE > 85 NE NE NE NE > 0.37 > 1.1 NE NE 1.7-2.5 0.15-0.3 1.2-1.9 1.5-2.0 0.025-0.05 0.07-0.10 0.25-0.35 25-150 25-150
il.1
Normal Range 2 .O -2.6 0.09-? 0.7-1.3 1.0-2.0 0.3-0.7 0.3-? NE 29-85 5-11 NE NE 0.19-0.27
<1.5 <0.13 <1.00 <0.7 <0.02 C0.07 <0.25 <25 NE
NE NE NE
Leaf Leaf
July July
Deficiency Range <2.0 NE <0.7 NE NE NE NE < 29
Tissue Sampled Leaf Leaf Leaf Leaf Leaf Leaf
Time Sampled July July July July July July
July July July July Harvest Harvest July July
~~~~
Concentration of Element in Tissue
~
Normal range is that in which normal growth and production can be expected. Deficiency range is that level below which some type of symptom may appear. Where a gap exists between the deficiency and normal range, increased growth might be expected as concentrations increase between these levels. Deficiency and normal ranges for nonessential elements are left blank. NE indicates that dependable data have not been established.
TABLE 3.1. NUTRIENT CONTENT OF PLANT TISSUE
2
C
z
crf
!a
2 !a
Cherry (Prunus cerasus and P. auiurn)
Apricot (Pr u n us armeniaca)
Species
Element
TABLE 3.1. (Continued)
Leaf Fruit Leaf Leaf Leaf
Leaf Leaf Leaf Leaf Leaf
August
July July July July July
Leaf Leaf Leaf Leaf Basal shoot leaves
Fruit flesh Leaf Leaf Leaf Leaf
Tissue Sampled
July Harvest July July
Summer
July July July
Harvest July July July July
Time Sampled
NE
NE
NE NE
<1.0
NE NE
NE NE NE NE
<20 <5 <12
<20
1.8-3.3 0.16-0.4 1.0-3.0 0.7-3.0 0.4-0.9
(0.8
NE
0.31&
NE
20-50 30-60 5-10 12-?
NE NE NE NE NE
>6
NE
> 1.0
NE NE NE NE NE >0.5
> 80
NE NE NE
30-?
<30
NE
NE NE
NE NE NE NE NE 2.3-3.0 0.15-0.3 2.0-3.0 ?-3.0 0.8-1.5
NE NE NE NE NE NE NE NE NE
Toxicity Range
<2.0 <0.15 <1.75
<500
10-30 5-12 15-200 0.10-0.20 0.01-0.10
Normal Range
< 10 <4 < 14 <0.05 <0.01
Deficiency Range
Concentration of Element in Tissue
persica)
(Prunus
Peach
Mg (5%) Mn (ppm) Fe b u m ) B (ppm)
ca(%)
N (%I P (9%) K (5%)
As
A1
c1
July July Julv July
JUG
~
Julv ..~
July July
September September September September September September September September September September
N (96)
Filbert (Cory1u s maxima)
P (%I K (96) Ca ("lo) Mg (96) Mn (ppm) Fe (ppm) B (ppm) Cu (ppm) Zn (ppm) Mo S Na
Reliable data not established
July July July July July
Chestnut (Castanea sp.)
A1 As
Mn (ppm) Fe (ppm) B (ppm) Cu (ppm) Zn (ppm) Mo
Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf
Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf
Leaf Leaf Leaf
Leaf Leaf Leaf Leaf Leaf
<20
L
<1.7 10.11 <0.75 <1.0 <0.20 <20
2.5-4.0 0.14-0.40 1.5-2.5 1.5-2.0 0.25-0.60 20-300 100-200 20-80
NE: NE NE NE NE NE
1.5-2.8 0.1-0.4 0.3-1.3 0.8-1.6 0.18-0.26 166-828 ?-500 11-40 8-11 27-85
NE
NE
NE NE NE NE NE NE NE NE NE NE NE NE NE NE NE NE
15-70 NE 0.13-0.84
5-?
20-300 20-250 20-60
NE NE NE NE
(15
< 20
2
NE NE NE NE NE NE NE NE
NE NE NE NE NE NE NE NE NE NE NE NE NE NE NE NE
NE NE
> 0.5 >0.3
~~
NE NE NE NE
> 100
NE NE
2
C
z
Te
z
z
Pecan (Carya illinoensis)
Pear (Pyrus comm unis)
Species
Element
TABLE 3.1. (Continued)
September September September
Leaf Leaf Leaf
Leaf
September
August August August Summer
August
August August
August
September
Leaf
Leaf Leaf Leaf
Leaf Leaf
Tissue Sampled
Spur Leaf Spur Leaf Leaf Spur Leaf Spur Leaf Leaf Leaf Leaf Spur Leaf Leaf
August
Summer
July
Time Sampled
<0.9
2.5-3.0 0.1-0.2 0.9-1.3
NE
NE (2.4 <0.1
20-60 NE 0.01-0.03
20-170 100-800 20-60 6-20
0.25-0.90
1.0-2.0 1.0-3.7
0.12-0.25
< 16 NE <0.01
< 15 (5
(14
2
<0.25
<0.7 <0.7
<0.11
1.8-2.6
<1.0
NE 11.8
6-15 12-50 NE 0.25-0.75
Normal Range
<3 <12 NE < .01
Deficiency Range
NE NE NE
NE NE NE NE NE NE NE
NE NE NE NE
NE
NE NE
NE
NE
NE NE NE NE > 0.5 >1.0 NE >1.3
Toxicity Range
Concentration of Element in Tissue
F; 8 u)
c
a M
Tung (Aleurites fordii)
Plum and Prune (Prunus dornestica)
Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf
August August August August August August August
N (%) P
Mg (%I Mn (ppm) Fe (ppm) B (ppm) Cu (ppm)
A1 As
c1(%I
Leaf Leaf
Leaf Leaf
October
Bippm) Cu (ppm) Zn (ppm) Mo
S (%I Na
Leaf Leaf Leaf Leaf Leaf Leaf
Leaf
Leaf Leaf
August August August August August
September September
N (%)
A1 As
c1
Na
S
Ca (%) Mg (%) Mn (ppm) Fe B (ppm) cu Zn (ppm) Mo NE
NE
<0.69
NE
2.0-2.5 0.12-0.25 0.8-1.0 1.0-4.0 0.25-0.6 50-3100 NE 35-75 4-10
2.0-3.5 2.0-4.0 0.2-4.0 50-150 NE 30-56 5-10 NE NE 0.2-0.7
<2.0 <1.6 (0.2 < 20 NE < 20 <5 NE NE <0.05
<1.85 <0.1 <0.6 <0.75 <0.2 < 50 NE NE <4
2.1-3.0
<2.0
NE
0.8-2.5 0.2-0.65 100-2000 NE 60-450 NE >15-300 NE NE
NE 10.2 < 100 NE
>3.0 NE NE NE NE NE NE > 125 NE
NE NE NE NE NE NE NE > 56 NE NE NE NE >0.18 > 0.69 NE NE
NE NE NE NE > 450 NE NE NE NE NE NE NE NE
W
cn
A1 As
c1
Ye B (ppm) Cu (ppm) Zn (ppm) Mo S (96) Na
P (96) K (96)
N
A1 As
c1
Zn (ppm) Mo S Na
Element
Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf
July July July
Leaf
Tissue Sampled
July July July July July
August
Time Sampled
10.12 (0.9 (1.25 <0.2 <25 NE < 25 (5 < 20 NE NE NE NE
<35 NE NE NE NE
Deficiency Range
0.12-0.30 1.0-3.0 1.25-2.5 0.2-1.0 25-270 NE 25-300 5-20 20-200 NE 0.17-0.40 NE NE
Normal Range
NE NE NE
NE
NE
NE NE > 300 NE NE NE
NE
NE NE NE
NE NE
Toxicity Range
Concentration of Element in Tissue
This level will vary depending on level of other elements, particularly Ca and B. Since so many factors other than Fe concentration affect appearance of Fe chlorosis, no level can be established for Fe deficiency symptoms.
Walnut (Juglans regia)
Species
TABLE 3.1. (Continued)
NUTRITION RANGE IN DECIDUOUS FRUITS & NUTS
161
storage can result from low levels of fruit Ca and/or B when leaf levels are adequate for normal growth. Either peel or flesh analyses have been used to determine Ca status of the fruit. Whole fruit analyses should be avoided as the presence of different numbers of seeds in the sample can cause extreme variations in results. Through combination of visual diagnosis and tissue analysis the current nutritional status of deciduous fruit and nut trees can be diagnosed. Unfortunately, predicting the exact amount of nutrient required to bring the tree into nutritional balance is not simple. The method of trial and error must still be used. Nevertheless, combined with a knowledge of the soil and environmental factors that affect uptake and distribution in the tree, symptoms and nutrient concentrations can hasten the achievement of optimum nutrition. Most plants are tolerant of a wide range of nutrient variability, especially with respect to expression of visible symptoms of nutritional imbalance. There is often considerable overlapping of tissue concentrations between plants showing symptoms and ones without symptoms. This overlapping may be the result of variations in environmental variables such as moisture, temperature, or light intensity, for example, which subject the plant to stresses that may alter its tolerance for or response to a specific nutritional imbalance. Also, the level of one element in relation to that of others can greatly affect its function and, therefore, the level a t which deficiency or toxicity symptoms will appear. Toxicity levels of an element may appear as a deficiency of some other element. Some elements may accumulate to levels far above the plant’s actual need without showing any toxicity symptoms. Since these variations do exist, and since so much available data were obtained on different cultivars growing over wide ranges of soil and climatic conditions and from samples taken a t different times and from slightly different positions on the plant, the data of any single investigator could be misleading. To present all available data not only would be space-consuming, but without detailed interpretation would be confusing and totally unusable by the uninitiated. Therefore, we have taken the liberty to distill all available data and present in Table 3.1 those values that, in our judgment, represent the best estimates possible on the basis of current knowledge. Specific references cannot be cited for individual data; rather, the source material from which these data were evolved and from which illustrations have been taken are cited a t the end of this compilation.
IV. LITERATURE CITED BALLINGER, W.E., H.K. BELL, and N.F. CHILDERS. 1966. Peach nutrition. p. 276-390. In N. F. Childers (ed.) Nutrition of fruit crops: tropical,
162
HORTICULTURAL REVIEWS
sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. BENSON, N.R. and R.C. LINDER. 1966. Plum, prune and apricot. p. 504-517. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. BOULD, C. 1966. Leaf analysis of deciduous fruits. p. 651-684. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. BOULD, C. 1970. The nutrition of fruit trees. p. 223-234. In L. C. Luckwill and C.V. Cutting (eds.) Physiology of tree crops. Academic Press, London. BOYNTON, D. and G.H. OBERLY. 1966a. Apple nutrition. p. 1-50. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. BOYNTON, D. and G.H. OBERLY. 196613. Pear nutrition. p. 489-503. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. CAIN, J.C. and C.B. SHEAR. 1964. Nutrient deficiencies in deciduous tree fruits and nuts. p. 287-326. In H. B. Sprague (ed.) Hunger signs in crops. David McKay Co., New York. CHAPMAN, H.D. (ed.) 1966. Diagnostic criteria for plants and soils. Univ. of California, Riverside, Division of Agricultural Sciences. FAUST, M. 1979. Evolution of fruit nutrition during the 20th century. HortScience 14:321-325. HANSEN, C.J. and E.L. PROEBSTING. 1949. Boron requirements in plums. Proc. Amer. SOC. Hort. Sci. 53:13-32. KENWORTHY, A.L. and L. MARTIN. 1966. Mineral content of important fruit plants. p. 813-87O.In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. PROEBSTING, E.L. 1966. Edible nuts. p. 262-275. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. SHEAR, C.B. 1966. Tung nutrition. p. 549-568. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate; tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N. J. WALLACE, T. 1961. The diagnosis of mineral deficiencies in plants by visual symptoms. Chemical Publishing Co.,New York. WESTWOOD, M.N. and F.B. WANN. 1966. Cherry nutrition. p. 158-173. In N. F. Childers (ed.) Nutrition of fruit crops: tropical, sub-tropical, temperate;
NUTRITION RANGE I N DECIDUOUS FRUITS & NUTS
163
tree and small fruits. Horticultural Publications, Rutgers-The State University, New Brunswick, N.J. WOODBRIDGE, C.G. 1976. Nutritional disorders that resemble virus disorders. p. 316-346. In Virus diseases and noninfectious disorders of stone fruits in North America. USDA Agr. Handb. 437.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
4 The Lettuce Industry in California: A Q uarter Century of Change, 1954-1979 Edward J. Ryder U S . Agricultural Research Station, 1636 East Alisal Street, P.O. Box
5098, Salinas, California 93915 Thomas W. Whitaker U S . Department of Agriculture (Collaborator) P.O. Box 150, La Jolla, California 92038 I. Introduction 165 A. Present State of the Industry 165 1. Area, Yield, Value 165 166 2. Production Districts 11. Major Changes in the Industry 166 A. Planting Methods and Seed Research 166 166 1. Spaced Planting 2. Seeding Rates 168 169 3. Seed Coating 170 4. Research on Seed Physiology 172 5. Research on Seed Quality 6. Research on Lettuce Seed Germination 173 7. Transplanting Methods 174 8. Sprinkler Irrigation 175 9. Fertilization 175 B. Harvesting and Shipping 176 1. Packing Methods 177 178 2. Mechanical Harvesting 3. Unionization 181 C. Shipping and Postharvest Quality 181 181 1. Transportation-Rail vs. Trucks 2. Quality Traits 181 a. Firmness 181 b.Decay 182 c. Visual Appearance 182 d. Physical Damage 182 164
T H E LETTUCE INDUSTRY IN CALIFORNIA
183 a. Russet Spotting 183 b. Rusty Brown Discoloration 183 c. Internal Rib Necrosis 184 d. Rib Discoloration 184 e. Brown Stain 184 f. Pink Rib 185 g. Low Oxygen Injury 185 4. Film Wrapping 185 185 D. Changes in the Research Sector 1.Cultivar Development 185 2. Disease Research 187 a. Lettuce Mosaic 188 b. Beet Western Yellows 191 c. Big Vein 191 d. Tipburn 193 e. Downy Mildew 195 3. Research on Insects and Nematodes 197 4. Weed Research 198 5. California Iceberg Lettuce Research Program 111. Literature Cited 199
165
3. Postharvest Disorders
199
I. INTRODUCTION Whitaker and Bohn (1953) reviewed the state of the lettuce industry in the Southwest. The thrust of their review focused upon the close cooperation that existed among research scientists such as plant breeders, plant pathologists, soil scientists, postharvest physiologists, and agricultural engineers. There also was close association among scientists, individual grower-shippers, and the organizations that represented them. This close cooperation gave the industry a solid scientific base for its operation, and helped answer many vexing production and postharvest problems. There remained, however, many unanswered questions to be grappled with during the 1960’s and 1970’s. It is our purpose in the following pages to review and assess the important advances that have been made by the lettuce industry in California during the past quarter century with the idea of establishing a firm benchmark from which future improvements and breakthroughs reasonably can be anticipated. A. Present State of the Industry 1. Area, Yield and Value.-There were 50,100 ha (123,600 acres) planted to lettuce in California in 1953. A quarter century later, in 1977, the area planted stood a t 63,400 ha (156,700 acres), an increase of 9,400 ha (23,100 acres) or roughly 15%. This compares to an increase for the
166
HORTICULTURAL REVIEWS
entire country from 85,000 ha (209,920 acres) in 1953 to 92,600 ha (228,700 acres) in 1977, an increase in 7,600 ha (18,800 acres) or about 8%. Thus the land planted to lettuce in California has increased twice as fast as in the remainder of the country (15% vs. 8%) for the period in which we are interested. The increase in California has been a steady one over the past 25 years. It is largely accounted for by new areas transferred to vegetable production from cereal crops. Table 4.1 shows the season, area, yield, price per unit, and value of the crop. The value of the crop has increased 286% for the past 25 years. Even allowing for a high inflation rate, it represents a solid advance. 2. Production Districts.-The traditional lettuce production districts have not changed much during the past quarter century, but there has been a significant addition through the development of two new areas, the central San Joaquin Valley (mainly Fresno County) and the southern San Joaquin Valley (Kern County), each with substantial plantings (see Table 4.2). Also, the Salinas-Watsonville district has been augmented by a considerable summer acreage in the King City area of southern Monterey County. Normally there is not a serious overlap in harvest dates between districts, but vagaries in weather patterns occasionally cause an overlap that results in a temporary glut with attendant difficult marketing conditions.
11. MAJOR CHANGES IN THE INDUSTRY
The lettuce industry has undergone major changes in the last quarter century. These span the entire array of practices for raising lettuce: planting, culture, harvesting, packing, and shipping. Some of these changes have arisen in the industry itself, utilizing the ideas of growers, seedsmen, researchers, engineers, and others. Many have come from the research people in the public institutions such as the USDA and University of California, including statewide and county extension workers. At least one major change, the unionization of field labor, has come about partly through social and economic pressure from outside the industry. Many of these changes have been directed toward, or in response to, a trend toward mechanization. A. Planting Methods and Seed Research 1. Spaced Planting.-Although interest in transplanting has been increasing, direct seeding is still the primary method of planting lettuce. Early in the past century, lettuce seed was sowed or drilled a t rather high rates. These ranged from about 1.1kg/ha (1lb/acre) in the central coast districts to about 3.4 kg/ha (3 lb/acre) in the desert areas, when planted in the traditional western manner on 2-row raised beds with 102 to 107
16,600 16,900 16,600 13,400
63,500
Total
50,100
Total
Winter Spring Summer Fall
(ha) 14.200 121100 10,700 13,100
Season Winter Spring Summer Fall
156,700
40,900 41,800 41,000 33,000
123,600
(acres) 35.100 291800 26,400 32,300
16,926
3,891 4,738 4,731 3,265
10,390
(1000 kg) 2.657 11970 3,186 2,576
41,806
9,612 11,704 11,685 8,065
22,857
(1000 cwt) 5.845 41335 7,009 5,668
Yield'
3.56
3.63 2.49 3.26 4.52
1.25
(100 kg) 1.13 1.09 1.43 1.35
($ )I
7.84 (Avg)
7.98 5.47 7.17 9.95
2.75 (Avg)
(cwt) 2.48 2.39 3.15 2.97
Price/Unit
304.9
76.7 64.0 83.8 80.4
78.9
17.9 13.0 27.3 20.8
($ million)
Total Value
In 1953, yield and price were stated for 1000 crates and price/crate, respectively. Assuming a weight of 90 lb/crate, the figures were multiplied by 0.90 to give yield in 1000 cwt and price/cwt (Johnson 1979). From these figures, metric yields and prices were calculated.
Source: USDA (1954, 1978).
1977
Year 1953
Area
TABLE 4.1. PRODUCTION OF CALIFORNIA CRISPHEAD LETTUCE IN 1953 AND 1977
168
HORTICULTURAL REVIEWS
TABLE 4.2. CALIFORNIA LETTUCE DISTRICTS, AREA AND HARVEST PERIODS FOR 1977
District Salinas-Watsonville-King City Santa Maria-Lompoc Central San Joaquin Southern San Joaquin Blythe Imperial
Area (ha) (acres) 29,200 72,200 6,000 14,700 5,000 12,300 2,200 5,400 3,500 8,700 16,600 40,900
Harvest Periods Spring; summer; early fall Spring; summer; early fall Early spring; late fall Early spring; late fall Early spring; late fall Late fall; winter; early spring
Source: Federal State Market News Service (1978a,b).
cm (40 to 42 in.) centers. This method of planting required over 988,000 seeds/ha (400,00O/acre) in the coast districts and as much as three times that amount in the desert areas. A t the above rates, seedlings emerged in a crowded condition in the row. As thinning was required to reduce the frequency in the row, large numbers of plants had to be eliminated and the remaining plants were likely to be damaged by the action of the metal hoe or by crowding. There were, therefore, several reasons for changing the seeding method and pattern, specifically by reducing the rate of seeding. The expected benefits were reduction and perhaps elimination of thinning costs, and less damage to surviving seedlings, with consequent increases in uniformity a t harvest. Three trends then were established: (1)seeding rates were reduced, (2) seeds were coated with various materials, and (3) research on seed traits was intensified. These trends took place simultaneously, emphasizing the fact that each seed was acquiring an identity. 2. Seeding Rates.-Seeding rates dropped quickly from the former rate to 0.6 kg/ha (0.5 lb/acre) and then to 0.3 kg/ha (0.25 lb/acre). This meant that seeds were dropped 2.5 to 7.6 cm (1to 3 in.) apart. They were individually spaced or spaced in groups or clumps a t an average desired distance. At wider spacings, it is easier to thin undesired seedlings without damaging those left in place. This is particularly important as a result of a new law in California prohibiting the use of the short-handled hoe. Instead of stooping low over the plants, the thinner stands nearly erect. As he is unable to separate plants with a free hand, the hoe itself must be used for this purpose. The wide spacings enable the thinner to eliminate unwanted plants without leaving an overabundance of doubles or damaging the plants. A t the higher seeding rates, seeds were sowed with the relatively simple Planet, Jr.' planter. For planting a t the lower rates, various planters were 'Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the U S . Department of Agriculture and does not imply its approval to the exclusion of other products that also may be suitable.
T H E LETTUCE INDUSTRY IN CALIFORNIA
169
devised to separate the seeds and plant them individually. The Stanhay' planter picks up coated seeds by means of a belt with appropriately sized holes that each hold one seed. The holes are spaced to provide a desired spacing in the seed row. The John Deere-Hansen' planter picks up coated or non-coated seed on a rotating plate with holes of appropriate size and spacing. 3. Seed Coating.-A lettuce seed is small, long, and narrow, and light in weight. These characteristics make the seed difficult to handle singly as compared to a larger, rounder, and heavier seed. A lettuce seed can be transformed into a more desirable shape and size by coating it with various substances. The first coating substances appeared in the late 1940's. Since that time, seed coating has become increasingly popular, and most lettuce seed is now coated. Several vegetable seed companies have developed their own coating processes. Each process varies in the nature and amount of coating material used, the shape of the pellet formed, and the method of assembling the pellet. In addition, attempts have been made to incorporate various useful substances (nutrients, herbicides, insecticides, and fungicides) into the coating material. There was a penalty for the convenience of using coated seed. Lettuce seeds germinate under relatively restricted conditions. Temperature and moisture are critical. The coating material is an additional barrier to the emergence of the developing embryo. Under conditions of high temperature and moisture stress, coated seed did not germinate as well as uncoated seed. Zink (1955) studied the effect of seed coating on germination, rate of emergence, plant stand, thinning time, and yield. The material used in coating was montmorillonite clay. Full-coated and non-coated seeds were planted a t the same rate. Both the number of plants that emerged and the rate of emergence were reduced significantly for the coated seed. The final plant stand after thinning, however, was the same for both types of seed. Thinning time was less for the coated seed, undoubtedly because of the reduced emergence. Yield from the coated seed was greater in some trials but was not improved in others. McCoy et al. (1969) compared mini-coated and non-coated seeds a t several spacings. They rated emergence and stand loss. They found no main effect germination differences between coated and non-coated seed, but coated seed emerged earlier under sprinkler irrigation compared to furrow irrigation. Stand losses a t higher planting rates-sowed, or spaced a t 5.1 cm (2 in.), 7.6 cm (3 in.), 10.2 cm (4 in.), and 15.2 cm (6 in.)-were negligible or a t least were acceptable. But a t the theoretical 'Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that also may be suitable.
170
HORTICULTURAL REVIEWS
planting-to-stand spacing, 30.5 cm (12 in.), the stand loss was unacceptably high with coated seed. The combination of sprinkler irrigation and uncoated seed gave an acceptably low stand loss even a t the plantto-stand spacing. Full-coated seeds were formulated a t a ratio of 50 parts clay coating to 1 part seed. The ratio was reduced to 1 O : l with mini-coating. New materials and methods largely have eliminated emergence problems (Johnson 1979). 4. Research on Seed Physiology.-The planting of lettuce seed a t reduced rates and wider spacing gave each seed greater identity than when sowed a t high rates. Surrounding the seed with a coating material placed constraints on its ability to germinate. These two facts focused attention on the seed, and stimulated seed research on the physiological and structural characteristics affecting germination, emergence, subsequent growth, and yield. The areas of research include light and thermally regulated seed dormancy, seed quality, and seed aging. Light and temperature are the two primary environmental factors affecting germination. Visible light promotes germination, whereas darkness inhibits germination. More specifically, red light (660 nm) promotes and far red light (735 nm) inhibits germination. The reaction is endlessly reversible, and depends upon the action of light on the pigment phytochrome. Red light converts phytochrome to a germination-promoting form, and far red light converts it to an inhibiting form. The last radiation exposure determines the pigment state and its effect on germination (Borthwick et al. 1954). Germination is affected by temperature. Lettuce seed germinates a t a range of temperatures, but the optimum is 18" to 21°C. At 25", some genotypes are inhibited. The degree of inhibition and the number of genotypes affected increase with increasing temperature. Gray (1975) found that the highest germination temperature permitting 50% germination for 'Hilde', a butterhead type, was only 25.7"C, while for the crisphead type 'Avoncrisp', the upper limit was 32.8'C. The upper limits for 20 other cultivars tested fell between these two extremes. In general, the upper limits for crisphead cultivars were higher than for cos, which were, in turn, higher than for butterheads. Light and temperature may interact in affecting germination. In addition, germination may be affected by seed moisture content and by the addition of certain chemicals. Ikuma and Thimann (1964) analyzed the physiological properties of germination by subjecting seeds to a range of temperatures during the several germination phases, and also conducted germination studies in a nitrogen atmosphere to analyze oxidative properties. They found that germination takes place in three phases:
T H E LETTUCE INDUSTRY IN CALIFORNIA
171
1. Pre-induction phase: Under an arbitrary standard temperature (25"C), this takes about 1.5 hours. Water is taken up and the rate of uptake increases with increasing temperature. During this period sensitivity to red light increases a t an increasing rate with higher temperatures. Subsequent germination is inhibited a t the higher temperature during this phase. The inhibition is weaker with exposure to red light. 2. Induction phase: During this phase, the seeds are a t maximum sensitivity to radiation. Reactions take place a t all temperatures and in the absence of oxygen and are, therefore, independent of these influences. 3. Post-induction phase: At 25"C, this takes about 9 hours. Immediately after exposure to red light, an oxidative process takes place, leading to an escape from the inhibitory effects of far-red light. This escape process is hindered by exposure to nitrogen early in the phase. This phase is temperature-sensitive; germination is inhibited a t high temperature and enhanced a t low temperature. This phase is followed by actual germination. Parallel work by Gray (1977) showed that the first four hours of inhibition and the period between the beginning of mitosis and emergence of the radicle were most sensitive to high temperature. These periods correspond to the pre- and post-induction phases described by Ikuma and Thimann. The interaction of temperature and light may vary depending upon the cultivar used. Heydecker and Joshua (1976) found that 'Cobham Green', a butterhead, was more sensitive to temperature than the crisphead 'Great Lakes'. 'Great Lakes', however, is more sensitive to light. Growth regulators can modify the effect of light on germination. For example, gibberellin overcomes the inhibitory effect of far-red light (Kahn et al. 1957). When ethylene and gibberellin together are added, the promotive effect is greater than with gibberellin alone. The enhancement is greater in red light than in far-red light. Other chemicals may overcome thermal dormancy. These include kinetin (Smith et al. 1968) and ethrel (Harsh et d.19731, and combinations of gibberellin and kinetin (Haber and Tolbert 1959) and ethylene and COz (Negm et al. 1972). Moisture is critical for germination. When the moisture content of the seed was lowered, either by drying to about 7% (Hsiao and Vidaver 1971) or to 6% by the use of water uptake inhibitors (Berrie et al. 19741, seed germination was reduced, possibly by an adverse effect on membrane permeability. Reynolds (1975) decreased the maximum temperature a t which lettuce seeds would germinate by making the osmotic po-
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tential increasingly negative. This effect was greater in the dark than in the light. Salts in the soil have deleterious effects on the growth of lettuce. One of these is inhibition of germination by the limitation of water uptake. This effect can be overcome with kinetin (Odegbaro and Smith 1969) or by kinetin plus gibberellin (Gray and Steckel 1976). 5. Research on Seed Quality.-Seed quality has been of great research interest. A paper by Scaife and Jones (1970) showed that fresh weight of lettuce plants a t harvest was directly and linearly related to the weight of the seeds, provided that the plants were grown under uniform conditions and in the absence of interplant competition. A series of papers was published shortly thereafter by 0. E. Smith, with his colleagues and students, exploring various aspects of the relationship between seed quality characters and subsequent growth and development. This work was parallel to, and stemmed from, the interest of the industry in the individual seed. The first task undertaken by the group was the development of a slant test for seed vigor. They (Smith et al. 1973a) measured maximum radicle length after three days of germination on slanted blotters immersed in water in the dark. Seed vigor, as measured in this manner, was considered to be a more realistic measure of seed quality than was germination ability. Seed weight, thickness, and width were tested as predictors of vigor. Seed weight was found to be the best indicator. A second paper (Smith et al. 1973b) showed performance differences in field trials between low vigor (light-weight)seeds and high vigor (heavier) seeds. Light-weight seeds emerged more slowly and the percentage of emerged seedlings was lower. Seedlings from light-weight seeds also were smaller a t thinning time. Yield from light-weight seeds was reduced in those trials in which the seeds were planted individually a t measured depth and spacing to minimize environmental differences. In a later paper, however, Soffer and Smith (1974b) found a growth advantage for heavier seeds during early growth, but not a t harvest stage. This work was done under closely controlled conditions in a growth chamber and in a hydroponic greenhouse. Correlations between lengths and weights of seeds were significant. Seed measurements were not correlated with final measurements including head weight. Two other papers by Soffer and Smith completed the series on seed quality. In the first (1974a) they studied flowering pattern and its relationship to seed yield and quality. Lettuce plants showed flowering peaks over a 70-day flowering period. Over 90% of the seed yield came from flowers opening in the first half of this period. Seeds from the first two flowering peaks were heavier than those from later flowers. Seed size was not related to the number of seeds per head. Neither seed yield nor
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vigor was affected by early harvest, or by removing water and nutrients at the middle of the 70-day flowering cycle. In the second study (Soffer and Smith 1 9 7 4 ~they ) found a relationship between nutrient supply and seed yield in soil-grown plants supplied by half-strength modified Hoagland's solution. Increased nutrient supply produced increasing, then decreasing, seed yields. Seed vigor, however, did not respond to increased nutrient supply. In a second experiment, they found that seed yield, weight per seed, and seed vigor increased linearly with increased N in hydroponic solution, but lipid and amino acid contents of the seed were not affected by N concentration. Although seed vigor increased, the level was low compared to that of soil-grown plants. They concluded that lettuce seed weight was useful in predicting seedling vigor only among seed lots grown under identical conditions. Lettuce seed does not store well. It has a relatively short storage life, which decreases with increasing temperature and relative humidity. Kosar and Thompson (1957) stored seeds a t relative humidities (RH) ranging from 0 to 100% for periods of up to 4 years. Viability remained high for the full 4 years a t relative humidities of up to 58%. At 67% and 75% RH, viability was reduced by as much as 100% after 1 year. When stored a t lO"C, they found that viability remained high a t any relative humidity up to 67%. Barton (1966) adjusted moisture contents of the seeds themselves, ranging from 5 to 50%, and stored them a t several temperatures (room, 5"C, -2"C, and -18°C) for periods of up to 18 years. At low moisture contents, the seeds remained viable a t 5°C up to 18 years. At -2°C and -18"C, they remained viable a t moisture contents of up to 19%. Loss of viability is the last stage of deterioration of stored lettuce seeds. The first stage is slower germination; this is followed by development of malformed seedlings and by the appearance of a disorder called "red cotyledon." This disorder is characterized by reddish necrotic spots on the cotyledon. The exact cause is unknown, but the disorder appears to result from aging and is accelerated under poor storage conditions. Bass (1970) found that storage a t low temperature and low relative humidity decreased the amount of red cotyledon in five cultivars. Storage a t -12°C and 70% humidity prevented red cotyledon completely for 4 years. 6. Research on Lettuce Seed Germination.-The practical impact of information on lettuce seed germination and viability is in the procedures used in planting to produce a final stand that will result in a maximum number of harvestable plants. This requires that growers be aware of the constraints on germination and emergence and on subsequent growth, and that they be able to minimize these constraints. Various measures are employed, including:
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1. Planting of seeds tested for, and having, a high germination rate. 2. Minimizing the effect of the seed coating by restricting the amount of material used to coat the seed, and by providing sufficient moisture to dissipate coating material from around the seed. 3. Use of sprinkler irrigation to leach salts below the germination line. Also, thermodormancy is a greater problem in the desert areas of California than in the coastal districts. Planting in the desert areas starts in August and September when air and soil temperatures are high, 40°C and 60°C, respectively, during the day. Sprinkling during the early evening cools the seed environment and the wetting starts the germination process during the cooler night hours. 4. Protection of the seed and seedling environment by use of preemergence herbicides, and by space planting to avoid overcrowding and damage during the thinning procedure. 5 . Use of other protective measures, such as chemical treatments to minimize loss of seedlings due to insects and diseases. 6. Use of alternative planting methods to avoid the hazards of germination.
Two planting methods enabling the grower to avoid the problems related to germination are available. One is the planting of germinated seed by a process called fluid drilling. The other is the transplanting of seedlings a t a later stage of growth. Fluid drilling is a two-part procedure. First, the seeds are imbibed (pregerminated) under optimum conditions. Then they are mixed in a gel material, which is extruded under pressure through the planting mechanism into the seed row. Seed spacing is regulated by the proportion of seeds to the volume of gel. The emergence of lettuce seeds imbibed for 24 hours and fluid-drilled was slightly faster than that for dry seeds, but the uniformity of emergence was substantially better for the fluid drilled seeds (Currah et al. 1974; Gray 1976). Gray (1978) found earlier and more uniform maturity for fluid-drilled than for conventionally planted crops for some plantings but no difference for others. He concluded that improvements may be obtained with fluid drilling as compared to dry planting in earliness and time of emergence, percentage of emergence, and crop uniformity. More consistent results than those presently obtained should be realized when more is known about specific factors of germination and emergence. 7. Transplanting Methods.-Although transplanting has been common practice in parts of the Southeast, it is a recent development in California. There are several advantages of this procedure. The plants are placed a t final stand spacing so that no thinning is required and losses due to diseases and insects are minimized. Plants can be chosen selectively to maximize uniformity. The amount of time the plants are in the
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field and subject to environmental stresses is reduced by about 20 days. Theoretically, a t least, uniformity a t harvest should be improved. The method of transplanting now used in California is called the Speedling method. Seeds are planted in a growing mix in Styrofoam containers with 120 cone-shaped cells. The containers are placed in a greenhouse where they are kept for about 28 days. Each cell has a hole in the bottom for drainage and the tap root is destroyed upon reaching this hole. Upon transplanting, the plant forms five or six secondary roots and a large number of feeder roots in the top few centimeters of soil. The effect of this on growth is not well understood. Transplanting is done with a standard cabbage planter and is a partially mechanized process. In Europe, much lettuce is transplanted in peat blocks. Blocks are placed by hand a t the desired spacing. The prospects for this procedure in California are not known a t this writing. 8. Sprinkler Irrigation.-Sprinkler irrigation for lettuce, initiated in the Imperial Valley in California in the late 1960’s, has become an accepted practice for lettuce culture through the state. It is used almost exclusively a t the time of germination and seedling emergence. The fields are prepared in conventional fashion with beds and furrows, but are sprinkle irrigated to prevent salt accumulation on the seed row surface a t emergence. After the seedlings emerge, the field is furrow irrigated, and the sprinkler equipment is moved to the next field where the process is repeated (Robinson 1972). The primary advantages of sprinkler irrigation are the prevention of surface salt accumulation on seed beds and the maintenance of more favorable soil aggregation. The higher emergence rates of lettuce seed achieved under sprinkler irrigation have ensured the feasibility of precision seed placement, and in turn, the use of mechanical thinners and long-handled hoes. Secondary advantages of sprinkler irrigation are more uniform development of the plants, leading to the possibility of a single harvest, improved water use efficiency, increased land use efficiency, and saving of irrigation labor requirements (Robinson 1969). Sprinkler irrigation must be considered as one of the most beneficial practices to have entered the lettuce production picture during the past 25 years. 9. Fertilization.-In spite of relatively low nutrient requirements, a good crop of lettuce cannot be grown without the aid of mineral fertilizers and it does best on soils of high native fertility. In nutrient studies in the Salinas Valley, Zink and Yamaguchi (1962) found, averaging 15 fields, that lettuce removed 107 kg/ha (95 lb/acre) of nitrogen, 30 kg/ha (27 lb/acre) of phosphoric acid (P206),and 234 kg/ha (208 lb/acre) of potash (KzO). These are indeed modest requirements as compared with most other vegetable crops. Most of the uptake (about 70%)occurs in the last 3 weeks of growth before harvest.
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Of the three major elements applied in commercial fertilizers, nitrogen and phosphorus are most likely to be deficient in California soils. Potassium is usually in sufficient supply (Whitaker et al. 1974). Recently substantial research has taken place on the growth response to specific elements and on methods of testing for elemental presence in the plant as a means of determining the effectiveness of the fertilization program. Berry (1971a) devised a procedure for evaluating the phosphorus status in seedling lettuce, establishing critical levels for evaluation of various parts of the seedling. Similar criteria were established for potassium in seedling lettuce (Berry and Carey 1971) and for zinc (Berry 1971b). Scaife and Smith (1973) proposed a computer simulation model of phosphorus uptake and lettuce growth, in which they broke the P response down to specific components. Temple-Smith and Menary (1977) compared lettuce and cabbage response to phosphorus and found the lettuce to require higher levels of phosphate in solution in order to achieve the same relative growth rates. Several areas of nitrogen fertilization have been explored. Grogan and Zink (1956) found that highly ammoniated nitrogen fertilizers appeared to be responsible for a constriction and browning of the roots that later came to be known as corky root rot. Work in Wisconsin (Amin and Sequeira 1966) indicated toxic lettuce residues as the cause, and recent reappearance of the problem in the Salinas Valley indicates a more complex situation may be involved. Recommendations for fertilizer use vary from district to district and season to season. As an example, a current recommendation for the Imperial Valley is as follows: 168 kg/ha (150 lb/acre) of 11-48-0 (oxide) broadcast before planting and listed into the beds, followed by 93.5 literdha (10 gal./acre) of 10-34-0 (oxide) liquid injected 7.6 to 10.1 cm (3 to 4 in.) under the seedline. This provides ample phosphorus for early growth and does not add too much nitrogen (Mayberry 1979). Some work has been done on micronutrients. Zink (1966) demonstrated that on certain soils of the Salinas Valley, growth and maturity were accelerated by the application of 11.2 to 38.2 kg/ha (10 to 34 lb/acre) of zinc sulphate. It has been proposed (Welch et al. 1979) that nitrapyrin, if registered for use on vegetables, might be used to stabilize nitrogen in the NH, form, prevent its loss by leaching, and therefore help to reduce costs of fertilizer application.
B. Harvesting and Shipping The most radical and far-reaching changes in the California lettuce industry have taken place in the harvesting and marketing procedures.
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Except for harvest mechanization, these changes have originated and developed in the industry itself. 1. Packing Methods.-In the early 1950’s the practices of packing lettuce in cardboard cartons and of vacuum cooling were still relatively new. Since then, they became and have remained the standard methods of handling lettuce a t the shipping point. In conventional harvest, lettuce heads are cut by hand, trimmed to several wrapper leaves and packed in a corrugated cardboard container. They are usually placed in 2 layers of 12 heads each. The standard carton is of sufficient size to hold 24 heads weighing about 1 kg (2.2 lb) each, resulting in a total carton weight of about 24 kg (52.8 lb) (Fig. 4.1). An alternate method is the wrap-pack. Most lettuce is now sold in supermarkets in a film wrap. This wrapping may be done in the market itself or a t the shipping point. In the latter case, it is done in the field a t the time of harvest. Heads are cut, trimmed of all wrapper leaves, and placed on the “wings” of a vehicle moving slowly through the field. The heads are wrapped in a clear plastic material, which is heat sealed. The heads are conveyed on a belt to a point where they are loosely packed in a carton that is taller and narrower than the conventional one. After packing by either method, the cartons are loaded on trucks and taken to a vacuum cooling plant. Lettuce trucks are designed for produce handling. They have six wheels, with each pair of rear wheels in tandem. The wheels are 203.2 or 213.4 cm (80 or 84 in.) apart, in order to enable the truck to straddle two beds in the field. The cab has room only for a driver and the bed is flat and holds 320 cartons in the standard load. A t the cooling plant, the pallets holding the cartons are removed from the truck, placed on flat cars, and wheeled into the vacuum tube. This is sealed and a vacuum is drawn either mechanically or by steam jet. The lettuce is cooled by evaporation of water in the head to just above 0°C. This procedure usually takes about 10 to 30 minutes, depending upon the temperature of the load a t the start. After cooling, the lettuce is then loaded onto a conveyor belt, which carries it to a railroad car or truck trailer for shipping. Recently, a new method of handling lettuce has been devised, in response to the growth of the fast-food restaurant industry. Lettuce is marketed in a shredded form to such restaurants for use in hamburgers, tacos, salads, and other dishes. Most of the lettuce used is from fields that have already been partially harvested. The remainder is cut, loaded in bulk containers and carried to a central station. The lettuce is cored, shredded, cooled, and washed with cold water. It is packed in plastic bags, often with shredded carrot and red cabbage, which are placed in containers for shipping.
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Courtesy of Western Grower and Shipper FIG. 4.1. CUTTING AND PACKING CRISPHEAD LETTUCE IN A TYPICAL 24-HEAD CARTON
A relatively small proportion of lettuce is now shredded, but in the future, this proportion may increase. Foster (1978) proposes, on the assumption that over 95% of lettuce is consumed in the shredded form, that most lettuce should be marketed in that way. He cites as advantages that fields could be cut once, that yields would be higher, utilizing all the lettuce in the field, and that simpler, cheaper, non-selective harvesters could be used. 2. Mechanical Harvesting.-Several types of selective mechanical harvesters have been developed, either experimentally or to the point of
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commercial acceptance. Early models used pressure-sensing devices to detect mature heads by size and firmness. A University of California model had a selector unit t h a t pressed down on the head from above, while one developed a t the University of Arizona squeezed the head on the sides (Harriott and Barnes 1964; Garrett et al. 1966). Pressure selection may damage heads left in the field for late harvest, so that a search for a selector that would not touch the heads was conducted. This resulted in the development of a gamma ray sensor by the University of California and an X-ray selector by the USDA (Garrett and Talley 1970; Lenker and Adrian 1971). The principle of radiation sensing is that the denser, and therefore, the more mature the head, the greater the obstruction to passage of the beam through the head. The head can be accepted or rejected on this criterion. If accepted, a knife that cuts the head is activated. If rejected, the head is passed over. Refinement of the X-ray model has continued with the addition of a mechanical trimmer. In present models, the head is cut, oriented with the stem end passing over rotary trimming knives, trimmed, and conveyed to the back of the machine, where it is ready for packing (Adrian et al. 1976). A non-selective lettuce harvester has been developed a t Cornell University. I t lifts heads and roots and is appropriate for eastern muck plantings where lettuce is usually cut once only, and the soil is loose enough to pull up the entire plant. Roots are trimmed off on the machine (Shepardson et al. 1974). Mechanical harvesting is a desired goal among many lettuce growers, principally as a means of reducing the relative cost of harvest. Although the machines have deen devised, mechanical harvesting is not yet a reality. There are several reasons for this. Lettuce is now packed into cartons. The packing is tight and requires considerable force to get the heads into the carton. There is disagreement in the industry as to whether to preserve this method of packing or discard it in favor of a bulk method requiring less work and precision. The volume of lettuce arriving a t the back of the harvester may be too great (even a t low ground speed) to allow packing by the conventional method except with many packers on a platform so large as to make the equipment unwieldy. An alternative method is to load the lettuce in bins and move them to the side of the field for packing. Loading in bulk is the third alternative. There is some resistance to this because it requires changing the entire system as far as the retail outlet. These changes would include the method of truck loading in the field, handling a t the distribution centers, and handling in the supermarket storerooms and a t the produce counter. I t would require changes in loading equipment, storage facilities, door sizes, and inside dimensions of containers and cars for most efficient use of space.
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A second uncertainty is that of cost. The cost of investing in a selective harvester, which will be high, must be balanced against the cost of present labor use. Zahara et al. (1974) studied labor requirements and harvest costs for the conventional hand harvesting system and for a projected mechanical harvesting system. First, they compared present and past practices and found that the average time for harvesting a carton of lettuce had decreased substantially from 12.7 minutes in the period of 1960 to 1963 to 3.6 minutes in 1970 to 1973. Several reasons were given for this. The number of harvests per field had been reduced. Crew assignments had been changed to increase efficiency even with reduced crew size. Pay incentives had been increased with the institution of piece-rate payments. On the basis of results with an experimental one-bed harvester, they calculated that the cost of mechanical harvest would be $0.29 per carton, compared to the cost of hand harvest of $0.45 per carton. Most of the cost would be due to labor, and the cost of investment in the machine itself would have little effect on the cost per carton. In a later study, Johnson and Zahara (1976) considered the impact of mechanization on the labor force in California. They assumed a low rate of adoption of the machine by lettuce shippers, year-round use, wage scales extant at the time of the study, and standard rates of harvest, machine output, and worker output. Of several alternative methods of packing, they compared the conventional hand pack with two mechanized systems: regular (naked) pack on the machine and a fieldside shed system for wrapping. On average, worker loss of 1.56% of the total was estimated to occur with the adoption of a mechanized system a t the rate of 5% per year. Rates of research investment and economic return also were calculated and showed a positive rate of return. They concluded that it would be justifiable for some form of compensation to be made to job-losers. A recent paper considers the conditions affecting whether or not the industry makes the transition to mechanical harvesting (Friedland et al. 1979). They attribute the delay in transition to development of the crew system in which there is efficiency, stability, and high productivity, and the uncertainty over handling after harvest. The circumstances leading to mechanization would be disruptions in labor supply, increased wage demands, and the prospect of participation in management decisions by labor. They also consider the possible consequences of mechanization. These include loss of jobs, transfer of job availability to the agricultural equipment industry, an increase in the proportion of female workers, stabilization of the job structure in the industry, and concentration of lettuce production among fewer firms.
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3. Unionization.-After the labor strife of 1936, the shed workers of the industry became unionized. In 1961, the AFL-CIO United Farm Workers Organizing Committee attempted unsuccessfully to organize field workers. One major shipper affiliated with the Teamsters Union a t that time. After a successful boycott campaign, UFWOC organized the grape field workers in the San Joaquin Valley in 1970. Under the leadership of Cesar Chavez, they attempted to organize the lettuce workers. Many shippers signed with the Teamsters Union a t that time. However, after several years of competition, election, and some strife, the Teamsters withdrew from the field and most contracts were signed with the United Farm Workers. The remainder of the workers remained either with the Teamsters, with a new independent union, or joined no union.
C. Shipping and Postharvest Quality 1. Transportation-Rail vs. Trucks.-Maintenance of quality is vital in long-distance shipping of a perishable product. Concern for quality was a natural consequence of changes in shipping methods that occurred in the lettuce industry over the past quarter century. This concern stimulated much research on postharvest quality and postharvest disorders. By 1950, most lettuce was shipped from California in ice-cooled railroad cars. The use of vacuum-cooled cardboard cartons had eliminated ice in the package and on top of the load. Cooling was obtained by the use of ice in bunkers on either end of the car and the cooled air was circulated through the load with fans. These cars were relatively small and the cooling was relatively inefficient. They were gradually replaced by larger mechanically refrigerated cars, eliminating the use of ice completely. Some lettuce also was shipped in refrigerated truck trailers. Until recently, about 90% of shipped lettuce was carried by rail car. However, because of disagreements over rail rates and other shipping factors, the ratio of railroad cars to trucks changed quite rapidly. In 1977, 78,445 carlot equivalents (1,000 carton lots), or 84%, were shipped by truck and only 15,545 cars (16%) by rail (Federal State Market News Service 1978). Present fuel costs and supply prospects may alter this ratio in the future. 2. Quality Traits.-The quality traits for which there is concern and in which great variation may exist are firmness, decay, general visual appearance, physical damage, and several postharvest disorders.
a. Firmness.-The optimum stage for firmness is a fully matured head, well filled with leaves and yielding slightly to pressure. Firmness reflects maturity. A head harvested too early will be poorly filled and soft. An
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overmature head will be quite hard and may have cracked or broken ribs (Kader et al. 1973b). Firmness is a basic quality trait. A hard overmature head is likely to be bitter. The outer leaves may be yellowed and the inner ones bleached white. Not only is an overmature head more susceptible to physical damage, but it is more likely to be subject to some postharvest disorder.
b. Decay.-Decay is caused by one or both of two organisms. Pseudomonas spp. produce bacterial soft rot, the more important of the decay problems. Botrytis cinerea Pers. ex Fr. incites gray mold. In rating postharvest problems of California lettuce on the Chicago market in 1973 and 1974, Beraha and Kwolek (1975) found twice as much decay in lettuce from the coastal districts in July as a t other times or in other districts. They also found no correlation between the incidence of decay and the incidence of other disorders, including crushing and bruising, tipburn, russet spotting, rusty brown discoloration, brown stain, pink rib, and rib discoloration. c. Visual Appearance.-Lettuce is marketed on the basis of its visual quality, as are all produce commodities. Defects in appearance detract from sales appeal. These defects include blemishes, breaks, tears or holes, dirt, insects, and wilting. Shipment under various conditions of controlled atmosphere to maintain visual quality has been of interest. In particular, addition of small amounts of carbon monoxide retards discoloration and other oxidative effects. However, with combinations of low O2 and high C02, CO may increase brown stain (see below). Kader e t al. (1973a) tested the effects of CO on visual quality a t levels of C02 not conducive to development of brown stain. When lettuce heads were held a t 2.5"C for 10 days, a t various levels of 0 2 and either 0% or 1% C02,followed by 4 days in air a t 10°C, the visual quality was good a t all treatments after the 10 days, but was reduced to fair after 4 additional days in air. When held for 20 days in controlled atmospheres, treatment differences appeared. After the 20 days, visual quality was best (fair) on the heads a t 5 or 10% 02,1% C o n , and either 0% or 1% CO, and poorer a t either 2% or 21% 02.After four days in air, visual quality deteriorated to the unsaleable class. This emphasizes the temporary effect of controlled atmospheres and the loss of effect when the lettuce is removed to air.
d. Physical Damage.-Physical damage refers primarily to crushing and bruising. Beraha and Kwolek (1975) found this to be the major problem with lettuce on the Chicago produce market. It reached a peak in September shipments from the coastal district. At that time, 63% of the heads showed damage. Lettuce heads are usually largest during this
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period and more difficult to squeeze into the carton, a situation which probably accounts for the increase in damage. 3. Postharvest Disorders.-In the ratings by Beraha and Kwolek (1975) of postharvest problems, russet spotting and rusty brown discoloration were considered as major problems along with physical damage and decay. Brown stain, tipburn, pink rib, and rib discoloration were less common. Incidence varied by season, and there appeared to be differences attributable to cultivars and to rate of growth and harvest size.
a. Russet Spotting.-This consists of clusters of olive-brown spots on the lower midribs of outer leaves. I t may occur on both sides of the midribs, and in severe cases the spots may become quite large and appear on the leaf blades as well. Russet spotting is induced by ethylene produced either by the lettuce itself or by other ripening produce, or from outside sources. The incidence is increased on more mature hard heads and on heads kept a t higher-than-optimum temperature (0°C) (Rood 1956). Beraha and Kwolek (1975) found that the incidence of russet spotting was higher on desert-grown lettuce than on coastal lettuce, possibly because the desert lettuce was firmer. The difference also may have been due to the different cultivars grown in the two areas. Lipton (1963) found that high temperatures 9 to 14 days before harvest led to higher incidences of russet spotting after harvest than did lower, more optimal temperatures. In a more recent study, Morris et al. (1978) showed that russet spotting can be induced by ethylene a t 0.1 ppm in the atmosphere. Development was accelerated a t temperatures over 5°C. The incidence is higher on susceptible cultivars, overmature heads, and when the interval between harvest and consumption becomes excessive. Heads in good condition produce little ethylene. Heads damaged physically or by pathogens may produce ethylene a t a high rate. They also studied the environments in which ethylene may be produced a t high levels. These include (1) cold storage in which there are forklift trucks with fuel emissions, particularly from propane, (2) retail storage rooms with ripening fruit, and (3) the home refrigerator, also with ripening fruit. Ethylene damage can be avoided by the use of non-emitting fuels in forklift trucks, air flushing of confined spaces, wrapping of lettuce in polythene, or by the use of gas-capturing devices.
b. Rusty Brown Discoloration.-This is a reddish brown discoloration of the midrib and nearby tissue on outer leaves. It occurs on ‘Climax’, a midwinter cultivar grown in the Imperial Valley. Ceponis et al. (1970) described and named the disorder. They reported that 90% of the lettuce
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arriving on the New York market in February 1969 was affected. Coakley et al. (1973) induced symptoms of rusty brown discoloration in heads of lettuce inoculated with lettuce mosaic virus a t relatively late stages of growth followed by storage a t 1°C. c. Internal Rib Necrosis.-Considered a postharvest problem, this actually occurs in the field. I t is also a seasonal, cultivar-specific problem, occurring on mosaic infected ‘Climax’ in the midwinter desert season. I t is a gray or black discoloration of the lower midrib near the base of the leaf (Johnson et al. 1970; Coakley et al. 1973). Zink and Duffus (1972) found that lettuce mosaic alone induced symptoms on ‘Climax’. However, they found that symptoms could be induced in ‘Vanguard’ also when both lettuce mosaic and beet western yellows viruses were present. No symptoms were induced in other cultivars tested. Both rusty brown discoloration and internal rib necrosis are associated with lettuce mosaic, and both are essentially controlled when lettuce mosaic is controlled through use of mosaic-free seed in desert plantings of ‘Climax’. Further guarantee of control will occur when ‘Climax’ is replaced by another cultivar resistant to mosaic or a t least to the subsequent effects.
d. Rib Discoloration.-Sometimes called rib blight or brown rib, this occurs on the midrib of the outer head leaves, usually where the rib curves. It appears on the inner (adaxial) surface. The discoloration is a t first yellow or tan, becoming brown or black. The cause is unknown, but the discoloration appears to be favored by higher temperatures (Lipton et al. 1972). e. Brown Stain.-Lettuce shipped in an excess carbon dioxide atmosphere may show injury due to a disorder called brown stain. Small sunken lesions with dark edges occur on either leaf surface, usually near the leaf base, and on or near the midrib. Lesions are water soaked when young, but become darker and may coalesce when the injury is severe. Heart leaves in injured heads may have reddish brown margins or the entire leaves may be discolored (Stewart et al. 1970; Lipton et al. 1972). Brown stain was first observed on the New York market in 1965. Incidence increased in subsequent years. In 1969, 25% of heads sampled from the California coastal districts were affected (Ceponis and Kaufman 1970). There is probably a cultivar effect on the incidence of the disorder. Shipments of lettuce from the coastal districts showed more brown stain than those from either the desert or the San Joaquin Valley (Ceponis and Kaufman 1970; Stewart and Matoba 1972; Beraha and Kwolek 1975).
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Brecht et al. (1973) found th at the incidence of brown stain increased as the level of CO, increased from 1 to 50% and as 0, decreased from 21 to 1%.Although CO alone has no effect, Kader et al. (1973a) found t h a t when CO was present, brown stain increased a s CO, level increased, regardless of the 0, level.
f. Pink Rib.-In mild cases of p i n k rib, the midrib of outer leaves of th e head shows a diffuse pink discoloration near the base. This disorder may be quite severe, affecting all but the inner leaves of the head and extending well up the midribs and into the larger veins a s well. Pink rib may appear on plants still in the field before harvest. I t is more common, however, as a postharvest problem. It occurs more commonly on overmature heads and is likely to be more severe under high transit temperatures and under low O2 atmospheres (Marlatt and Stewart 1956; Lipton e t a1 1972). Hall et al. (1971) found the bacterium Pseudomonas marginalis Brown (Stevens) in pink rib lesions. Lettuce inoculated with the organism a t low temperatures (2°C and 8.6”C) developed pink lesions after 7 days. At higher temperatures (15.5”C and 22.2”C) brown lesions appeared. g. Low Oxygen Injury.-This is a postharvest disorder. I t was not rated by Beraha and Kwolek (1975). Low oxygen injury occurs on lettuce shipped in a low O2 atmosphere. Wrapper and cap leaves on the head develop patches of shiny or watersoaked dead gray patches. Young heart leaves may turn reddish brown (Lipton e t al. 1972). 4. Film Wrapping.-Film wrapping of produce became common in the mid 1940’s a t one of the receiving points of the shipped produce, usually the supermarket. Wrapping a t the shipping point became important later. Field or shed lettuce wrapping has been practiced since the early 1960’s. T he effect of film wrapping on quality was studied by Ceponis a n d Kaufman (1968). They found less wilting of wrapped than of unwrapped lettuce. However, they sprayed aqueous spore suspensions of Botrytis cinerea Pers. ex Fr. on both types and found more decay on the lettuce in the film wrap.
D. Changes in the Research Sector 1. Cultivar Development.-In the early 1950’s, most of the lettuce grown in California were cultivars of the ‘Great Lakes’ type. Nearly all the lettuce in the Salinas Valley was of this type. In the desert districts much of the lettuce was still of the ‘Imperial’ type, including particularly ‘Imperial lOl’, ‘Imperial 615’, and ‘Imperial 847’.
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In the late 1950’s, R. C. Thompson of the USDA released four cultivars, which very quickly became dominant in the desert districts. One was ‘Empire’, released in 1956. It eventually became the major fall cultivar. Another, released in 1957, was ‘Merit’, a big vein tolerant cultivar which was planted during a short period just after ‘Empire’. A third was ‘Climax’, released in 1958. Several years later it replaced ‘Imperial 101’ as the principal mid-winter cultivar. ‘Vanguard’, released in 1958, soon became the most important cultivar for spring harvest in the desert (Thompson and Ryder 1961). ‘Great Lakes 659’ also became an important early fall and late spring cultivar (Fig. 4.2).
FIG. 4.2. TYPICAL HEAD OF ’CLIMAX’ LETTUCE
In the coastal districts, ‘Great Lakes’ cultivars were solidly entrenched in the 1950’s and early 1960’s. The principal strains were ‘Great Lakes 118’’ ‘Great Lakes 366’’ ‘Great Lakes R-200’, ‘Great Lakes 65’, ‘Great Lakes 659’’ ‘Great Lakes 66’’ and ‘Great Lakes 407’. In 1960, ‘Calmar’ was released by J.E. Welch of the University of California, Davis (Welch et al. 1965). By 1966, it comprised nearly all the lettuce planting in the
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Salinas and Santa Maria Valleys. It remained the dominant cultivar for about ten years, although for summer plantings it eventually was replaced by ‘Montemar’ (Ferry-Morse Seed Co. release) and several other cultivars. In 1975, E. J. Ryder of the USDA released ‘Salinas’, a cultivar of the ‘Vanguard’ type. By 1978, it had established itself as an important 4.3). cultivar in the Salinas Valley (Ryder 1 9 7 9 ~(Fig. ) Other cultivars which have been released recently and found a place in the desert areas are ‘Winterhaven’, released by Harnish-Brinker Seed Co. for the later winter-early spring period in the desert, and ‘Red Coach 74’ and ‘Moranguard’, from Quali-Sel and Moran Seed Co., respectively, for the same period. ‘Valmaine’, a cos, and ‘Valrio’, ‘Valverde’, and ‘Valtemp’ were released by P.W. Leeper of the Texas Agricultural Experiment Station with T . W. Whitaker and G. W. Bohn of the USDA primarily for the Rio Grande Valley, but all except ‘Valverde’ are grown also in the California and Arizona desert valleys (Leeper et al. 1963, 1969). ‘Vanguard 75’, the first mosaic-resistant cultivar, was released in 1975 (Ryder 1979d). For the coastal districts, ‘Calmaria’, ‘Morangold’, and ‘Cal K-60’, from Moran Seeds, are occupying some plantings. Many other cultivars from both the public and private agencies have been released and either have fallen by the wayside or have not yet become established. I t is reasonable to think that the industry will continue to depend upon several cultivars in each location. The temperature, humidity, daylength, and light intensity change sufficiently through the growing season that it is unlikely that one cultivar will be adapted widely enough to perform equally well in all environments. Although ‘Calmar’ occupied the Salinas Valley for nearly the entire season for a few years in the rnid-l960’s, it was quickly replaced in certain environments by new cultivars when they became available. Specifically, ‘Calmar’ tended to be oversized and puffy in the summer and largely was replaced in that period by the smaller, firmer ‘Montemar’. 2. Disease Research.-In the early 1950’s, there was concern in the industry over several problems. Downy mildew continued to be a problem with the appearance of a new race, to which the Great Lakes and Imperial types were susceptible. A problem called June yellows, evidently complex, was causing severe damage in the Salinas Valley. Most of the cultivars were susceptible to big vein in the spring and tipburn in the summer. In the ensuing quarter century, much research was conducted on the components of June yellows and on lettuce mosaic, beet western yellows, downy mildew, tipburn, and big vein.
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FIG. 4.3. TYPICAL HEAD OF ‘SALINAS’ LETTUCE
a. Lettuce Mosaic.-In the early and mid-l950’s, lettuce mosaic was a worldwide problem wherever lettuce was grown. It was particularly serious in areas like the Salinas Valley where lettuce was grown continuously over a long period of time. Work in England by L. W. Broadbent, G. C. Ainsworth, and others had disclosed much about the nature of the disease: that it is virus caused, spread by aphids and seedborne, and about patterns of spread, etc. According to Grogan et al. (19521, the spread of mosaic could be minimized by the use of mosaic-free seed, thus controlling the primary source of inoculum. Zink et al. (1956) found that the percentage of plants that develop mosaic depends upon the amount of seedborne virus and the number and activity of aphid vectors. In 8 trials, in each of which the initial seedborne transmission was 1.6%, the average infection level a t time of first harvest was 29.5%. When the initial rate was O.O%, the average infection a t first harvest was only 3.4%. At 0.1%. it was 7.6%.
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In 1958, an ordinance was passed in Monterey and Santa Cruz counties prohibiting the planting of seed containing greater than 0.196 seedborne infection. Several years later, this was amended, setting the requirement a t zero infection in 30,000 seeds. Seedborne transmission was tested by visual inspection of seedlings a t about the 3- to 4-leaf stage. Seed was tested first by the seed companies, and later by a growers’ committee. Pelet (1965) showed th at seedborne virus could be assayed by grinding seed in buffer solution and rubbing it on leaves of Chenopodium quinoa Willd. The appearance of local lesions indicates th a t the virus is present. This method was taken up by some of the seed companies and by the growers’ association in the Imperial Valley. In the interim, searches for alternate methods of control were begun. At the University of California, Couch (1955) found th a t the English butterhead ‘Cheshunt Early Giant’ failed to transmit the virus through the seed even though infected. Forms of wild lettuce (L. serriola) also showed this property, and a program to exploit this character through development of non-transmitting cultivars was initiated by J. E. Welch. The USDA began a program of searching for a source of resistance to mosaic. This was successful with the location of resistance in three wild lettuce collections from Egypt (Ryder 1968, 1970b). Earlier, resistance was identified in ‘Gallega’, a Latin-type lettuce Won der Pahlen a n d Crnko 1965). Both types of resistance were shown to be identical a n d controlled by a single recessive gene (Ryder 1970a). Several aspects of the nature of resistance were explored. As the same allele confers resistance in each source, as well a s in two Spanish cultivars, ‘Madrilene’ and ‘Mataro de 10s Tres Osos’, a probable evolutionary relationship is suggested. Lettuce evolved in the Mediterranean basin and it is probable th at one of the wild forms there was segregating for resistance, and both the susceptible and resistant alleles passed into domesticated populations (Ryder 1976, 1979b). Resistance appears to be due to a relatively low rate of multiplication of the virus or a low rate of movement in the plant. About three weeks after inoculation, one to several chlorotic lesions appear on leaves younger than those inoculated. Th e infection is systemic. Symptoms appear several days to two weeks later than on susceptible plants. Resistant plants also exhibit resistance to infection, as the proportion of escapes is higher than t h a t observed with susceptible plants (Ryder 1976). Symptom expression varies with the environment. In greenhouse a n d growth chamber studies, symptom expression was restricted and the number of escapes higher during warm periods. Under cooler conditions, symptoms were sometimes widespread enough to make the plants appear to be susceptible (Ryder 1976). Seed transmission of virus by infected resistant plants occurs a t a very low rate compared to susceptible plants. In one series of experiments,
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91% of resistant plants tested did not transmit. Only 16% of susceptible plants did not transmit. Of those plants transmitting the virus, the rate was 0.49% for resistant plants and 3.40% for susceptible plants (Ryder 1973). Several factors evidently interact in causing a plant to transmit, as it evidently is not a mechanism simply switched on or off, but rather a series of mechanisms that decide first on whether a plant will transmit and then, if so, how much. Two methods of control of lettuce mosaic are now available. Seed indexing has been used since 1958 in the Salinas-Watsonville district and more recently in other districts. When properly observed and enforced, it has been extremely effective, whether the seedling test or the Chenopodium test was used. As an example, indexing became mandatory in 1969 and mosaic was essentially eliminated. Since then, internal rib necrosis, a mosaic-caused disorder in ‘Climax’, also has become virtually non-existent (Kimble et al. 1975). With the 1975 release of ‘Vanguard 75’, a mosaic-resistant crisphead cultivar, protection by resistance became a reality. This method offers an important advantage over seed indexing; it is not subject to human error (Ryder 1979d). There is, however, the possibility of a new virulent virus form appearing, a development which would require further search for other sources of resistance. The two methods are compatible in the sense that resistant lettuce can be indexed for seed transmission. Whereas inoculated resistant plants show restricted chlorotic lesions that are difficult to detect, resistant seedlings with seedborne infection produce symptoms exactly like those on susceptible seedlings and are easily observed (Ryder 1979d). I t may be necessary to continue the indexing program until growers and seedsmen are convinced that there is little or no danger of virus spread from resistant to susceptible lettuce. A number of fundamental and practical studies on the nature of the disease have been conducted during the past quarter century. McLean and Kinsey (1962) identified three variants of the virus. These were not separable on ‘Great Lakes’, but showed differences in symptom expression or in transmission characteristics when tested on ‘Parris Island’, a cos type, and the non-related species, garden pea, and common groundsel. In a later paper, a fourth variant was identified (McLean and Kinsey 1963). This variant acted as a lethal. Zink et al. (1973) found a variant lethal to crisphead cultivars that are resistant to downy mildew and susceptible to turnip mosaic, another virus disease. The two lethals were probably different. Seed transmission is characteristic of lettuce mosaic virus. Couch (1955) found much variation in rate of transmission among plants of ‘Bibb’, a butterhead cultivar. Single plant transmission varied from 0.2 to 14.2%, with an average of 7.9%. Most crisphead cultivars show similar variation
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in single plant tests in the greenhouse, but a t a lower average level. Transmission in the field has been found to range from 1 to 3%. T h e non-transmission of ‘Cheshunt Early Giant’ found by Couch (1955) is evidently due to a hypersensitive reaction leading to complete abortion of seeds from the early flowers. The virus is transmitted primarily through the ovule. In a study with reciprocal crosses of all combinations of diseased or healthy male-sterile or male-fertile plants, the transmission rate was 5.5% through the ovule and only 0.2% through the pollen (Ryder 1964). Seed production is reduced drastically in mosaic-infected plants. In a greenhouse study, the virus reduced total seed weight by 62% and the number of seeds by 69%. Mosaic virus also caused a delay in flowering and a reduction in seed stalk height (Ryder and Duffus 1966). Lettuce mosaic reduces yield of lettuce. Part of the yield loss is the reduction of rate of growth and final weight. This was shown in a study by Zink and Kimble (1961). In two trials they inoculated ‘Great Lakes 118’ a t 41,56, and 63 days (Trial 1)and a t 29,43, and 64 days (Trial 2) after planting. The earlier the infection, the greater the reduction in growth rate and final weight. Plants were rendered unmarketable by reduction in size or poor head formation. T h e percentage of unmarketable heads was greater with the earlier inoculations. Poor appearance due to disease symptoms accounts for the other part of yield loss.
b. Beet Western Yellows-For many years, the “June yellows” complex was considered to be a result of activity by lettuce mosaic virus and nutritional factors. However, Duffus (1960) proposed that beet western yellows (formerly radish yellows) might be an important constituent of June yellows. Beet western yellows is known to infect 146 species in 23 plant families. These include such crops as sugar beet, table beet, spinach, lettuce, cauliflower, broccoli, radish, turnip, pea, broad bean, and flax (Duffus 1973). Beet western yellows virus in lettuce causes an interveinal yellowing on the outer leaves. In severe cases, the entire leaf may be yellowed and inner leaves also may be affected. Cultivars differ in degree of yellowing, and in general the butterhead lettuces seem to be more severely affected as a group than the crispheads. Although lettuce cultivars react differently to beet western yellow virus, no specific genetic resistance or tolerance has been identified. Actual crop losses from the disease on butterhead cultivars have been reported in England. Symptoms were identified on all of 68 cultivars in trial (Watts 1975). Tomlinson et al. (1976) found that symptoms of beet western yellows were completely suppressed in nearly all plants sprayed with a substance called methyl benzimidazole-2-yl carbamate or carbendazim.
c. Big Vein.-Although first identified many years ago, big vein still presents difficulties of understanding, and less progress has been made
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than might have been expected. The agent for the disease was first identified as a virus, mainly because it could be grafted transmitted (Campbell e t al. 1961; Campbell and Grogan 1963). Because other evidence of the presence of a virus, particularly isolation of a virus particle, has not been forthcoming, the cause is now referred to as “big vein agent.” This agent is introduced into the plant through the roots by a soil-borne root-infecting fungus, Olpidium brassicae (Wor.) Dang. (Campbell and Grogan 1963). Big vein symptoms are vein clearing, caused by chlorosis of tissue on either side of the veins, and crinkling and stiffening of outer leaves, giving the plant an upright bushy appearance. The incidence of big vein symptoms is related to two major factors: air temperature and soil type. These environmental agents regulate its appearance according to season and location. Westerlund et al. (1978a) found that big vein symptoms were most severe a t 14°Cair temperature, whether the soil temperature was a t 14°C or 24°C. Practically no symptoms developed when the air temperature was 24”C, regardless of the soil temperature. Soils may be classified as big vein prone, big vein intermediate, and big vein suppressive. Prone soils have a high water-holding capacity (Westerlund et al. 1978b). These two factors make big vein a serious lettuce disease in cold, wet heavy soils during the cooler parts of the growing season. This means that big vein is most likely to be a problem in the late winter plantings in the desert and the early spring plantings on the coast, given appropriate soils. Big vein causes a delay in maturity and consequent reduction in head size. This was shown to occur in ‘Great Lakes’ lettuce by Zink and Grogan (1954) in the Salinas Valley and by Marlatt and McKittrick (1962) in Arizona. In fields showing big vein symptoms, more healthy than infected plants were harvested and the latter were smaller. Zink and Grogan (1954) also found that big vein affected quality; the differences in harvest were increased when the market price was low, presumably because of the unsightliness of the infected heads and their relative unsalability . In a more recent study, Ryder (1979a) found that big vein can reduce harvestability but that the relationship depends upon several factors. One is temperature; the effect occurred in the coolest part of the cool season and tended to disappear with increasing temperature. Another is genotype; ‘Great Lakes 65’, a relatively small, highly susceptible cultivar, was more affected than ‘Calmar’, a larger, more tolerant cultivar. These in turn were more affected than two resistant lines, ‘Merit’, a crisp cultivar, and 72-136, a crisp breeding line. Big vein is difficult to control. Two measures that have been attempted are soil fumigation and regulation of irrigation to avoid excess water. ‘Merit’ is the only resistant cultivar, but it is not widely adapted.
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d. Tipburn.-Tipburn, like big vein, has been a difficult problem, primarily because of a seeming multiplicity of causes and consequent confusion over methods of control. In the field, tipburn occurs a t the time of harvest and if it is sufficiently severe, may cause loss of an entire field. I t manifests itself as a necrosis of the margins of actively growing inner head leaves. Expression varies; it may consist of one small brown or black lesion, or several small or large lesions on several leaves. No organism has been associated with the disorder. I t is considered to be a physiological breakdown. The basic internal causes and environmental influences on tipburn are not clearly understood. Calcium nutrition seems to be basic to the events leading to tipburn, but the specific role of calcium and the reason for its critical role in the tipburn syndrome are matters of speculation. One factor is calcium mobility in the plant. I t moves slowly, and during periods of rapid growth it may fail to keep pace with tissue development, thus leading to tissue weakness. Ashkar and Ries (1971) believe that an inadequate supply of calcium restricts protein synthesis. The presence of free amino acids may be indicative of toxicity. Crisp et al. (1976) noted that calcium increases cell wall strength and restricts cellular growth. Thibodeau and Minotti (1969) controlled tipburn on ‘Meikoningen’, a butterhead cultivar, by spraying exposed young leaves with Ca(N0;J2or CaC12. Leaves were kept exposed after head formation began by opening the leaves outward as the head formed. Spraying outside leaves had no effect in reducing tipburn, because the calcium moves too slowly from the outer to inner tissues. They showed that the amount of total and available calcium decreased from basal, to outer, to inner leaves. They were able to increase the rate of tipburn development by adding organic acids that chelated calcium, thereby reducing the soluble portion. Ashkar and Ries (1971) also reduced tipburn in ‘Great Lakes 659’ plants grown in the greenhouse and in the growth chamber by adding calcium as CaC12 to the growing medium. They found less calcium in tipburned than in healthy leaves and less in marginal tissue than in midrib or basal tissue. However, even in tipburn-free plants, there was less calcium in marginal tissue, indicating that other influences also may be important. A number of environmental causes have been implicated in the occurrence of tipburn. In general, they have one thing in common: they increase growth rate, leading to the belief that it is during periods of rapid growth that calcium becomes limiting in susceptible tissue and leads to tipburn. Ashkar and Ries (1971) compared two levels of nitrogen addition to plants of ‘Grand Rapids’, a leaf lettuce, and found that tipburn occurred only a t the higher level where growth rate increased. Tibbitts and Rao (1968) found more tipburn with greater duration or intensity of light, whereas Tibbitts and Bottenberg (1971) were able to induce tip-
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burn with a temperature increase by transferring plants from a 21°C environment to a 29°C one. Both experiments were with ‘Meikoningen’. Cox et al. (1976) compared six cultivars, two butterhead, two cos, and two crisphead types, in a range of controlled environments affecting relative growth rate, measured in g/g/day. As growth rate increased, less time was required for tipburn to occur. In listing the conditions associated with the occurrence of tipburn, Cox et al. (1976) and Shear (1975) indicate growth rate as a common factor in nearly all cases. The role of latex must be considered. Lettuce and other members of the Asteraceae (Compositae) are species in which latex is produced in a system of ducts called laticifers. Tibbitts et al. (1965) and Olsen et al. (1967) hypothesized that the laticifers rupture near the leaf margins, releasing latex into the surrounding tissues. This causes dark brown spots to form a t the points of rupture. These in turn affect processes in the surrounding tissues, with resulting necrotic collapse of the whole marginal area. Endive, chicory, cabbage, and celery also have similar disorders, but only the first two form latex. The logical conclusion is that the latex breakdown accompanies tipburn development, but is not necessarily the cause. Methods of tipburn control, other than resistance, are of doubtful applicability on a field scale. Foliar sprays control tipburn when applied directly to inner leaves, but are ineffective in the field once heading has begun. Application of calcium fertilizer in late growth stages is unlikely to aid in control. However, avoidance of light, warm soils planted for summer harvest may be helpful. Most effective control is obtained with the use of resistant cultivars. In California, ‘Salinas’, ‘Calmar’, and ‘Montemar’ are the most resistant of the cultivars available for the coastal districts; ‘Vanguard’is relatively tolerant in the desert areas. Much of the research on tipburn has been done in the greenhouse and growth chamber with induction of the disorder occurring a t relatively immature stages. However, in the field, tipburn is a mature plant problem and differences in mode of induction, cultivar reaction, and symptom expression in the different environments could be important. Cox and McKee (1976) compared eight lettuce cultivars of various types in field and greenhouse experiments. Only in ‘Great Lakes 659’ and ‘Borough Wonder’ was the expression of tipburn a t the same level in both environments. Recently, Misaghi and Grogan (1978a,b)have made progress in attacking the fundamental causes of tipburn. They have been able to induce tipburn on detached field-grown heads of lettuce by exposing them to high temperatures (24” to 33°C) in growth chambers. This accomplishment leads to the possibility of development of a laboratory screening
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procedure to select for resistance, which would be superior to the less reliable field screening now used by breeders. They also were able to induce tipburn development in mature heads held a t 21°C by treatment with potassium salts of several organic acids. This led them to suggest that, “tipburn is a manifestation of local calcium deficiency that results from chelation of calcium by organic acids and other metabolites t h a t are increased in plants during exposure to elevated temperature.” In spite of the enormous amount of research on tipburn, none of the data is inconsistent with the theory proposed by Misaghi and Grogan for the development of tipburn.
e. Downy Mildew.-Downy mildew is less serious in California than in the Rio Grande Valley of Texas and in Europe, but it can be troublesome in all the lettuce-growing areas in the state, particularly the Santa Maria Valley. Several areas of research have been explored: resistance, other means of control, and the nature of the disease. The disease is caused by the fungus Bremia lactucae Reg. The typical symptoms are yellow angular areas, delimited by veins, appearing on the upper leaf surfaces and sporulation on the lower surfaces. The lesions turn brown and may coalesce. They appear on lower leaves first, but in severe infections the leaves of the head itself may be affected. Invasion by secondary organisms may cause rotting during shipment. Since the identification of a dominant gene for resistance by I. C. Jagger over 50 years ago (Jagger 1924), much evidence has accumulated from research conducted in various parts of the world that the fungus produces races capable of infecting previously resistant cultivars. Many sources of resistance have been identified. Much confusion over identification and naming of genes and races developed until Crute and Johnson (1976) attempted to bring order with the construction of a gene-for-gene relationship between host and pathogen. They postulated resistant factors in lettuce cultivars and virulence factors in the pathogen, such that a cultivar was resistant to those strains of the fungus not carrying the same numbered virulence factor as the resistant factor in the cultivar. A cultivar carrying two or more resistant factors is immune from those races in which a t least one of the corresponding virulence factors is absent. The study of F, data from lettuce cultivar crosses enabled them to label some factors as genes (Johnson et al. 1978). The genetics of the virulence factors has not been studied. In California, all cultivars except one, ‘Imperial 410’, were susceptible to a race of the fungus that had appeared in 1932 in the Salinas Valley. The resistant source used in the breeding of ‘Imperial 410’, a Plant Introduction line of L. serriola from Russia, P. I. 91532, was used in subsequent crosses. ‘Calmar’ and its related cultivars were derived from these
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lines. These cultivars were grown extensively in the coastal districts. Also derived from such crosses were ‘Valverde’, important in saving the lettuce industry of the Lower Rio Grande Valley, and two cultivars used in the desert districts, ‘Valrio’ and ‘Valtemp’. ‘Valverde’ was released in 1959, ‘Calmar’ in 1960, and the others subsequently (Whitaker et al. 1958; Leeper et al. 1959, 1969; Welch et al. 1965). Resistance to mildew in the cos cultivar ‘Valmaine’ was obtained from another introduction, P. I. 167150, from Turkey. ‘Valverde’, Valmaine’, and ‘Calmar’ were shown to be susceptible to a new race of the fungus that appeared in Texas in 1965. ‘Calmar’ remained resistant in California until 1973. Evidently a new race had appeared. Likewise, the cultivars related to ‘Calmar’ also were susceptible. Zink (1979) clarified what had occurred in California, using the nomenclature developed by Crute and Johnson (1976). He found that the California mildew population was composed of nine virulence factors (V1, V2, V3, V5, V6, V7, V8, V9, and V11). These occurred in various proportions in the different lettuce districts. Overall, V6, V7, and V8 were most common. No cultivars now grown in California are resistant to downy mildew. However, Zink identified 13 European butterhead cultivars, with a t least 8 different dominant genes among them, resistant to the races containing the virulence factors. Some of these resistant cultivars are being used in breeding programs to develop new cultivars for California. In Europe, the mildew virulence picture has changed rapidly and constantly, such that new virulent forms appear that can infect previously resistant cultivars, which are then replaced, only to be susceptible to still newer virulent forms. In California, this has not happened. New sources of resistance have remained resistant for relatively long periods. However, this may not always remain true, and the present method of breeding for resistance has been questioned by Crute and Johnson (1976). They have suggested investigating alternate methods of control. One is to search for a more generalized form of resistance independent of the gene-for-gene system and presumably, therefore, having more stability. Another is the use of isogenic lines, each containing different genes for resistance. One line may be replaced by another when the virulence form attacking the first becomes too frequent. Chemical control is a third possible method. Systemic fungicides with excellent control have been tested in England (Crute et al. 1977), where they are now in use, and in California (Paulus et al. 1977). A new source of resistance has been identified in the related wild species, L. saligna L. (Netzer et al. 1976). It is not known how the resistance of L. saligna fits genetically into the system established by Crute and Johnson (1976).
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Most of the studies on the nature of the fungus and its behavior on lettuce have been conducted in England. These include studies by Dixon et al. (1973) on colonization of adult plants by the fungus, by Dickinson and Crute (1974) on the influence of seedling age on infection by the fungus, by Crute and Dickinson (1976) on behavior of the fungus on cultivars of lettuce, and on other related and non-related species, and by Wellving and Crute (1978) on virulence characteristics. Reports of systemic infection in mature head lettuce in Arizona led Marlatt et al. (1962) to inoculate plants in the seedling stage; they found evidence of systemic infection. Later, Phillips and Lipton (1974) found the first evidence of systemic infection in California, on mature lettuce. Downy mildew has postharvest effects on the plants that it infects. Zink and Welch (1962) compared healthy and infected ‘Great Lakes’ lettuce with immune ‘Calmar’ in simulated transit tests. The healthy ‘Great Lakes’ retained good visual quality as well as the ‘Calmar’, but infected ‘Great Lakes’ deteriorated more rapidly than ‘Calmar’. The number of downy mildew lesions increased, and soft rot organisms invaded the infected tissues. 3. Research on Insects and Nematodes.-The most damaging and persistent insect pests of lettuce continue to be the cabbage looper, salt marsh caterpillar, and the beet army worm, with the cabbage looper perhaps presenting the number one hazard to a successful crop. Efforts to achieve biological control of the cabbage looper are coming to fruition. Bacillus thuringiensis, a bacterial parasite of the cabbage looper larvae, developed within the past five to ten years, gives good control under optimum conditions. It does not give immediate relief, and in severe infestations a chemical insecticide will be necessary. Methonyl, under the trade names Lannate and Nudrin, is suggested. The latter, along with Parathion and Mevinphos (Phosdrin), is recommended for the beet army worm and the salt marsh caterpillar. The cabbage looper (Trichoplusia ni (Hubner)) is among the most destructive pests of the late fall and winter lettuce crop in the inland desert valleys of California. The larva of this pest quickly defoliates the young plants, and if left unchecked it can destroy the seedlings almost overnight. Chemical control is effective, but must be timely and is costly. Two or three applications of an insecticide are minimal, but with heavy infestations as many as seven applications may be required for control. If genotypes resistant or tolerant to cabbage looper could be found and combined with the acceptable horticultural characteristics of conventional crisphead type cultivars, the potential for enormous savings of insecticides and consequent reduction in pollution would be substantial. The presence of this pest on lettuce is largely dependent upon the
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discrimination of gravid females. It follows th a t if preferential oviposition on cultivars and species of Lactuca could be discovered, looper injury might be decreased significantly on nonpreferred lettuce. Kishaba et al. (19731, working on the above hypothesis, screened more than 200 entries of Lactuca sativa cultivars and species of Lactuca. They found significant reduction in oviposition on 8 cultivars, 4 breeding lines, and 17 foreign Plant Introductions. Furthermore, one introduction each of L. serriola and L. saligna was less attractive to loopers than any of the entries of L. satiua. With this material as a base, efforts are being made to incorporate preferential oviposition into lettuce cultivars. The root-knot nematode (Meloidogyne hapla) and the needle nematode (Longidorus african us) are serious pests of lettuce in warmer areas. Fields known to be infested are fumigated with 1-3-dichlorapropine a t least 14 days prior to planting. The needle nematode recently has been demonstrated to be a more serious pest of lettuce than was formerly thought, and can be responsible for significant economic loss (Radewald et al. 1969). 4. Weed Research.-Weeds can seriously affect the development of the lettuce crop. Particularly in the seedling or prethinning stage, a dense crop of weeds can restrict growth and make thinning difficult. As late as 1965 most weeds in California lettuce fields were eliminated with the hand hoe in the rows and with the tractor-drawn cultivator between rows (Zink and Agamalian 1965). Thinning time was the opportune time to eliminate weeds as well as extra lettuce plants. Historically, the development of herbicides useful for lettuce began much earlier. In terms of obtaining a label for accepted use on lettuce, Chemhoe (IPC or propham) and Furloe (chloro-IPC or chlorpropham) became available in 1956 to 1957; Vegadex (CDEC) in 1958 to 1959; Balan (benefin) in 1962 to 1963; Prefar (bensulide) in 1965; and Kerb (pronamide) in 1970 to 1972. These have been the principal substances useful in lettuce (Agamalian 1979). Present recommendations include Kerb alone a s a preplant or preemergence herbicide to control a wide spectrum of weeds including mustard, shepherd’s purse, pigweed, an d purslane, or Kerb and Vegadex in combination to control groundsel as well. Kerb also controls nightshade and volunteer cereals (Agamalian 1979; Cudney et al. 1977). At present about 90% of the lettuce crop is treated with herbicides (Whitaker e t al. 1974). Th e acceptance of herbicides appears to have accompanied the use of sprinkler irrigation and coated seed. T h e former permits the herbicide to remain in place for most effective action on emerging weed seeds while the latter means fewer crop seedlings to compete with the weeds and therefore greater need to control the weeds a t a n early stage.
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5. California Iceberg Lettuce Research Program.-Under the California Marketing Act of 1937, commodity groups are permitted to assess themselves to raise money to support research. The lettuce handlers of California requested such a program, which was duly formed in June, 1973. Assessments are collected under the taxing power of the state, deposited in a trust fund by the California Department of Food a n d Agriculture, and used to support various research projects in production, harvesting, handling, and distribution of lettuce. This research is conducted by the University of California, the U. S. Department of Agriculture, and occasionally, other organizations. This program has given great impetus to lettuce research in California. It has fostered greater cooperation among researchers and has encouraged the performance of research oriented toward production and shipping problems. I t has kept the researcher and grower-shipper in closer contact and given the researcher greater insights into the lettuce industry and industry people greater awareness of research. Projects supported by the program include breeding, diseases, insect control, fertilization, seed studies, growth studies, harvesting, postharvest physiology, and handling systems.
111. LITERATURE CITED ADRIAN, P.A., D.H. LENKER, and D. NASCIMENTO. 1976. A mechanical trimmer for crisphead lettuce-refinements, field tests and performance. Trans. Amer. SOC. Agr. Eng. 19:835-839. AGAMALIAN, H. 1979. Personal communication. Salinas, Calif. AMIN, K.S. and L. SEQUEIRA. 1966. Phytotoxic substances from decomposing lettuce residues in relation to the etiology of corky root rot of lettuce. P hy topa thology 56 :105 4 - 106 1. ASHKAR, S.A. and S.K. RIES. 1971. Lettuce tipburn as related to nutrient Hort. Sci. 96:448-452. imbalance and nitrogen composition. J. Amer. SOC. BARTON, L.V. 1966. Effects of temperature and moisture on viability of stored lettuce, onion and tomato seeds. Contrib. Boyce Thompson Inst. Plant Res. 23:285-290. BASS, L.N. 1970. Prevention of physiological necrosis (red cotyledons) in letHort. Sci. 95:550-553. tuce seeds (Lactuca sativa L.1. J. Amer. SOC. BERAHA, L. and W. F. KWOLEK. 1975. Prevalence and extent of eight market disorders of Western-grown head lettuce during 1973 and 1974 in the Greater Chicago, Illinois area. Plant Dis. Rptr. 59:lOOl-1004. BERRIE, A.M.M., J. PATERSON, and H.R. WEST. 1974. Water content and the responsivity of lettuce seeds to light. Physiol. Plant. 31:90-96. BERRY, W.L. 1971a. Evaluation of phosphorus nutrient status in seedling lettuce. J. Amer. SOC. Hort. Sci. 96:341-344.
200
HORTICIJLTURAL REVIEWS
BERRY, W.L. 1971b. The nutrient status of zinc in lettuce evaluated by plant analysis. J. Amer. SOC. Hort. Sci. 96:412-414. BERRY, W.L. and R. CAREY. 1971. Evaluation of the potassium nutrient status of seedling lettuce by plant analysis. J. Amer. SOC. Hort. Sci. 96: 298-300. BORTHWICK, H.A., S.B. HENDRICKS, E.H. TOOLE, and V.K. TOOLE. 1954. Action of light on lettuce seed germination. Bot. Gaz. 115:205-225. BRECHT, P.E., A.H. KADER, and L.L. MORRIS. 1973. The effect of composition of the atmosphere and duration of exposure on brown stain of lettuce. J. Amer. SOC. Hort. Sci. 98:536-538. CAMPBELL, R.N. and R.G. GROGAN. 1963. Big vein virus of lettuce and its transmission by Olpidium brassicae. Phytopathology 53:252-259. CAMPBELL, R.N., R.G. GROGAN, and D.E. PURCIFULL. 1961. Graft transmission of big vein of lettuce. Virology 15:82-85. CEPONIS, M.J. and J. KAUFMAN. 1968. Effect of relative humidity on moisture loss and decay of eastern lettuce prepackaged in different films. USDAARS 51-18. CEPONIS, M.J. and J. KAUFMAN. 1970. Brown stain of western head lettuce on the New York market. P l a n t Dis. Rptr. 54:856-857. CEPONIS, M.J., F.M. PORTER, and J. KAUFMAN. 1970. Rusty-brown discoloration a serious market disorder of western winter head lettuce. HortScience 5:219-221. COAKLEY, S.M., R.N. CAMPBELL, and K.A. KIMBLE. 1973. Internal rib necrosis and rusty brown discoloration of Climax lettuce induced by lettuce mosaic virus. Phytopathology 63:1191-1197. COUCH, H.B. 1955. Studies on seed transmission of lettuce mosaic virus. Phytopathology 45:63-70. COX, E.F. and J.M.T. MCKEE. 1976. A comparison of tipburn susceptibility in lettuce under field and glasshouse conditions. J. Hort. Sci. 51:117-122. COX, E.F., J.M.T. MCKEE, and A.D. DEARMAN. 1976. The effect of growth rate on tipburn occurrence in lettuce. J. Hort. Sci. 51:297-309. CRISP, P., G.F. COLLIER, and T.H. THOMAS. 1976. The effect of boron on tipburn and auxin activity in lettuce. Sci. Hort. 5:215-226. CRUTE, I.R. and C.H. DICKINSON. 1976. The behavior of Bremia lactucae on cultivars of Lactuca sativa and on other composites. Ann. Appl. Biol. 82:433-450. CRUTE, I.R. and A.G. JOHNSON. 1976. The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Ann. Appl. Biol. 83:125-137. CRUTE, I.R., S.A. WOLFMAN, and A.A. DAVIS. 1977. A laboratory method of screening fungicides for systemic activity against Bremia lactucae. Ann. Appl. Biol. 85:147-152. CUDNEY, D.W. et al. 1977. Weed control in lettuce. Div. Agr. Sci., Univ. of Calif. (Riverside) Leaflet 2987.
T H E LETTUCE INDUSTRY IN CALIFORNIA
201
CURRAH, I.E., D. GRAY, and T.H. THOMAS. 1974. The sowing of germinating vegetable seeds using a fluid drill. Ann. Appl. Biol. 76:311-318. DICKINSON, C.H. and I.R. CRUTE. 1974. The influence of seedling age and development on the infection of lettuce by Bremia lactucae. Ann. Appl. Biol. 76:49-61. DIXON, G.R., M.H. TONKIN, and J.K. DOODSON. 1973. Colonization of adult lettuce plants by Bremia lactucae. Ann. Appl. Biol. 74:307-313. DUFFUS, J.E. 1960. Two viruses that induce symptoms typical of “June yellows” in lettuce. P l a n t Dis. Rptr. 44:406-408. DUFFUS, J.E. 1973. The yellowing virus diseases of beet. Adu. Virus Res. 18:347-386. FEDERAL STATE MARKET NEWS SERVICE. 1978a. Marketing lettuce from Imperial Valley and Blythe districts. 1977-78 Marketing Season. USDA-AMS, State of Calif. FEDERAL STATE MARKET NEWS SERVICE. 1978b. Marketing lettuce from Salinas-Watsonville-King City and other Central California districts. 1977 Marketing Season. USDA-AMS, State of Calif. FOSTER, R.E. 1978. Is chopped the answer for lettuce? Western Grower & Shipper 49:6-9. FRIEDLAND, W.H., A.E. BARTON, and R.J. THOMAS. 1979. Conditions and consequences of lettuce harvest mechanization. HortScience 14:llO-113. GARRETT, R.E. and W.K. TALLEY. 1970. Use of gamma ray transmission in selecting lettuce for harvest. Trans. Amer. SOC. Agr. Eng. 13:820-823. GARRETT, R.E., M. ZAHARA, and R.E. GRIFFIN. 1966. Selector component development for a head-lettuce harvester. Trans. Amer. SOC. Agr. Eng. 9:56-57. GRAY, D. 1975. Effects of temperature on the germination and emergence of lettuce (Lactuca sativa L.) varieties. J. Hort. Sci. 50:349-361. GRAY, D. 1976. The effect of time of emergence on head weight a t maturity in lettuce (Lactuca satiua). Ann. Appl. Biol. 82:569-575. GRAY, D. 1977. Temperature sensitive phases during the germination of lettuce (Lactuca satiua) seeds. Ann. Appl. Biol. 86:77-86. GRAY, D. 1978. Comparison of fluid drilling and conventional establishment techniques on seedling emergence and crop uniformity in lettuce. J. Hort. Sci. 53:23-30. GRAY, D. and J.R.A. STECKEL. 1976. The effects of pre-sowing seed treatments on the germination and emergence of lettuce seeds a t high salt concentrations. Sci. Hort. 5:l-9. GROGAN, R.G., J.E. WELCH, and R. BARDIN. 1952. Common lettuce mosaic and its control by the use of mosaic-free seed. Phytopathology 42:573-578. GROGAN, R.G. and F.W. ZINK. 1956. Fertilizer injury and its relationship to several previously described diseases of lettuce. Phytopathology 46:416-422. HABER, A.H. and N.E. TOLBERT. 1959. Effects of gibberellic acid, kinetin and light on the germination of lettuce seed. p. 197-206. I n R.W. Withrow
202
HORTICULTURAL REVIEWS
(ed.) Photoperiodism and related phenomena in plants and animals. AAAS, Washington, D.C. HALL, C.B., R.E. STALL, and H.W. BURDINE. 1971. Association of Pseudomonas marginalis with pink rib of lettuce. Proc. Flu. State Hort. SOC.84: 163-165. HARRIOTT, B.L. and K.K. BARNES. 1964. Mechanical selection of crispAgr. Eng. 7:195-199. head lettuce for harvest. Trans. Amer. SOC. HARSH, G.D., O.P. VYAS, S.P. BOHRA, and N. SANKHLA. 1973. Lettuce seed germination: prevention of thermodormancy by Z-chloro-ethanephosphonic acid (ethrel). Experientia 29:731-732. HEYDECKER, W. and A. JOSHUA. 1976. Delayed interacting effects of temperature and light on the germination of Lactuca sativa seeds. Seed Sci. & Tech. 4:231-238. HSIAO, A.I.H. and W. VIDAVER. 1971. Water content and phytochrome induced potential germination responses in lettuce seeds. P l a n t Physiol. 47: 186-188. IKUMA, H. and K.V. THIMANN. 1964. Analysis of germination processes of lettuce seed by means of temperature and anaerobiosis. P l a n t Physiol. 39:756-767. JAGGER, I.C. 1924. Immunity to mildew (Bremia lactucae Reg.) and its inheritance in lettuce. Phytopathology 14:122. (Abstr.) JOHNSON, A.G., S.A. LAXTON, I.R. CRUTE, P.L. GORDON, and J.M. NORWOOD. 1978. Further work on the genetics of race specific resistance in lettuce (Lactuca satiua) to downy mildew (Bremia lactucae). Ann. Appl. Biol. 89:257-264. JOHNSON, H., J R . 1979. Personal communication. Riverside, Calif. JOHNSON, H., JR., D.R. WOODRUFF, and T.W. WHITAKER. 1970. Internal rib necrosis of head lettuce in Imperial Valley. Calif. Agr. 24 (9):lO-11. JOHNSON, S.S. and M. ZAHARA. 1976. Prospective lettuce harvest mechanization. Impact on labor. J. Amer. SOC.Hort. Sci. 101:378-381. KADER, A.A., P.E. BRECHT, R. WOODRUFF, and L.L. MORRIS. 1973a. Influence of carbon monoxide, carbon dioxide and oxygen levels on brown stain, respiration rate and visual quality of lettuce. J. Amer. SOC. Hort. Sci. 98:485-488. KADER, A.A., W.J. LIPTON, and L.L. MORRIS. 1973b. Systems for scoring quality of harvested lettuce. HortScience 8:408-409. KAHN, A., J.A. GOSS, and D.E. SMITH. 1957. Effect of gibberellin on germination of lettuce seed. Science 125:645-646. KIMBLE, K.A., R.G. GROGAN, A S . GREATHEAD, A.O. PAULUS, and J.K. HOUSE. 1975. Development, application and comparison of methods for indexing lettuce seed for mosaic virus in California. P l a n t Dis. Rptr. 59: 461-464. KISHABA, A.N., T.W. WHITAKER, P.V. VAIL, and H.H. TOBA. 1973. Differential oviposition of cabbage loopers on lettuce. J. Amer. SOC. Hort. Sci. 98:367-370.
T H E LETTUCE INDUSTRY I N CALIFORNIA
203
KOSAR, W.F. and R.C. THOMPSON. 1957. Influence of storage humidity on Hort. Sci. 70:273dormancy and longevity of lettuce seed. Proc. Amer. SOC. 276. LEEPER, P.W., T.W. WHITAKER, and G.W. BOHN. 1959. Lettuce mildew resistant variety. Amer. Veg. Grower 7(9):18. LEEPER, P.W., T.W. WHITAKER, and G.W. BOHN. 1963. Valmaine-a new cos type lettuce variety. Amer. Veg. Grower 11(9):7,16. LEEPER, P.W., T.W. WHITAKER, and G.W. BOHN. 1969. Valtemp and Valrio. Amer. Veg. Grower 17(3):56,58. LENKER, D.H. and P.A. ADRIAN. 1971. Use of X-rays for selecting mature lettuce heads. Trans. Amer. SOC. Agr. Eng. 14:894-898. LIPTON, W.J. 1963. Influence of maximum air temperatures during growth on the occurrence of russet spotting in head lettuce. Proc. Amer. Soc. Hort. Sci. 83:590-595. LIPTON, W.J., J.K. STEWART, and T.W. WHITAKER. 1972. An illustrated guide to the identification of some market disorders of head lettuce. USDA Marketing Res. Rpt. 950. MARLATT, R.B., R.W. LEWIS, and R.T. MCKITTRICK. 1962. Systemic infection of lettuce by Bremia lactucae. Phytopathology 52:888-890. MARLATT, R.B. and R.T. MCKITTRICK. 1962. Effects of big vein on the irrigated head lettuce crop. P l a n t Dis. Rptr. 46:428-429. MARLATT, R.B. and J.K. STEWART. 1956. Pink rib of head lettuce. P l a n t Dis. Rp tr. 40 :742 - 74 3. MAYBERRY, K. 1979. Personal communication. El Centro, Calif. MCCOY, O.D., F.E. ROBINSON, H. JOHNSON, JR., R.G. CURLEY, C. BROOKS, G. GIANNINI, and F. LEBARON. 1969. Precision planting of Hort. Sci. 94:344-345. lettuce. J. Amer. SOC. MCLEAN, D.L. and M.G. KINSEY. 1962. Three variants of lettuce mosaic virus and methods utilized for differentiation. Phytopathology 52:403-406. MCLEAN, D.L. and M.G. KINSEY. 1963. Transmission studies of a highly virulent variant of lettuce mosaic virus. P l a n t Dis. Rptr. 47:474-476. MISAGHI, I.J. and R.G. GROGAN. 1978a. Effect of temperature on tipburn development in head lettuce. Phytopathology 68:1738-1743. MISAGHI, I.J. and R.G. GROGAN. 1978b. Physiological basis for tipburn development in head lettuce. Phytopathology 68:1744-1753. MORRIS, L.L., A.A. KADER, J.A. KLAUSTERMEYER, and C.C. CHEYNEY. 1978. Avoiding ethylene concentrations in harvested lettuce. Calif Agr. 32 (6):14-15. NEGM, F.B., O.E. SMITH, and J. KUMAMOTO. 1972. Interaction of carbon dioxide and ethylene in overcoming thermodormancy of lettuce seeds. P l a n t Physiol. 49 :869-87 2. NETZER, D., D. GLOBERSON, and J. SACKS. 1976. Lactuca saligna L., a new source of resistance to downy mildew (Bremia lactucae Reg.). HortScience 11:612-613.
204
HORTICIJLTI1RAL REVIEWS
ODEGBARO, O.A. and O.E. SMITH. 1969. Effects of kinetin, salt concentration and temperature on germination and early seedling growth of Lactuca satioa L. J. Amer. SOC.Hort. Sci. 94:167-170. OLSON, K.C., T.W. TIBBITTS, and B.E. STRUCKMEYER. 1967. Morphology and significance of laticifer rupture in lettuce tipburn. Proc. Amer. Soc. Hort. Sci. 91:377-385. PAIJLUS, A.O., J . NELSON, M. SNYDER, and J . GAFNEY. 1977. Downy mildew of lettuce controlled by systemic fungicide. Calif. Agr. 31(12):9. PELET, F. 1965. Determination of lettuce mosaic virus by indexing the seed on Chenopodium quinoa Willd. (in French). Rev. Hort. Suisse 38:7-10. PHILLIPS, D.J. and W.J. LIPTON. 1974. Systemic downy mildew found in California head lettuce. P l a n t Dis. Rptr. 58:118-119. RADEWALD, J.D., <J.W.OSGOOD, K.S. MAYBERRY, A.O. PAULUS, and F. SHIBAYA. 1969. Longidorus africanus a pathogen of head lettuce in the Imperial Valley of Southern California. P l a n t Dis. Rptr. 53:381-384. REYNOLDS, T . 1975. Characterization of osmotic restraints on lettuce fruit germination. Ann. Bot. 39:791-796. ROBINSON, F.E. 1969. Stands for automation achieved by sprinkling. Irrig. & Drainage Dir. 95:385-389. ROBINSON, F.E. 1972. Solid set sprinkler irrigation. Agr. Eng. 53:15-16. ROOD, R. 1956. Relation of ethylene and post-harvest temperature to brown spot of lettuce. Proc. Amer. SOC.Hort. Sci. 68:296-303. RYDER, E.J. 1964. Transmission of common lettuce mosaic virus through the gametes of the lettuce plant. Plant. Dis. Rptr. 48:522-523. RYDER, E.J. 1968. Evaluation of lettuce varieties and breeding lines for resistance to common lettuce mosaic. USDA Tech. Bul. 1391. RYDER, E.J. 1970a. Inheritance of resistance to common lettuce mosaic. J. Amer. SOC.Hort. Sci. 95:378-379. RYDER, E.J. 1970b. Screening for resistance to lettuce mosaic. HortScience 5:47-48. RYDER, E.J. 1973. Seed transmission of lettuce mosaic virus in mosaic resistant lettuce. J. Amer. SOC.Hort. Sci. 98:610-614. RYDER, E.J. 1976. The nature of resistance to lettuce mosaic. Eucarpia Meeting on Leafy Vegetables, Wageningen, Holland. March 15-18,1976. Institute for Horticultural Plant Breeding, Wageningen. p.110-118. RYDER, E.J. 1979a. Effects of big vein resistance and temperature on disease incidence and percentage of plants harvested of crisphead lettuce. J. Amer. SOC. Hort. Sci. 104:665-668. RYDER, E.J. 1979b. Leafy salad vegetables. AVI Publishing, Westport, Conn. RYDER, E.J. 1979c. ‘Salinas’ lettuce. HortScience 14:283-284. RYDER, E.J. 1979d. ‘Vanguard 75’ lettuce. HortScience 14:284-286. RYDER, E.J. and J.E. DUFFUS. 1966. Effects of beet western yellows and lettuce mosaic viruses on lettuce seed production, flowering time, and other characters in the greenhouse. Phytopathology 56:842-844.
T H E LETTlJCE INDUSTRY I N CALIFORNIA
205
SCAIFE, M.A. and D. JONES. 1970. Effect of seed weight on lettuce growth. J. Hort. Sci. 45:299-302. SCAIFE, M.A. and R. SMITH. 1973. The phosphorus requirement of lettuce. 11. A dynamic model of phosphorus uptake and growth. J. Agr. Sci. Camb. 80:353-361. SHEAR, C.B. 1975. Calcium-related disorders of fruits and vegetables. HortScience 10:361-365. SHEPARDSON, E.S., J.G. POLLOCK, and G.E. REHKUGLER. 1974. Research and development of a lettuce harvester. Trans. Amer. SOC. Agr. Eng. 17:212-216. SMITH, O.E., N.C. WELCH, and T.M. LITTLE. 1973a. Studies on lettuce seed quality: I. Effect of seed size and weight on vigor. J. Amer. SOC. Hort. Sci. 98 :52 9- 533. SMITH, O.E., N.C. WELCH, and O.D. MCCOY. 1973b. Studies on lettuce seed quality: 11. Relationship of seed vigor to emergence, seedling weight and yield. J. Amer. SOC. Hort. Sci. 98:552-556. SMITH, O.E., W.W.L. YEN, and J.M. LYONS. 1968. The effects of kinetin in overcoming high temperature dormancy of lettuce seed. Proc. Amer. SOC. Hort. Sci. 93:444-453. SOFFER, H. and O.E. SMITH. 1974a. Studies on lettuce seed quality: 111. Relationship between flowering pattern, seed yield and seed quality. J. Amer. SOC. Hort. Sci. 99:114-117. SOFFER, H. and O.E. SMITH. 197410. Studies on lettuce seed quality: IV. Individually measured embryo and seed characteristics in relation to continuous plant growth (vigor) under controlled conditions. J. Amer. SOC. Hort. Sci. 99 :270-2 7 5. SOFFER, H. and O.E. SMITH. 1974c. Studies on lettuce seed quality: V. Nutritional effects. J. Amer. SOC. Hort. Sci. 99:459-463. STEWART, J.K., M.L. CEPONIS, and L. BERAHA. 1970. Modified atmosphere effects on the market quality of lettuce shipped by rail. USDA Mktg. Res. Rpt. 863. STEWART, J.K. and F. MATOBA. 1972. Some factors influencing the susceptibility of lettuce to C02 injury. Plant Dis. Rptr. 56:1051-1054. TEMPLE-SMITH, M.G. and R.C. MENARY. 1977. Growth and phosphate absorption in lettuce and cabbage plants in dilute solution culture. Austral. J. P l a n t Physiol. 4:505-513. THIBODEAU, P.O. and P.L. MINOTTI. 1969. The influence of calcium on Hort. Sci. 94:372-376. the development of lettuce tipburn. J. Amer. SOC. THOMPSON, R.C. and E.J. RYDER. 1961. Description and pedigrees of nine varieties of lettuce. USDA Tech. Bul. 1244. TIBBITTS, T.W. and G.E. BOTTENBERG. 1971. Effects of temperature increase on tipburn injury of lettuce. HortScience 6:306. TIBBITTS, T.W. and R.R. RAO. 1968. Light intensity and duration in the development of lettuce tipburn. Proc. Amer. SOC. Hort. Sci. 93:454-461.
206
HORTICULTURAL REVIEWS
TIBBITTS, T.W., B.E. STRUCKMEYER, and R.R. RAO. 1965. Tipburn of Hort. Sci. 86:462-467. lettuce as related to release of latex. Proc. Amer. SOC. TOMLINSON, J.A., E.M. FAITHFULL, and C.M. WARD. 1976. Chemical suppression of the symptoms of two virus diseases. Ann. Appl. Biol. 84:31-41. USDA. 1954. Agricultural statistics. U S . Govt. Printing Office, Washington, D.C. USDA. 1978. Agricultural statistics. U S . Govt. Printing Office, Washington, D.C. VON DER PAHLEN, A. and J. CRNKO. 1965. Mosaic virus (Marmor lactucae Holmes) of lettuce in Mendoza and Buenos Aires (in Spanish). Rev. Invest. Agro. B. Aires. Ser. 5, 2:25-31. WATTS, L.E. 1975. The response of various breeding lines of lettuce to beet western yellows virus. Ann. Appl. Biol. 81:393-397. WELCH, J.E., R.G. GROGAN, F.W. ZINK, G.M. KIHARA, and K.A. KIMBLE. 1965. Calmar. Calif. Agr. 19(8):3-4. WELCH, N.C., K. TYLER, and D. RIRIE. 1979. Nitrogen stabilization in the Pajaro Valley in lettuce, celery and strawberries. Calif Agr. 33(9): 12-13. WELLVING, A. and I.R. CRUTE. 1978. The virulence characteristics of Bremia lactucae populations present in Sweden from 1971 to 1976. Ann. Appl. Biol. 89:251-256. WESTERLUND, F.V., R.N. CAMPBELL, and R.G. GROGAN. 1978a. Effect of temperature on transmission, translocation and persistence of the lettuce big-vein agent and big-vein symptom expression. Phytopathology 68:921926. WESTERLUND, F.V., R.N. CAMPBELL, R.G. GROGAN, and J.M. DUNIWAY. 1978b. Soil factors affecting the reproduction and survival of Olpidium brassicae and its transmission of big vein agent to lettuce. Phytopathology 68:927-935. WHITAKER, T.W. and G.W. BOHN. 1953. Contributions of applied science to the lettuce industry of the Southwest. Econ. Bot. 7:243-256. WHITAKER, T.W., G.W. BOHN, J.E. WELCH, and R.G. GROGAN. 1958. History and development of head lettuce resistant to downy mildew. Proc. Amer. SOC. Hort. Sci. 72:410-416. WHITAKER, T.W., E.J. RYDER, V.E. RUBATZKY, and P.V. VAIL. 1974. Lettuce production in the United States. USDA Agr. Handb. 221. (Revised). ZAHARA, M., S.S. JOHNSON, and R.E. GARRETT. 1974. Labor requirements, harvest costs, and the potential for mechanical harvest of lettuce. J. Amer. SOC. Hort. Sci. 99:535-537. ZINK, F.W. 1955. Studies with pelleted lettuce seed. Proc. Amer. SOC.Hort. Sci. 65:335-341. ZINK, F.W. 1966. The response of head lettuce to soil application of zinc. Proc. Amer. Soc. Hort. Sci. 89:406-414. ZINK, F.W. 1979. Personal communication. Davis, Calif.
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ZINK, F.W. and H. AGAMALIAN. 1965. Influence of CDEC on growth maturity, and yield of head lettuce. Weeds 13:19-22. ZINK, F.W. and J.E. DUFFUS. 1972. Association of beet western yellows and lettuce mosaic viruses with internal rib necrosis of lettuce. Phytopathology 62:1141-1144. ZINK, F.W., J.E. DUFFUS, and K.A. KIMBLE. 1973. Relationship of a nonlethal reaction to a virulent isolate of lettuce mosaic virus and turnip mosaic susceptibility in lettuce. J. Amer. Soc. Hort. Sci. 98:41-45. ZINK, F.W. and R.G. GROGAN. 1954. The interrelated effects of big vein and market price on the yield of head lettuce. Plant Dis. Rptr. 38:844-846. ZINK, F.W., R.G. GROGAN, and J.E. WELCH. 1956. The effect of the percentage of seed transmission upon subsequent spread of lettuce mosaic virus. Phytopathology 46:662-664. ZINK, F.W. and K.A. KIMBLE. 1961. Effect of time of infection by lettuce mosaic virus on rate of growth and yield in Great Lakes lettuce. Proc. Amer. SOC. Hort. Sci. 76:448-454. ZINK, F.W. and J.E. WELCH. 1962. Postharvest deterioration of the downy mildew susceptible lettuce variety Great Lakes and the resistant variety Calmar. Plant Dis. Rptr. 46:719-722. ZINK, F.W. and M. YAMAGUCHI. 1962. Studies on the growth rate and nutrient absorption of head lettuce. Hilgardia 32:471-500.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
Light Interception and Utilization by Orchard Systems J o h n E. J a c k s o n Department of Pomology, East Malling Research Station, Maidstone, Kent, U.K. I. Introduction 209 11. Light Interception by the Canopy as a Whole 210 210 A. The Concept of Light-Interception as a Yield-Limiting Factor B. Canopy Development and Structure 210 1. The Basic Approach as Used in Productivity Studies on ContinuousCanopy Crops 210 2. Measurement of Leaf Area Index in Orchards 21 1 3. Orchard Canopy Development over the Season 214 217 4. Canopy Development over the Orchard Lifetime 218 5. Leaf Area Indices of Mature Orchards 219 C. The Relationship Between Orchard LA1 and Light Interception 1.Theoretical Studies of the Effects of Canopy Arrangement and Density 219 a. General Concepts 219 b. Solid-Model Hedgerow Studies 220 i. Hedgerow “Form” Limits to Light Interception 221 222 ii. Hedgerow “Form” Effects on Light Distribution iii. Effects of Row Orientation and Latitude 222 224 c. Transmission Models Assuming Beers-Law Relationships 225 d. Monte Carlo Simulation Techniques e. The Simple General Model 226 230 D. Measurement of Light Interception by Orchard Systems 1.Techniques of Measurement 230 a. Basic Requirements 230 231 b. Selenium and Silicon Cells c. Tube Solarimeters 231 d. Photochemical Methods 232 e. Fisheye Photography 233 233 2 . Measured Light Interception by Orchard Systems 234 a. Light Interception over the Season 234 b. Light Interception by Branches and Fruits 208
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111.
IV.
V. VI.
209
c. Light Interception over the Orchard Lifetime 235 d. Evidence of Lowered Productivity Associated with Very High Interception Levels 235 Light Penetration and Distribution in Relation to Fruit Production 237 A. Relationships Between Light and Fruit Production with Respect to Optimizing Canopy Design for Penetration and Interception 237 1.Light Intensity Effects on Photosynthesis 237 238 2. Light Intensity Effects on Growth and Cropping B. Light Penetration into Apple Tree Canopies 240 1.Transmittance and Reflectance by Apple Leaves and Canopies 240 2. Measurement of Light Within the Canopy 241 3. The Extinction Coefficient of Light Penetrating Apple Canopies 242 C. Patterns of Light Penetration into Trees and Their Effects on Growth and Cropping 243 1.Light Relations in Round-Headed Trees 243 245 2. Light Relations in Hedgerow and Center-Leader Trees D. The Interaction Between Light Interception and Water Use 248 E. Management Practices Which Influence Light Interception and Distribution 249 249 1. Choice of Rootstock 2. Pruning 250 3. Reflection of Light from theorchard Floor 252 4. Row Orientation and Between- and Within-Row Spacing 252 Current Concepts in Canopy Design to Optimize Light Interception and Distribution 254 A. General Objectives 254 B. Multi-Row and Bed Systems 254 C. Meadow Orchards 256 256 D. Horizontal and V Trellis Systems Conclusions 256 Literature Cited 257
I. INTRODUCTION Studies of light interception provide the scientific basis for the practical management of orchard canopies, i.e., for the choice of tree size, number per hectare, arrangement and pruning, so a s to optimize the production of assimilate and its conversion into economic yield. Two distinct objectives are involved. Th e first is to find ways of maximizing light interception by the trees because light energy falling on the grass in the alleyways obviously is not producing fruits. The second is to optimize light distribution within the canopy, and interception of light by different parts of the canopy, so as to maximize the efficiency of light utilization in photosynthesis and fruit growth, fruit bud formation, and fruit coloring. A brief general review on many aspects of this subject has been
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published recently in French by Odier (1978a,b). Most of the work to date has been on apples and this review, therefore, concentrates on these. 11. LIGHT INTERCEPTION BY THE CANOPY AS A WHOLE
A. The Concept of Light-Interception as a Yield-Limiting Factor The dry matter yields of many other crops appear to be directly proportional to their interception of radiant energy (Duncan et al. 1973; Loomis and Gerakis 1975; Monteith 1977; Gallagher and Biscoe 1978). Recent studies (Palmer 1976; Jackson 1978) indicate th a t the same holds true for both dry matter and economic (fruit) yield of apple orchards, a t least when comparing young orchards of the same rootstock/scion combination managed in a consistent way but growing a t a range of densities. In annual crops the greatest loss of light interception occurs a t the beginning and a t the end of the season. Such crops frequently intercept virtually all the available light a t full canopy (Sceicz 1974) but may be slow to attain this because of delayed leaf emergence and slow leaf growth in spring (Watson 1952; Sibma 1977), while in the autumn senescence of leaves may reduce interception while conditions are still suitable for growth. Orchard crops, on the other hand, tend to attain their maximum leaf area by mid-summer but usually intercept no more than 65 to 70% of available light a t full canopy and may take many years to attain this level. This slow buildup of canopy structure over the years, together with the relatively low light interception a t full canopy, offers real scope to the crop physiologist, pomologist, and plant breeder to improve lifetime orchard light interception.
B. Canopy Development and Structure 1. The Basic Approach as Used in Productivity Studies on Continuous-Canopy Crops.-In annual crops much information about the size of the photosynthetic system has been obtained by measuring leaf area index (LAI) which is the ratio of leaf area (one side) to ground area. This can be measured simply, although laboriously, without use of sophisticated equipment and, for annual crops, has given a large body of information which can be considered to parallel th a t which is now being gained on light interception (Monteith 1977). LA1 d a ta are being used in conjunction with light interception records to analyse the basis of canopy productivity (Loomis et al. 1971; Cooper 1976; Monteith 1977). In general the penetration of light down the canopy follows Equation 1.
IJIo = e -K'.
(Equation 1)
L I G H T INTERCEPTION & IJTILIZATION BY ORCHARD SYSTEMS
21 1
when I,, = incident light energy, IL = light penetrating a leaf area index of L, and K = the extinction coefficient for visible radiation. Light intensity therefore declines logarithmically with LA1 from the top of the canopy, and total interception is consequently a logarithmic function of LAI. T h e extinction coefficient K varies among species, but once this has been determined data on LA1 can be used to estimate interception retrospectively or, a t least, to provide information as to when interception must have been virtually complete. 2. Measurement of Leaf Area Index in Orchards.-In contrast to other crops there is very little published data on orchard LAI. One reason for this is doubt as to the way in which information on LA1 can be used in orchard studies. The typical orchard does not form a continuous canopy but consists either of “round headed” trees grown with access to each from all sides or as hedgerows in which the trees are contiguous in one direction (the row) and adjacent hedgerows are separated by alleyways. Typical foliage distributions in orchards of these types have been shown by Heinicke (1963b), Jackson (1970), and Verheij and Verwer (1973). Under these conditions some light reaches the orchard floor without passing through the canopy while the ground under the center of the trees is shaded by a much greater LA1 than the orchard average. A single equation of the type given previously cannot, therefore, simply relate LA1 to light interception and penetration. To meet this problem of the discontinuous canopy, Barlow (1970) suggested t hat LA1 be considered in relation to ground area covered by the tree a s well as in the more usual sense in relation to total ground area. He did not elaborate on this concept but it is obvious th a t a single figure for mean LA1 over the ground area covered by a tree would not necessarily give useful information in relation to energy interception. For example, a very tall columnar tree or thin hedgerow of the palmette type could have a high vertically-summed LA1 a t the base, but unless shaded by adjacent trees or hedgerows the light a t any point in the canopy would be more dependent on distance from the outside (the outer vertical surface) than from the top, i.e., than on vertically-summed LAI. As in other discontinous canopies, it is essential to know leaf area distribution in both horizontal and vertical dimensions over the entire orchard surface before the information can be integrated successfully with light measurements by means to be discussed. A three-dimensional grid method of measurement, as used by the above authors, including a record of “empty” space, is needed. Orchard LA1 measurements in themselves do, however, provide a useful measure of the amount of photosynthetic surface for comparisons with annual crops which then suggest some obvious approaches to increasing crop production. In making such comparisons it must be remembered th at a discontinuous canopy with, in
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effect, clumps of relatively tightly packed leaves separated by large spaces is less efficient in light interception than a continuous canopy with randomly dispersed leaves. A given value for orchard LA1 therefore represents less potential for light interception and photosynthetic production than an equivalent value in a continuous canopy crop. A second reason for the paucity of information on orchard LA1 is that of technical difficulty. The usual techniques of growth analysis in which leaf area is estimated involve destructive sampling which is very difficult and expensive if applied to experiments covering the productive life of large trees. As a result destructive sampling methods have been used primarily on small potted trees (Maggs 1960, 1963; Avery 1969; Priestley 1969; Hansen 1971), although some studies on orchard trees have been reported (Verheij 1972; Dudney 1974). Standard growth analysis techniques may become more widely used as tree size is reduced and tree numbers per hectare are increased. For example, the bed-systems on M 27 rootstock a t East Malling Research Station involve plants of an individual size and a t a spacing not dissimilar to that of cotton (which has proved very suitable for growth analysis). However, a t present the emphasis is on non-destructive measurement techniques. Individual leaf area can be measured in the field with methods using the ratio of linear dimensions to area. Gladysev (1969) found consistent relationships between the area of a leaf and that of its containing rectangle for six apple cultivars; the ratios ranged from 0.681 to 0.735, and those for leaves from the external and the internal parts of the crown were the same. Kumar and Srivastava (1974) determined the leaf area of 31 apple cultivars by multiplying width X length X 0.708 and found that this agreed well with planimeter measurements. Fulga (1975) found that width X length X ?4gave a good measure of the area of leaves of three apple and three plum cultivars. Kumar et al. (1977) calculated leaf areas of a number of apricot, peach, plum, pear, and guava cultivars from lengths (0, breadths (b), and leaf factors (K) and found the latter to vary from 0.67 to 0.758. Serafimova (1974) used a different equation which when converted to the standard form shows leaf area to equal 1 X b X 0.66, 1 X b X 0.67, and 1 X b X 0.73 for three cultivars of apricots. Other recent studies are those of Abramov and Kutnetzov (1973), Gyuro and Molnar (1974), Molnar and Szakall (1971), Analytis et al. (19711, and Ovsyannikov (1972). Freeman and Bolas (1956) developed a very rapid technique involving a transparent grid which is calibrated so as to read leaf area directly from observation of the maximum leaf width and the distance from the leaf base a t which this is found. This method has been widely used (Maggs 1963; Jackson 1970; Palmer and Jackson 1977). Alternative approaches are to use photoelectric leaf area meters (Marshall 1968; Schurer 1971; Cox 1972). Some commercially available
LIGHT INTERCEPTION & UTILIZATION BY ORCHARD SYSTEMS
213
meters can be used in the field but they are generally better used in the laboratory, to measure samples brought back from the field, than in the orchard, especially where large trees and the need to use ladders are involved. The convoluted nature of outside leaves also makes it difficult to measure their area in situ. Extension shoot leaves are usually appreciably larger than short-shoot (i.e., spur) leaves (Barlow 1969; Jackson 1970), so sampling methods must ensure that both populations are properly represented. Barlow (1969) did this by counting all extension shoot leaves and removing one in seven for measurement in the laboratory, and by counting the total number of short-shoots and removing one in ten for measurement of its total leaf area. While this technique is not too difficult for small trees it is extremely laborious if applied to enough trees to provide an adequate sample of an orchard. To obtain good estimates of orchard LA1 the relationship between leaf area and the girth of the branch or trunk bearing the leaves can be used to supplement the detailed measurements. Holland (1968) showed that the total leaf area (A) on a branch of ‘Cox’s Orange Pippin’ scion cultivar on M 2 rootstocks was related to its girth (GI according to the equation: log A = log K + b log G
(Equation 2)
The coefficient (b) varied with time of season, as would be expected since tree leaf area obviously rises to a plateau then declines as the season progresses (Palmer and Jackson 1977), whereas girth rises but does not decline. Taking July values, when apple trees are a t full canopy, he found that the equation: log A = 3.159 + 2.215 (k0.202) log G
(Equation 3)
applied to leaf area per branch or to whole trees when G is taken as branch girth or trunk girth, respectively. He suggested that leaf area per tree could be estimated from trunk girth provided that the K value (in this case 2.215) was first established from a sample of 15 to 20 branch girths and leaf areas (not necessarily from the same tree). A similar approach has been used by Indenko and Rasulov (1976) who devised a system based on the relationship between the cross sectional area of the first four primary branches and the total leaf surface of these branches. Barlow (1969) studied leaf area-branch diameter relationships for ‘Cox’ trees on M 9 and M 16 which had been pruned either very lightly or very heavily for 14 years and either deblossomed or allowed to crop, so giving 8 factorial treatment combinations. For seven of these treatments
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HORTICULTURAL REVIEWS
branch leaf area was related to diameter (measured a t the point above which the leaf area was recorded) as shown in Equation 4. log A = 0.3298 + 2.5866 log D
(Equation 4)
where the standard error for the regression coefficient was apparently similar to Holland’s. Only the lightly pruned cropping trees on M 16 failed to fit this relationship although they did show their own highly significant regression of leaf area on branch diameter. Verheij (1972) measured the leaf areas of large numbers of unpruned, pruned, fruiting, and deblossomed apple trees of ‘Golden Delicious’ on M 9 and related these to measured trunk diameters. The overall correlation was high (R = 0.85)’ with the single regression corresponding to : log A = -2.05
+ 2.23 (*0.09) log D
(Equation 5)
where A = tree leaf area and D= trunk diameter, giving a significant fit to the complete scatter of points. Although detailed analyses showed no significant differences between the slopes of the regressions calculated for the different treatments separately they did show significant differences in intercept. This is made clear from Fig. 5.1, which is a simplified version of Verheij’s scatter diagram with two of the treatments omitted. In the three detailed studies the regression coefficients of 2.22, 2.59, and 2.23 are remarkably similar (the fact that Equation 2 deals with girth and the others with diameter affects intercept but not slope), but the differences in intercept are great. The regression equations, therefore, cannot be regarded as consistent enough for any single one to be used generally to estimate leaf area from trunk girth. Such an approach could be particularly misleading in comparing young with old orchards in which girth increment continues for many years although pruning can stabilize the leaf area. However, measurement of the leaf area to diameter relationship within a treatment within a season, can, if it establishes as good a relationship as found by the three authors cited, greatly reduce the sampling problem of which trees to measure in an orchard to establish the orchard LAI. If a sufficiently wide range of tree, or even branch, girths are measured in relation to leaf area, the leaf areas on all the other trees can be calculated from their girths. Summing the total leaf areas obtained in this way is likely to give a better measurement of orchard LA1 than simply assuming that the trees taken for detailed leaf area measurements are an adequate random sample. 3. Orchard Canopy Development over the Season.-In annual crops increasing the length of the growing season often would allow them to
LIGHT INTERCEPTION & UTILIZATION BY ORCHARD SYSTEMS leaf area
dm2
1500
1000
500
o
unpruned fruiting
A
pruned deblossomed
0
b
0
I
30
I
LO
I
50
I
60
I
70
trunk diameter, mm FIG. 5.1. THE RELATIONSHIP BETWEEN LEAF AREA AND TRUNK DIAMETER OF TREES OF GOLDEN DELICIOUS / M 9 The regression curve shown is from the original diagram of Verheij (1973) which included 4 treatments. The points from two of these have been removed to make the difference in intercepts between extreme treatments clearer.
215
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HORTICULTURAL REVIEWS
intercept more light (Watson 1947). Sibma (1977) has shown th a t the time a t which a closed crop canopy can be obtained in spring is a n important determinant of yield of potatoes, sugar-beets, and winter wheat. He also showed that maize yields can be improved by accelerating leaf development in spring. In tree crops the rate of canopy development in spring varies with cultivar and also with the proportions of the foliage borne on preexisting short shoots (spurs) and on current year’s extension shoots. The apple spur leaf canopy emerges first, and Cain (1973) noted t ha t its development appeared to be complete by the end of petalfall (in May) a t a stage when new shoots were 1%to 2 in. long with 1 or 2 partially expanded leaves. These shoots then continue to grow, in England, up to July or even August. Palmer and Jackson (1977) found th at a t full leaf in late July only 63% of the leaf area of 3-year-old apple trees of ‘Golden Delicious’/M 9 was on spurs, but the proportion rose to 80% in the following year. This effect of tree age on the proportion of leaves on preexistent spurs and on current season’s growth renders d ata from young trees, especially from very young potted trees of the type suited to growth analysis experiments, unsuited for extrapolation to the mature orchard situation. Barlow (1969) found th at the proportion of the total leaf area borne on short shoots was reduced by heavy pruning a n d by the absence of crop (i.e., by the treatments which promote extension shoot growth) a s shown in Table 5.1. Almost identical results were obtained on M 16 rootstock (Barlow 1969). The treatments were very severe, the trees having been pruned very lightly or exceptionally heavily and either deblossomed or allowed to crop for 14 years prior to the measurements so th a t the differences are greater than would be found normally. They do, however, indicate t ha t trees of similar peak LA1 could have very different leaf area durations (integrals of LA1 over the season) with the most rapid buildup to maximum LA1 coming from lightly pruned, heavily cropped trees. TABLE 5.1. LEAF AREA ON SHORT SHOOTS AS A PERCENTAGE OF THE TOTAL LEAF AREA OF MATURE APPLE TREES OF COX’S ORANGE PIPPIN /M 9
Pruning Light Heavv
Cropping Trees 86.4 55.4
Non-Cropping Trees 69.1 35.2
Modern orchards aim to combine heavy cropping with light pruning. The pattern of canopy development in such a n orchard of ‘Golden Delicious’/M 9a was described by Palmer an d Jackson (1977). Their results show attainment of maximum leaf area within a month of first leaf
LIGHT INTERCEPTION & UTILIZATION BY ORCHARD SYSTEMS
217
emergence, i.e., by early June, and maintenance of the plateau level of LA1 until mid- to late October. Although they commented that ‘Cox’ attained its maximum leaf area later than ‘Golden Delicious’, it seems that both cultivars attain ceiling LA1 earlier than many annual crops. However, since maximum energy availability is in mid-June (Jackson and Landsberg 1972) maximum LA1 in England is not attained until, from the irradiation point of view, the season is half over. Leafing-out of temperate fruit crops follows blossoming, and most blossoms are very frost-sensitive. Since in southern England frost severely reduces apple yields in about one year in five, and frost incidence is greater earlier in spring (Hamer and Jackson 1975), any attempt to obtain greater total radiation interception by earlier leafing-out, hence blossoming, would lead to considerable risk of crop loss unless frost protection could be guaranteed or frost-resistant cultivars produced. This limitation parallels that for grasses where Cooper (1964) has pointed out that good early growth has to be associated with frost hardiness. In apple the correlation between date of leafing and date of flowering (Tydeman 1964) is so close that late leafing-out was used as a selection criterion to obtain late flowering, hence frost-avoiding, types. T h e indirect as well as direct benefits which would come from genuinely frost-tolerant blossoms are obvious. Canopy Development over the Orchard Lifetime.-Comprehensive data on the buildup of LA1 over the years have yet to be published, but it is clear that the process is generally slow and is greatly dependent on tree vigor, spacing, and management. Preston (1958) commented on the results of a long-term experiment on apples as follows: “After thirtyfive years growth and cropping there appeared to be no falling off in shoot growth except during the period when the trees were overcrowded.” The latter comment referred to a period before year 27 in which some of the trees were removed to allow the others more room for growth. These results were obtained with ‘Lane’s Prince Albert’ on a range of rootstocks from the dwarfing M 9 to the very vigorous M 16. Even on the former rootstock the trees were still growing vigorously and increasing in size from the age of 30 to 35 and, in fact, continued to do so later (Preston, personal communication). Consequently, it is reasonable to suppose that if apple trees were planted a t a spacing appropriate to their potential size, the orchard would not attain its ceiling LA1 until it was more than 30 years old. This, of course, is not commercial practice. In previous years orchards were planted with “permanent” and “filler” trees; the latter were removed as the trees began to compete for light with each other and became so crowded t h a t management was difficult. In more modern systems the trees are deliberately grown in the nursery so as to have a large number of lateral “branches” already present a t the 4.
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time of planting (Van Oosten 1978; Quinlan 1978).Then they are planted as close together in the row as seems feasible from the point of view of constraint of the mature tree within its allotted space using all the best techniques of vigor control (Jackson 1975a; Jackson et al. 1978). The buildup to ceiling LA1 is thus as rapid as possible. In general, the less vigorous the rootstock used the more readily is the risk of overcrowding accepted, the smaller is that risk, and, in examples studied to date, the more rapidly has ceiling LA1 been attained. Little comprehensive data have been published. Jackson (197513)showed the curve of leaf dry weight per tree for the first nine years of an experiment involving ‘Cox’ on MM 104 (vigorous) and M 26 (semi-dwarfing)rootstocks. Whereas leaf weight per tree had increased steadily over this period on MM 104, on M 26 the curve was flattening by the seventh year and the leaf weights were the same in the eighth and ninth years. At 9 years the LAIs on an orchard basis would have been 1.49 (on MM 104) and 1.36 (on M 26). With ‘Golden Delicious’ on M 9a, with minimal pruning, according to slender-spindlebush practice, the buildup of LA1 was much more rapid. Palmer and Jackson (1977) found that where such trees were planted a t 2.9 m X 0.9 m spacing, the LA1 a t 5 years of age (1.5) was no greater than in the previous year. Where the very dwarfing M 27 was used as a rootstock, Palmer and Jackson (1977) found that 4-year-old trees of ‘Cox’ planted a t 1.5 m X 0.5 m between trees had a very similar LA1 to 2-year-old trees on the same system (51.4). In this planting (Preston 1978), the prime objective was to obtain a shallow cropping canopy over the orchard surface as quickly as possible. In general the larger the trees are a t planting in relation to their ultimate size, the more rapidly ceiling LAIs are obtained. Although this objective also could be achieved by using trees with a high growth rate (as is found when vigorous rootstocks are used), this approach is not likely to become acceptable until inexpensive methods become available for controlling the growth of such trees once they have filled their allotted space. 5. Leaf Area Indices of Mature Orchards.-Measured values, usually derived from very few trees, show orchard LAIs to be low by the standards of other crops. Verheij and Verwer (1973) found the LAIs for typical, well grown hedgerows of ‘Golden Delicious’ on M 9 and M 2 to be 2.15 and 2.45, respectively, and concluded from effects on fruit yield and quality that the latter was too dense. Palmer and Jackson (1977) found peak LA1 in the orchard of ‘Golden Delicious’/M 9a referred to above to be only about 1.5. Olaniran (1974) found LAIs for hedgerowstyle orchards of ‘Cox’/MM 106 to range from 1.66 (palmettes a t 4.11 m X 3.66 m) to 2.19 (pillars a t 4.11 m X 1.83 m). Heinicke (1964) studied mature trees pruned to either open center shapes, if they were very large “standard” trees, or as modified center-leader trees if they were smaller
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(semi-standard, semi-dwarf, and dwarf) and found LAIs ranging from 3.1 to 4.6. In this orchard, however, the individual trees overlapped especially in the denser plantings where the use of a hand gun for pesticide spraying permitted overlap in both directions. In more typical orchards with alleyways for tractor access, Jackson (1970) reported the highest LA1 recorded in a cropping orchard a t East Malling Research Station to be 2.6. The orchard was that described by Jackson and Palmer (1972) with 5 m high trees with almost spherical crowns, planted a t 5.9 m X 5.9 m, in contact within the row and touching over the top of the alleys.
C. The Relationship Between Orchard LA1 and Light Interception 1. Theoretical Studies of the Effects of Canopy Arrangement and Density.-a. General Concepts.-Monsi, Uchijima and Oikawa (1973) reviewed the relationships between canopy structure and light interception for a number of natural plant communities and crop stands. They pointed out the contrast between stands in which the foliage can be assumed to be randomly arranged, where equations such as IL/Io= e - K L (p. 210) can be applied, and those canopies where the leaves are not randomly distributed and the mathematical description is much more difficult. They also commented on the paucity of work on forests and orchards in this respect. A number of separate attempts have been made to provide adequate mathematical descriptions or computer models of light interception and distribution in discontinuous canopies like those of orchards. Such models could be, and are, extremely valuable as an aid to efficient orchard design because of the very great difficulty in carrying out adequate experimentation with a long-term tree crop to determine its optimal configuration in three dimensions. In considering these models in the course of writing this review it became obvious that it is helpful to consider light transmission through the orchard canopy a t two distinct hierarchial levels. First, for an orchard of any given geometry, there is the light which will reach the orchard floor irrespective of the leaf area index. This is the light which would be transmitted to the ground even if the trees were solid because it passes through gaps between the trees. Secondly, there is light which reaches the orchard floor after transmission through the tree canopy, i.e., through gaps between leaves within the tree volume and, to a much lesser extent, through the leaves. This can be expressed simply:
T = Tf + T,
(Equation 6)
where T = total transmission to the ground, Tf= transmission solely dependent on orchard form, i.e., which would be transmitted to the floor
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HORTICULTURAL REVIEWS
of a “solid model” orchard, and T, = transmission through the canopy, hence dependent on leaf area density, etc. This concept is expanded later in the review but is introduced here to assist in interpretation of other work.
b. Solid-Model Hedgerow Studies.-Over a considerable period of time there has been a trend for square-planted, round-headed trees to be replaced by orchards in which the trees are arranged in continuous hedgerows separated by alleyways to enable access by tractors for spraying and harvesting. These hedgerows offer easier and cheaper pruning, thinning, and picking (Gyuro 1978; Werth 1978) and, because of their higher densities of planting, give heavier crops per hectare in the early years after planting. Among the earlier successful orchards of this type were those of palmette-trained trees in Italy, typically planted with a spacing of 4 to 4.5 m between the centers of rows which are 4 to 4.5 m high and 1 to 2 m thick (Rosati 1978; Sansavini 1978). Especially where such orchards are mechanically pruned to a fixed “cutting plan,” they have a relatively sharply defined geometry which must be chosen so a s to optimize total interception (i.e., minimize T) while avoiding excess rowto-row shading which would reduce the productivity of the lower a n d more easily accessible parts of the trees. The consequent questions of row orientation, configuration, and spacing also arose with regard to the adoption of dwarf-tree spindlebush hedgerows (Wertheim 1978) in Holland a nd later over much of Europe. Moves toward over-row systems of mechanical harvesting, requiring the trees to be contained to a precise form, raise even more specific questions. It is obviously important to be able to calculate the effects of given tree configurations on light interception, hence potential productivity as a guide to over-row machine design. T he first approaches to this problem of tree design assumed th a t the hedgerows (Jackson and Palmer 1971, 1972; Cain 1972) or individual conical trees in rows (Ferguson 1960) were non-reflecting and non-transmitting. T he measured mean reflection coefficients of apple trees are 0.17 (Proctor et al. 1972) and 0.15 (Landsberg et al. 1975), and the former authors found th at the mean coefficients for the tree, dry grass, and inter-tree space components of the overall reflection were 0.142, 0.169, and 0.179, respectively. These figures refer to total shortwave radiation. Palmer and Jackson (1977) found the reflection coefficient for visible light to be 0.055. Ignoring reflection altogether probably introduces little error into the calculation of relative interception by trees of differing dimensions, although it may bias estimates of total energy capture. T he degree of error which results from assuming th a t the trees are non-transmitting depends on their total leaf area and leaf area density.
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Dense trees can produce virtually “solid” shadows without appreciable sunfleck penetration. Cain (1971) showed that with cutter-bar-hedged trees 12 feet high, 1 2 feet wide a t the base, and 4 feet wide a t the top, light intensity in the line of the tree center was 50% of full daylight a t 2 feet from the top declining to 30% a t 3 feet, 20% a t 6 feet, and 16% a t 8 feet when the rows were 20 feet apart. T o have passed through the trees, most light would have had to traverse more than twice the depth of canopy penetrated on the way to the vertical center line, so total transmission through the canopy to the ground below the trees or the alleys on either side must have been very slight. In typical northern European orchards with low LAIs, transmission through the trees (T,) is likely to be appreciable. Even in this latter case, however, the results of “solid model” analyses are useful. They define the effects of hedgerow “form” as such with regard to the limits to maximum interception, and also reveal the way in which the “shape” of an orchard results in significant effects of factors other than those found important in light interception by random foliage ((Monsi and Saeki 1953; de Wit 1965) or by square-planted stands (Oikawa 1977a,b).
i. Hedgerow “Form” Limits to Light Interception. The calculation of “solid model” light interception shows the maximum interception possible by hedgerows of given dimensions and can be used in conjunction with field measurements as a guide to orchard design. The maximum proportion of incident light which can be intercepted by a hedgerow is a function of (a) the proportion of ground which is directly covered and (b) the height of the hedge, especially of its “outside” edges, in relation to the clear alleyway width. This interception can be quite high. For example, a solid hedge with vertical sides which is twice as high as the clear-alley width and as wide as the latter (e.g., a 4 m high hedge, 2 m thick and separated by a 2 m wide clear alleyway (Fig. 5.2 (i)) would, if oriented N-S a t 51.3”N (England), intercept about 89% of direct and 87% of diffuse light (Jackson and Palmer 1972). If half this height (Fig. 5.2 (ii)), interception would be 81% and 77%, respectively. If then slimmed down to become only 1 m thick for mechanical over-row harvesting (Fig. 5.2 (iii)), it would intercept 74.6% of direct light (Table 1 in Jackson and Palmer 1972) and 69.3% of diffuse light. This latter configuration corresponds to hedgerows 2 m high and 1 m thick separated by a 2 m clear alleyway as described by Tukey (1978). From Fig. 5.2 (iv) and (v) it is, however, clear that triangular section hedgerows need to be appreciably taller to intercept a high proportion of available radiation. It is likely t h a t many orchards, especially on M 9 rootstock, which have trees of this shape (which is desirable from the point of view of even light distribution over the surface) do not attain the desirable ratio of hedge height equal to a t least twice clear-alley width. Where
222
H
HORTICULTURAL REVIEWS
IM B
C
A
B
d
(i i)
B
A
B
IH
(iii)
B
A
B
lH lH
Courtesy of Jackson and Palmer (1972) FIG. 5.2. LIMITING EFFECTS OF ORCHARD GEOMETRY ON LIGHT INTERCEPTION AND DISTRIBUTION The above non-transmitting, non-reflecting model orchards would intercept the following proportions of available radiation (assuming 50% direct, 50% diffuse from a S.O.C. at 51.3”N May-Oct). (i) 88 (ii) 79 (iii) 72 (iv) 79 (v) 67 When H = Hedge Height B = Hedge Base A = Alleyway. The angles c a d, c a d, c b d and c b d determine the sector of the sky from which direct and diffuse insolation is received at points a, a, b and b, respectively.
measured values of light interception fall appreciably below those estimated from “solid model” calculations, T, must be appreciable and interception could be increased by increasing leaf area within the existing tree shape. Where Tf, as calculated assuming solid hedgerows, is unacceptably large, the only solution is to increase tree dimensions or decrease spacing. ii. Hedgerow “Form” Effects on Light Distribution. For the same reasons that hedgerow form sets an upper limit to potential light interception it also sets an upper limit to the extent to which one hedgerow
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will shade its neighbor. I t is possible to calculate the maximum extent to which the light received by any part of a hedgerow surface is reduced by the effects of orchard geometry on the proportion of the sky which it "sees," i.e., from which it can receive direct and diffuse light. Clearly, in Fig. 5.2 both points a and a' receive diffuse light from a greater proportion of the sky than do points b and b', and also will be subject to direct shading from the adjacent hedge for a shorter period during the day. Also, a and b will receive more direct light and more diffuse light than a' and b'. The mathematical relationships are described fully by Jackson and Palmer (1972) and Cain (1972),who concluded that angled hedgerow surfaces would give much more even light distribution than vertical ones (Cain concluding that a 20" wall angle (70" to the horizontal) with tree height twice clear-alley width would give maximum efficiency), and that N-S rows would be preferable to E-W ones because they give much more even distribution over the surfaces. Jackson and Palmer (1972) showed that if the hedgerow sides were vertical, then increasing height from equal to alley width to twice or three times this simply increased the area of inadequately illuminated surface while a corresponding increase in height of a triangular section tree could give useful gains. I t should be noted that if the hedgerows transmit light then the relative surface irradiances shown by the solid model studies would be increased, i.e., they give lower limits to illumination.
iii. Effects of Row Orientation and Latitude. The percentage of available direct light which is intercepted, depending as it does on the length of shadows cast over the alleyways, is controlled by the position of the sun in relation to the hedges and by the distance between these. The effect of row orientation on interception therefore varies with time of day and season, latitude, and orchard geometry. Some apparently contradictory results in the literature arise from this complexity. T h e most detailed information is presented by Jackson and Palmer (1972) who showed that whereas a t 34" latitude all the "solid" hedgerow systems which they examined intercepted more radiation over the growing season if oriented N-S than if oriented E-W, this was the case only for low hedges (hedge height = alley width) a t 51.3'. At this latitude tall hedges (height = 3 X alley width) intercepted more light if oriented E-W. Moreover, while the relative efficiency of a N-S hedge in intercepting light changes little as the season progresses, E-W hedgerows are relatively inefficient in mid-summer due to the high sun angle (especially a t lower latitudes), but intercept more direct light than N-S hedges in August, September, and October (especially if tall and a t high latitudes). From the total interception point of view, N-S hedgerows therefore will tend to be preferable with low hedgerows and where leafing-out occurs early, E-W hedgerows only a t high latitudes with tall trees and late
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maturing cultivars. Ferguson (19601, who recommended E- W hedgerows from the results of his model study, did so on the basis of their higher light interception under his high latitude conditions in Holland in September with tall (4.5 m high) trees in rows with only 1.5 m clear space between them. Cain (19721, who found N-S orientation to intercept more light except very late in the growing season, noted that his results (initially calculated for 43" latitude) did not agree with Ferguson's even when re-calculated for 53",although they moved closer then. His calculations were, however, for effectively lower trees with a height of 3.05 m to a clear-alley width of 2.44 m and for a shorter growing season in New York than the western European one. He assumed termination on September 15 with the beginning of leaf senescence whereas, as noted earlier, in western Europe LA1 does not decline until mid- to late October. In England the main cultivars are harvested in late September or early October, 'Crispin' ('Mutsu') is not harvested until mid-October. Although there is little difference in total interception between E-W and N-S hedgerows with the relatively low trees which are now grown under western European conditions, the N-Sones are preferable because of the much more even distribution of radiation over their surfaces. The N side of an E-W hedgerow receives very little direct light unless gently angled.
c. Transmission Models Assuming Beers-Law Relationships.-Palmer (1977b) extended the "solid model" of Jackson and Palmer (1972) to incorporate transmission through the canopy (TJ. He measured the amount of shading structure (leaf area, projected fruit area, and projected branch area) in hedgerow orchards of 'Golden Delicious'/M 9a, and calculated the passage of a representative number of beams of light through such a structure so as to estimate the relative irradiance a t 40 positions on the orchard floor between the row and the alley centers. In this work it was assumed that the shading material was equally distributed throughout the hedge and that light attenuation within the hedge was logarithmic with respect to the amount of intercepting material. The area indices were reduced to densities, depending on hedge dimensions and spacing and clumping coefficients introduced as shown in Equation 7:
I
I,
=e
-kl"(L kzk3+ F/sin A + k5 (Bl/tan A + BPk 4 ) l (Equation 7)
where I, = irradiance above the canopy, I = the irradiance below the canopy, d = the vertical depth of canopy traversed by the light beam, L, F, B1 and BP= leaf area, fruit area, vertical branch area, and horizontal
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branch area indices, respectively; k, reduces the area indices into densities and depends on hedge dimensions and spacing; A = the solar altitude; k2 and kx = the leaf extinction coefficients depending on clumping and leaf angle, respectively; k5 = a clumping coefficient for branch areas (0.85 in winter), and k4 = the extinction coefficient for horizontal cylinders dependent on A, as calculated by Monteith (1973). Results predicted from the model were compared with measured values for three different hedgerow spacings. Prediction of diffuse light interception was excellent (r2averaging 0.98), and that of direct light was less (r2ranging from 0.90 to 0.95) but still very good. It made little difference to the results if leaves were assumed to be a t angles of 45" or 60" or following a spherical distribution. Since the combined Fruit Area Index, Vertical Branch Area Index, and Horizontal Branch Area Index ranged from 10 to 15% of the LAI, it is obvious that they had an appreciable effect on light interception but not a dominant one. In general this model confirmed the conclusions with regard to effect of row orientation and time of season which had been derived from the solid models. Charles-Edwards and Thorpe (1976) assumed apple hedgerow canopies to be ellipsoidal in shape and to be made up of a large number of small, randomly inclined and oriented leaves distributed with equal probability through the volume of the canopy. They then calculated direct beam and diffuse light transmission through such a canopy given dimensions equivalent to those of an actual orchard at Long Ashton, and found good agreement with measured values in the field. Seasonal variation in direct beam radiation as estimated by their model was similar to that calculated by Jackson and Palmer (1972) and, for an orchard of the dimensions which they studied, they found that E-W oriented rows intercept approximately 13% less direct beam radiation than N-S oriented rows in June. The canopy extinction coefficient used in this study related to a projected leaf area index in the beam path, so its numerical value (1)does not correspond with extinction coefficients as empirically determined in apple canopies (see p. 242).
d. Monte Carlo Simulation Techniques.-Oikawa and Saeki (1977) and Oikawa (1977a,b) used a computer model which defined the position of each individual leaf, including its azimuth and angle to the horizontal, in three dimensions. The leaves were assumed to have no thickness, not to reflect or transmit light, and to be the only light-intercepting structures present. For any given analysis they were assumed to have a constant, or regularly varying, inclination and arrangement, although this in itself was treated as an experimental variable. A large number of varying leaf arrangments then were simulated in the computer, and the passage of light through each of the chosen "canopies" was calculated for (usually) 2000 light beams. These light beams col-
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lectively had altitude and azimuth angle frequency distributions similar to the relative probability densities of these for diffuse light from a uniformly overcast sky (U.O.C.). T he assumptions about foliage characteristics which have been used in the Monte-Carlo approach do not correspond to real canopies. Because empirically determined extinction coefficients are not used, there is no way of adjusting general conclusions obtained from the model to take into account particular crop characteristics. Since the canopy has to be specified completely (leaf by leaf) within the computer, this approach is less than ideal for investigating the comparative productivity of a wide range of structurally complex orchard canopies. T h e Monte-Carlo method is, however, the only one which does not assume random foliage distribution a t least within the canopy, so it provides the best tests of the effects of particular types of non-randomness in foliage arrangement. (It should be noted, though, th at calculations of Tf as described earlier are based solely on known trigonometrical relationships and distribution of direct and diffuse light, and do not rest on any assumptions of foliage distribution .) The major points of relevance to the orchard situation which are demonstrated by Oikawa’s studies are: (1)If, instead of being randomly arranged throughout a canopy volume, leaves are grouped in vertical columns of the types shown in Fig. 5.3, then light penetration would be as shown in Fig. 5.4. This shows th a t with such “plants” (which would correspond to a meadow-orchard, singleshoot tree or an upright, unbranched spur-type like ‘Wijcik McIntosh’) the interception per unit of orchard LA1 is increased a s the number of plants per unit ground area is increased and the leaf area per plant reduced (by reducing leaf area density, not canopy volume).
(2) With constant planting density and LAI, light interception is increased as leaf area density is decreased (i.e., if the same leaf area is dispersed over a larger individual canopy volume). Non-random (square planted) populations differ markedly in this respect from “continuous canopy” populations with random leaf arrangement in which light penetration is fairly independent of leaf area density (Fig. 7 in Oikawa and Saeki 1977).
(3) A “forb” type of leaf density distribution (with closer packing of leaves nearer to the top of the plant) will give less light interception per unit LA1 than if the foliage is distributed evenly up the profile. e. The Simple General Model.-As mentioned earlier, light transmitted to the orchard floor (T)can be regarded as th a t which would have reached
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L.l-100
L.l-100
FIG. 5.3. SQUAREPLANTED POPULATIONS WITH DIFFERENT PLANTING DENSITIES (ND). LEAF DIVERGENCE, 1/3 (120+12"). LEAF INCLINATION ANGLE OF ALL LEAVES, 60" Left column: a plane figure of 100 leaves counted from the top of the foliage. Middle column: a v e r t i c a l figure of plants in the left column of the corresponding plane figure. Abaxial leaf surface is shown by illustrating the midrib. Right column: t r a c k s of beams emitted into the population. The first 50 tracks of 2000 beams are exemplified. a, a bare land; b, ND = 3; c, ND = 4; d, ND = 5; e, ND = 6.
L.1-100
L;1-100
Adapted from Oikawa (1977a)
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1 00
50
0
1
L 2
A
1 3
d=60° 5
D 50cm
>
t; v)
3 3-3cm
z W
I-
s
I-
I W
-1
10
2 5cm
W
2 I4 W
5
20cm
a
16.7cm
1
After Oikawa (1977a)
FIG. 5.4. LIGHT PENETRATION IN SQUARE PLANTED POPULATIONS WITH DIFFERENT PLANTING DENSITIES (SOLID LINES) COMPARED WITH PENETRATION INTO RANDOM POPULATIONS OF SIMILAR LAI'S (DASHED LINE) The numbers at the right end of each solid-line curve show the planting density (ND) as defined in Fig. 5.3 and the planting distance t o which this corresponds if the width per unit land area is taken as 1 m.
the ground even if the trees were solid (Tf)and that which has passed through the individual tree canopies (T,), i.e., T = Tr + T,. Tf can be measured by a range of techniques including (1)the use of solid physical models combined with photography from different angles to derive the equivalent of their projected shadow areas a t different solar altitudes and azimuths (Ferguson 1960), (2) calculations involving a large quantity of empirical data on light sources (Ferguson 19631, and (3) the type of computer or desk-machine modelling described by Jackson and Palmer (1972) and Cain (1972).
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T, is obviously a function of the leaf area in the pathway of light beams traversing the canopy, and as a first approximation the appropriate leaf area function (L’)is LAI/(l-Tf), i.e., LA1 expressed on the basis of the ground area shaded by the tree canopy as measured instantaneously or integrated over the appropriate period of time. Assuming a Beers-law relationship between light penetration and leaf area (Monsi and Saeki 1953), light transmission through an orchard of trees of any shape, spacing, and arrangement would be given by equation: (Equation 8) where K is the extinction coefficient within the tree canopy. Jackson and Palmer (1979) have tested this equation using a K value of 0.6 (see p. 242). Estimates of diffuse light interception by 6 hedgerow orchards were never more than 2% from measured values, and the average prediction of total direct and diffuse radiation was in error only by 2%, although in one individual case the discrepancy was 10% (which could be well within measurement error). Comparing estimates for interception (1-T) for an extremely wide range of hedgerow orchards by this technique and the fully validated model of Palmer (197713)showed a correlation coefficient of 0.99. Application of this type of analysis can be particularly useful to calculate the density of foliage required to maximize light interception in a canopy of any given dimensions. Jackson and Palmer’s (1979) data show that in a closely spaced (2.9 m X 0.9 m), high yielding orchard of ‘Golden Delicious’ on M 9 where 50% of available light was being intercepted, 26% was being lost as transmitted light because of form factors (Tf)and 24% because the canopy was insufficiently dense (Tc).At the wider spacing of 4.25 m X 0.9 m, 42% of all available radiation was lost (transmitted) because of form factors (too-wide spacing) and a further 25% by transmission through the trees. The two-part model also helps to clarify other results. The effects of leaf area density per plant and number of plants per unit area on light interception a t given LAIs (Oikawa 1977a,b) may be explained on the basis that, in a discontinuous canopy, changes which increase canopy volume (and reduce Tf)have a greater effect on interception than do corresponding changes in leaf area within the existing plant outline (which reauce TJ. At the extreme, for example, adding an extra plant into a gap between widely spaced plants can increase direct light interception in linear proportion to the increase in leaf area; increasing density within the existing plant outlines will increase interception in proportion to the increase in log leaf area. Thus, changes in planting density will have greater effects on light interception per unit change in LA1 than will changes in leaf density inside the canopies.
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D. Measurement of Light Interception by Orchard Systems 1. Techniques of Measurement.-a. Basic Requirements.-The major difficulty encountered is th at of sampling since the proportion of available radiation reaching the orchard floor varies with distance from the center of the tree or row and with time of day and season. T h e fraction of light intercepted is 1 - T (or in percentage, 100 - %T),and is measured by determining the intensity of transmitted radiation (T)over a representative part of the orchard floor in relation to the radiation available above the canopy. The minimum area of orchard floor which can be considered representative is th at which corresponds to the “repeating unit” of the planting pattern; the optimum area will consist of a number of such units to take into account variations in tree size. In a hedgerow orchard where the trees have grown into each other to form a continuous row of uniform height and thickness, a single, evenly spaced line of sensors across the alleyway from row center to row center (or even from row center to alley center) may be an adequate sample unit (Verheij and Verwer 1973). In all cases where the canopy is discontinuous in two directions the light sensors should be arranged in a grid. Preferably this should cover the ground area across the alley between the centers of the trunks of adjacent pairs of trees. Alternatively, the center of a single tree can be taken as the center point of a rectangular grid which reaches in each direction to the midpoint between the tree and its neighbors. T h e sensors should be evenly spaced or, if not, the results should be calculated to give even weight to all areas of the orchard floor. For productivity studies i t must be remembered th at light interception is measured a s a representative sample of interception by the orchard a s a whole and not as the interception by a single tree (which, a t all but very wide spacings, is more difficult). T he second sampling problem is th at of time. In canopies providing more or less complete ground cover, light penetration in relation to LA1 does not vary much, a t least over the central eight hours of the day (Monteith 1969). For the reasons described earlier, however, there is a pronounced effect of time of day and time of season on Tf in orchards as a result of changes in solar altitude and azimuth. For these reasons integrating sensors which can be produced cheaply in large numbers are preferred for orchard work. Another major requirement for measuring total interception is th a t the sensors should have a good angular response, i.e., proportional to the cosine of the angle of incidence of light. Jackson and Palmer (1972) showed t ha t large errors were to be expected if this was not the case. By direct measurement they found th at in a hedgerow orchard where the mean percentage of light interception measured by cosine-law sensors was 73%, sensors which responded equally to light from all directions
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above the horizontal measured 84% interception. This is particularly relevant to the use of photochemical methods described later. Finally, it is important that the sensor has an appropriate wavelength response. For productivity studies measurement of photosynthetically active radiation (P.A.R.) is required. This is usually quoted a s 400 to 700 nm, although 380 to 720 nm is more accurate. b. Selenium and Silicon Cells.-Inexpensive sensors meeting these requirements can be made easily by using ready “potted” selenium cells (Jackson and Slater 1967; Jackson 1970; Palmer 1976; Palmer and Jackson 1977). They respond only to light within the required range, and can be filtered easily to ensure a relatively even response over the greater part of this. When fitted with a plastic diffuser they have an excellent cosine response. This diffuser, plus neutral filters, ensures th a t current output is linearly related to incident radiation in the visible range, and this current either can be integrated using a very simple mercury coulombmeter (see also Cain 1969) or recorded a t frequent intervals on a data-logger. If coulombmeters are used, cell output may have to be restricted to ensure linear response. The major problem with selenium cells is t ha t they may fail suddenly or alter in their output characteristics a s they age, so need to be checked regularly. Silicon cells of similar dimensions are much more reliable. When properly assembled they have similar advantages in terms of angular response and linearity of response but are, unfortunately, sensitive to near infrared radiation. Because this is transmitted through leaves much more readily than is P.A.R., use of uncorrected silicon cells would greatly overestimate P.A.R. transmission. Appropriate filter combinations to use with silicon cells to enable measurement of photosynthetically active radiation are discussed by McPherson (1969). T he small size of selenium and silicon cells is, however, a disadvantage when attempting to measure incident radiation over large areas of the orchard floor.
c. Tube Solarimeters.-Tube solarimeters (Szeicz, Monteith and Dos Santos 1964) are usually about 1 m long, so are useful for spatial integration. They respond to total radiation. P.A.R. is estimated by using pairs of tube solarimeters-one with and one without a filter to screen out visible light. Since the filters available for this do not have a sharp cutoff point but do in fact prevent the transmission of some infrared radiation to the thermopiles, the simple difference between filtered and unfiltered solarimeters does not give a measure of visible light. Palmer (1980) has presented an equation for calculation of transmission of visible light from readings obtained with solarimeters with and without each of the two kinds of filters available, after demonstrating small
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but real errors in the original method of adjusting for filter response. Tube solarimeters, being non-circular about the vertical, have errors depending on their azimuth (Lang 1978). Very large cosine errors occur when the direction of the sun is close to the longitudinal axis of the cylinder. This is most likely to occur early in the morning and late in the evening. Lang found that the maximum error did not exceed 67 W/m2 and concluded that this, although representing a large fraction of the irradiance a t the time when it occurred, would be negligible for many purposes. The systematic variation in error with time of day could, however, render tube solarimeters unsuitable for some detailed studies in orchards because of the importance which lateral illumination can assume there. Lang concluded that no single arrangement of a cylindrical radiometer is best for all latitudes, dates, and times of day. d. Photochemical Methods.-Photochemical methods are widely used in orchards (Heinicke 1963a; Maggs 1967; Maggs and Alexander 1970; Verheij and Verwer 1973), but must be treated with caution. The maximum sensitivity of the chemical reaction is in the short wave region of the visible and in the ultraviolet. Consequently, although photochemical actinometers may show responses to variations in total irradiation which are linearly related to those found by physical measurements (Begg and Cunningham 1974),calibrations obtained by exposure of the actinometer and the standard instrument to varying periods of full sunlight do not necessarily apply to all situations. The sensitivity to blue light may lead to overestimation of the total irradiance and transmission where (blue) skylight is prevalent. Palmer (1977a) has shown t h a t skylight makes a large contribution to the light received under the shade of orchard canopies of low LAI. Actinometers could therefore tend to overestimate available radiation in the lower parts of canopies, although the fact that leaves have very low ultraviolet and blue light transmittance will tend to compensate for this. The errors resulting from this may not be too serious when actinometers are used to integrate light climate over some days, but it always will be better to check a proportion of their results under field conditions (e.g., by having a limited number of photocells or solarimeters situated a t varying shade levels among the array of actinometers). The most widely used method involves the photodecomposition of oxalic acid when sensitized by uranyl nitrate. The amount of photodecomposition is obtained by titrating the residual oxalic acid with potassium permanganate, and comparing the reading with the amount of permanganate required to titrate a similar aliquot of an unexposed mixture of oxalic acid and uranyl nitrate. The use of control titrations is essential, and the limits to the validity of the technique should be checked prior to its use. They may depend on the exact type of container
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and irradiation and laboratory conditions. T h e solution is usually exposed in a tube or round-bottomed flask which would tend to give a n equiangular rather than a cosine-law response to irradiation. As mentioned earlier, this can give a systematic error in measuring total light interception of a t least 1076, and could give more or less in specific circumstances. The use of tubes hung in trees, especially those with opaque stoppers, can lead to very serious errors due to their angular responses (Lakso, personal communication). e. Fisheye Photography.-Anderson (1971) described a technique using Fisheye (hemispherical) photographs to determine patterns of light penetration. Smart (1975) used this method in vineyards but it has not been used yet to estimate total light interception in conventional orchards, although it could be suitable for this. Th e photographs, looking upwards, show the proportion of sky which can be “seen” from any given point in or below the canopy and hence the size and frequency of canopy gaps. Early workers in this area used overlay grids with large numbers of “cells,” each of which was examined to estimate the percentage of sky or canopy. Modern techniques of False Colour Densitometry have speeded up the process greatly. Lakso (1976), studying the light climate within apple trees, reported a good relationship (r = 0.87) between integrated P.A.R. and percentage of sky visible in the central 60% of the corresponding fisheye photographs. More recently he has obtained even better agreement with r values generally higher than 0.9 (Lakso in press). Fisheye photography is obviously much less efficient as a light measuring technique than are light sensors with appropriate angular and wavelength response giving an electrical output. I t could, however, be used to estimate Tf and T, independently and so give direct information on the need to change tree dimensions and spacing or to prune to change canopy density within the existing geometry. Fisheye photography, combined with use of a Quantimet image analysing computer, was used to estimate light penetration into first and second cycle meadow orchards (Bennett and Turner 1978). T h e angular bias of the fisheye lenses must be taken into account. 2. Measured Light Interception by Orchard Systems.-In spite of the wide realization th at a high degree of effective ground cover Le., light interception) is essential for high yields (Jackson 1975a; Neuteboom 1978), there have been very few studies on light interception by orchard systems. T he lack of information on the pattern of light interception by different systems over their lifetimes is serious particularly in relation to the current development of many types of high density systems (Jackson 1978) which have the implicit or explicit goal of attaining high levels of productivity much more rapidly than was the case with conventional
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wide-spaced orchards. Because spacing and tree size tend to change simultaneously (so influencing Tf and T, independently) when systems are changed, information on planting density alone is of little use in assessing potential productivity. a. Light lnterception over the Season.-With N-S rows, seasonal changes of solar altitude and azimuth have very little effect on potential interception, so that the seasonal pattern of light interception is primarily determined by changes in tree canopy size and density. Jackson (1975b) found t ha t interception by a closely spaced (3.05 m X 2.44 m) mature apple hedgerow orchard of ‘Laxton’s Superb’ and ‘Fortune’ on M 26 expressed as a percentage of available light was 18, 35, 61 and 69 in late April, early May, early June, and early July, respectively. Palmer and Jackson (1977) found differing patterns in different seasons with hedgerow (‘Golden Delicious’/M 9) orchards, but interception in both years rose steeply in May then slowly to reach a peak in September/ October. This latter peak was not very pronounced and, since LA1 was actually lower then than previously, was most probably a result of a change in canopy dimensions with cropping and of lower solar angles. As the canopy becomes more widely spreading, Tf will decrease in such a way as to more than compensate for increase in T, (because a given leaf area in the larger canopy will intercept more light th a t would otherwise fall on the alley). Verheij and Verwer (1973) also found light interception in September to be slightly higher than in the earlier months in N-S hedgerows of Golden Delicious on M 9 and M 2. T h e changes are, however, so slight th at for most practical purposes interception measurement a t any time in July, August, and September gives a reasonable assessment of maximum interception by N-S hedges during the season. Field data for E-W hedges are not available, but interception can be expected to increase sharply over these months (Jackson and Palmer 1972).
b. Light lnterception by Branches and Fruits.-Natural and artificial forest stands have been shown to intercept an appreciable proportion of incident radiation even when leafless (Yim et al. 1969; Federer 1971). Similar effects might be expected in orchards. Jackson (1970) reported the light under a dense and large mature apple tree to be only 67% of t ha t above the canopy, even after all leaves and fruits had shed. T h e fruit area index of the tree, i.e., the summed fruit cross sectional area per unit of ground directly under the tree, was 0.22 so the fruit area also could have intercepted an appreciable amount of light. Similarly Verheij and Verwer (1973) showed the light levels under defoliated trees to be only 60 to 70% of incident. Although in both of these cases interference from neighboring trees cannot be ruled out, geometrical considerations suggest t ha t such errors would be slight. Palmer and Jackson (1977)
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found that light interception by leafless trees of ‘Golden Delicious’/M 9 and ‘Cox’/M 27 was between 10% and 20% of available light. These were small trees with a maximum LA1 of about 1.5 and since branch framework is proportional to LAI, higher light interception by branches would be expected from larger trees. Since the branch framework is effectively a skeleton clothed with leaves, the “useless” interception by branches may, however, be much smaller in the leafy tree than winter values suggest. The extinction coefficient for light in relation to leaf area (see p. 242), as determined by Cain (1973) and by Jackson (1978), effectively takes the branches and trunk into account although such a measured coefficient can be partitioned (Yim et al. 1969). c. Light Interception over the Orchard Lifetime.-Results of long-term studies of light interception by different types of orchard systems have not been published yet. Moreover, since the relationship between orchard LA1 and light interception varies with tree form and spacing, the scanty data available on the buildup of LA1 over the years cannot be directly translated into light interception. Interception in the early years is generally low even in modern hedgerow orchards (Table 5.2). I t is much greater in “bed system” orchards planted at very high densities (‘Cox’/M 27), and presumably is even lower in the early years after planting orchards a t wider spacings. There can be no doubt that this loss of light interception represents loss of economic yield. Jackson (1978) showed that yields increased linearly as light interception was increased up to about 60% of available light. This result was noted in a spacing trial with trees of ‘Golden Delicious’/M 9a which gave no indication of any flattening-off of the yieldhight interception relationship. I t is, however, significant that the maximum levels of interception noted in the orchards of Table 5.2 are between 60% and 70%, although the values quoted by Olaniran (1974) refer to total short wave (400 to 3000 nm). The latter values almost certainly represent higher interception of P.A.R. d. Evidence of Lowered Productivity Associated with Very High lnterception Levels-Levels of interception of more than 70% of available light have been reported where the trees have been spaced closely in relation to their size, but it has proved to be difficult to combine this with continued high yield, good quality, and easy management. Jackson and Palmer (1972) reported that an orchard of 5 m high apple trees on M 4 rootstock spaced a t 5.9 m X 5.9 m and overlapping the tractor alleyway as well as each other, intercepted 81%of available light in July, August, and September. A large proportion of the fruits produced by these trees was small and green. Verheij and Verwer (1973) reported a maximum
Cultivar/Rootstock Golden Delicious/M 9a Cox/M 26, Egremont/MM 106 Cox/M 26, Worcester/M 26 Golden Delicious/M 9a Golden Delicious/M 9a Golden Delicious/M 9 Golden DelicioudM 2 Cox/MM 106 free hedge Cox/MM 106 palmette Golden Delicious/M 9 Golden Delicous/M 2 Superb/M 26, Fortune/M 26 Cox/M 27
Spacing (m) 2.7 X 0.9 4.3 X 2.4 3.7 X 2.4 2.7 X 0.9 2.7 X 0.9 3.0 X 1.0 4.25 X 3.5 4.12 X 1.83 4.12 X 3.66 3.0 X 1.0 4.25 X 3.5 3.05 X 2.44 1.5 X 0.5 Date October July August/September Seutember September September September July/October July/October September September July Seutember
(4 11' 11' 30' 55' 50' 674 554 635 6g5 70' 61' 69' 60'
Light Interce tion'
2 and 3 are essentially P.A.R. measurements, 4 involved anthracene in benzene photolysis (c. 360 to 380 nm). Total short wave 400 to 3000 nm. *Jackson (1975). Palmer and Jackson (1977). Verheij and Verwer (1973). Olaniran (1974).
5 6 9 9 14 2
Age of Orchard (years)
TABLE 5.2. MEASURED LIGHT INTERCEPTION BY HEDGEROW AND BED-SYSTEM APPLE ORCHARDS
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interception of 83% by 9-year-old hedgerows of ‘Golden Delicious’/M 2 spaced a t 3.5 m X 2.5 m, but their maximum yields did not coincide with this high light interception. Verheij and Verwer concluded, therefore, that these trees’ sharp decline in yield from their seventh to their ninth year, not shown by more widely spaced trees, indicated that a t 80% light interception inter-tree competition was excessive and light distribution was unsatisfactory. They indicated that interception of about 70% of incident light may be close to the optimum for single-row planting systems under northwestern European conditions. In a separate study Verheij (1968) found that thinning-out of very dense orchards (resembling continuous-canopy forests rather than orchards) actually increased yields and fruit quality, although it must have reduced total light interception. This seems to have resulted from obtaining better light distribution in the trees. Apparently, dense orchard conditions led to adverse effects of shade on fruiting as opposed to growth, and also had very adverse effects on fruit size and color. Work to maximize effective interception must, therefore, include defining the effects of different light intensities on the basic processes involved in fruit production as well as studies on penetration to define the type of canopy which will maximize productivity in terms of crop. 111. LIGHT PENETRATION AND DISTRIBUTION IN RELATION TO FRUIT PRODUCTION
A. Relationships Between Light and Fruit Production with Respect to Optimizing Canopy Design for Penetration and Interception 1. Light Intensity Effects on Photosynthesis.-Whereas for consideration of total interception the relevant measurement is of percentage of available irradiation over the relevant wavebands, which can be converted into absolute units from meteorological records as required, consideration of effects of intensity requires definition of the units used. On a clear day full sunlight gives an illuminance of about 10,000 lm/ftz (foot-candles), i.e., 107,600 lm/m2 (lux), and an irradiance of about 1.3 cal/cm2/minute (equivalent to 907 W/mz) of which approximately 50% is in the 400 to 700 nm waveband (P.A.R. or photosynthetically active radiation is from 380 to 720 nm). The factors controlling apple tree photosynthesis recently have been reviewed by Avery (1975a, 1977), Seeley (1978), Proctor (1978), Barden (1978), Lakso and Seeley (1978), and Ferree (1978). The structure of the apple leaf varies with the light conditions under which it has developed and which it experiences. Jackson and Beakbane (1970) measured the light intensity near leaves of ‘Cox’s Orange Pippin’ a t a range of positions within a large tree, using sensors which gave an equal response to light a t
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all angles above the horizontal, and compared this to the thickness of the leaves and the thickness of their palisade layers. Both were positively and linearly correlated with light intensity (R2 = 0.90 and R2 = 0.89, respectively). Numerous other workers have shown th a t shading reduces specific leaf weight (SLW), i.e., the weight per cm2of leaf (Avery 1975a; Barden 1974, 1975, 1977; Jackson and Palmer 1977a; Maggs 1960). Skene (1974) showed influences of shade on chloroplast structure. Gabrielson (1948) showed effects of shade on the leaf thickness of Fraxinus excelsior and concluded th at shade leaves possess a maximum energy yield considerably less than th at of sun leaves of the same species. This has been confirmed for apple by Barden (1978), who found a positive linear relationship between specific leaf weight and rate of net photosynthesis when measured under standard conditions, i.e., leaves growing in full sunlight tend to be well adapted to take advantage of this to maximize their photosynthesis. Th e converse does not appear to apply, a s Barden (1977) found shade leaves to have similar levels of photosynthesis to sun leaves a t low levels of irradiance. I t seems, however, th a t leaves even in heavily shaded positions make a positive contribution. Avery (1975a) concluded (1)th at the compensation point of apple leaves, where photosynthesis balances respiration, occurs a t 2.4 to 7 W/m2 of 400 to 700 nm irradiation (less than 2% of full sunlight), (2) th a t 80% of full photosynthesis could be attained with between 10% and 40% of full sunlight, (3) that “full sun” leaves reached their maximum photosynthesis a t about 75% of full sunlight, and (4) th a t shade leaves attained this light-saturated photosynthesis level a t from 44 to 75% of full sunlight. These figures were obtained with single leaves. Lakso and Barnes (quoted by Lakso and Seeley 1978) found th a t single leaves attained about 80% of their maximum photosynthesis rate a t around 25% of full sunlight, and Lakso and Seeley quote other data to show whole tree photosynthesis to be about 60% of the maximum a t 25% of full sunlight (Sirois and Cooper 1964). 2. Light Intensity Effects on Growth and Cropping.-As might be expected from the effects on photosynthesis, shading reduces growth but growth continues even a t quite low light levels. Priestley (1969) found t ha t when potted rootstocks were shaded so a s to reduce irradiance by 9096, the total dry-matter increment was reduced to 6 to 12% of th a t of the controls. Under these conditions the lower leaves would, of course, have received much less than 10% of full sunlight. Barden (1977) found t ha t reducing irradiance on young ‘Delicious’ apple trees by 80%, using either green Saran cloth or wooden slats, reduced their dry weight increase to about 50% of those grown in full sun. Jackson and Palmer (1977a,b) and Jackson, Palmer, Perring and Sharples (1977) shaded mature cropping trees of ‘Cox’/M 26 with plastic netting of different
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mesh sizes, and found a much greater effect on fruit bud formation and yield than on vegetative growth as shown by increment in girth2 (Table 5.3). Their shades were applied only after fruit set so the treatment was less severe than th at applied by Priestley. TABLE 5.3. EFFECTS OF SHADING IN 1970 AND 1971 ON GROWTH AND CROPPING IN 1971-COX’S ORANGE PlPPlN/M 26
Light Level’ in 1970 and 1971 Variable Girth increment 1971 (cm2)2 Fruit bud clusterdtree 1971 Fruits harvested/tree 1971 Yield/tree 1971 (kg)’ c/; of fruits> % red4
100 61.4 159 151 17.6 47
37 43.1 96 74 8.8 30
25 42.8 69 51 4.7 16
11 24.6 26 6 0.6 13
Percentage of daylight inside shades but above canopy. Jackson and Palmer (1977a). 1 Jackson and Palmer (1977b). Jackson, Palmer, Perring and Sharples (1977).
In this table the effect on fruit bud numbers shows the effect of the previous year’s shading. Shade reduces individual fruit size a s long as it has not so greatly reduced the number of fruits th a t the lack of competition compensates for low photosynthetic productivity in the neighboring leaves. Hansen (1969, 1970a) has shown th a t the greater part of the photosynthates from the leaves of any spur is utilized by the fruits on t ha t spur. Although the evidence is not firm, the results of thinning fruits within clusters as compared to removing whole clusters or removing the fruits from whole branches or parts of trees suggest th a t the products of photosynthesis are mobile within the tree when they are in ample supply, but t ha t sinks (fruits or shoots) adjacent to the sources are a t a competitive advantage. Fruits near well illuminated leaves therefore have the greatest prospect of realizing their growth potential. Thorpe (1974), from temperature measurements of apples in the sun and in the shade and from known data on the effects of temperature on biochemical processes and apple fruit growth, has concluded th a t effects of sunlight on apple fruit size could, in large part, be due to a heating effect. T h e more rapid growth of such fruits as a result of the speeding up of metabolic processes should cause them to become more efficient sinks for assimilates. This could further stimulate photosynthesis by the adjacent, well exposed leaves since Maggs (1963), Avery (1969, 1975b), and Hansen (1970b) have shown t hat “sink-strength” may be a major factor in determining the photosynthesis rate of apple. Direct experimentation has shown th at fruit red color formation, due to anthocyanin, is controlled by a high energy photoreaction, with an action maximum a t 650 nm and a subsidiary one a t 430 to 480 nm, and by a
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subsequent photoreaction with an action maximum near 655 nm (Downs et al. 1965). Using appropriate artificial light sources, Proctor and Creasy (1971) found th at a minimum of 5 W/m2 irradiation for 48 hours was needed to initiate anthocyanin synthesis in green apples. Their technique did not permit accurate measurement of the highest energy levels in their experiment, but it seems from their results th a t anthocyanin production increased linearly with light intensity up to a t least 100 W/m2. Thorpe (1974) also has suggested th at the direct heating effect of sunlight on the apple skin speeds up anthocyanin production and red color formation. Auchter et al. (1926), who shaded either complete apple trees or halves of trees with muslin so th at the light intensity under the shades was only 1/20 of normal daylight, also found th at the shaded trees or parts of trees failed to form flower buds. These experiments in which the level of irradiation was varied by shading of field trees or varying the level of artificial illumination provide unequivocal proof of effects of light which cannot be obtained by purely observational orchard studies where the observed correlations might always involve the confounding effect of other factors. They complement the observational studies surprisingly well, but in relating their results to the field it is necessary to remember which natural conditions they simulate in quantitative terms and which they do not. As is discussed later, apple leaves transmit very little P.A.R. but a considerable amount of far red and near infrared radiation. If light climate under the shaded or artificial light conditions is defined in terms of P.A.R., the observed responses should relate to those observed in the orchard in so far as direct effects of P.A.R. are concerned (e.g., on photosynthesis and growth and on fruit color, which are influenced by the same wavebands). However, there will be a divergence in those processes (morphogenetic effects and fruit bud formation) which are influenced by wavelengths above 700 nm. In general, for any given level of P.A.R. there is less longer wave radiation in the experimental situation than in the natural one. Although there are these difficulties of comparison, results of the type shown in Table 5.3 make it clear why most studies on light interception in orchards have concentrated on the optimization of light distribution for fruit bud formation and fruit quality rather than on the maximization of interception and dry matter production.
B. Light Penetration into Apple Tree Canopies 1. Transmittance and Reflectance by Apple Leaves and Canopies.Shul’gin et al. (1960), Ghosh (1973), and Palmer (1977a) have published data on apple leaf transmittance. Palmer (1977a) measured transmit-
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tance and reflectance of sun and shade leaves of ‘Cox’ and ‘Golden Delicious’ a t different dates throughout the season and both confirmed and extended the results of the earlier authors. Reflectance was consistently greater than transmittance over all visible wavelengths, both showing a peak for green light near 550 nm and rising very rapidly beyond 680 nm to give low absorptance in the infrared. Mean reflectance over 400 to 700 nm was greatest in May (10 to l l % ) , and averaged between 8% and 9% for the rest of the season. Transmittance below 500 nm was negligible. The average transmittance for the 400 to 700 nm waveband declined from about 7% (for ‘Golden Delicious’) in May to 1.5% for sun leaves and 3.5% for shade leaves a t the end of September. Looney (1968), Maggs and Alexander (19731, Proctor et al. (1975), and Palmer (1977a) have measured transmittance of the different wavelengths of light through apple tree canopies and the latter reviewed and recalculated some of the earlier results. Their data show a progressive decline in transmission from 380 to 680 nm, approximately twice as much blue light as red light penetrating the canopy relative to their intensities above it, followed by very high transmission of infrared. Proportionately up to about 5 times as much radiation between 750 nm and 1400 nm is transmitted as between 400 nm and 680 nm. Suckling et al. (1975) found that for a dwarf orchard the transmission, absorption, and reflectivity were 0.53, 0.28, and 0.19 for global radiation (including infrared) compared with 0.42, 0.51, and 0.07 for photosyntheticallyactive radiation. From comparison of leaf and canopy transmittance it is clear that the greater canopy transmittance of blue than red light is because of the high proportion of unobstructed, blue-rich skylight in the light penetrating the canopy, whereas the very high canopy transmission of infrared is because this is readily transmitted through leaves. 2. Measurement of Light Within the Canopy.-The type of light sensor used for this must be appropriate to the purpose for which the data are used. If the light interception by horizontal bands of the canopy is required (an approach corresponding to “stratified clip” measurements of LA1 in studies of the ecology and crop physiology of continuous canopy crops), then cosine-law sensors with an appropriate wavelength response are required. On the other hand, if the light values are to be related to spot measurements of photosynthesis or fruit quality, a sensor giving an equal response to light from all angles (Maggs and Alexander 1970) or a t least all angles above the horizontal (Jackson and Slater 1967; Jackson 1970) is appropriate. For studies relating to photosynthesis or to fruit color, which is influenced by light within the photosynthetically active range, sensors responding evenly to light between 400 nm and 700 nm are required. It is particularly important that they do not respond to
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infrared radiation. Some error will be introduced also if they are especially sensitive to one or the other end of the visible spectrum. Details of instruments which meet these requirements were given earlier. 3. The Extinction Coefficient of Light Penetrating Apple Canopies.T h e intensity of irradiation a t any given depth within the canopy depends on the amount of foliage between that point and the irradiated surface and the relationship between foliage area and light interception. In general, it has been found th at the attenuation of light with canopy depth follows a Beers-law relationship:
where I” = the irradiation above the canopy, I = th a t beneath it, L = the intervening leaf area index, and K = the light extinction coefficient which can be calculated from measured values of I, I”, and L (Monsi and Saeki 1953). Cain (1973) used Heinicke’s (196310) data to calculate K to average 0.56 with a range from 0.43 to 0.77; Jackson (1978) quotes 4 separate determinations of K a t East Malling Research Station ranging from 0.44 to 0.76 with a mean of 0.60; and Proctor (1978) reported K values a t Simcoe ranging from 0.33 to 0.60 to give a mean of 0.43. Cain’s calculations were based on uranyl oxalate actinometry so are specifically for blue light and, because of the high proportion of blue skylight which is found below the canopy especially on blue-sky days, may slightly overestimate the transmission of P.A.R. Le., underestimate K). Jackson’s data refer to light sensors responding fairly evenly from 400 to 640 nm, whereas Proctor’s results were for global radiation (including infrared) with a correction for reflection (private communication) so th a t the extinction coefficient for visible light would have been appreciably higher. In other crops K ranges from 0.3 to 0.6 for erect-leafed plants such as grasses to about 1 for horizontal-leafed plants such as clover and cotton (Cooper 1976).Th e relatively low value for apple is most probably not so much related to leaf angle (which is certainly not vertical, c.f. Jackson 1970), but is more likely to be due to the clustering of leaves around branches (i.e., leaf clumping) which can result in large gaps for light penetration even when LA1 is high. Since the degree of clumping will vary with age of wood (i.e., proportion of leaves borne in dense rosettes on spurs) and tree type, it is important th a t K be measured directly for any particular circumstance. For example, an orchard consisting of single-stemmed spur-type shoots densely clothed with leaves as might be afforded by the Wijcik type ‘McIntosh’ mutants should have a much lower K value than one with long internodes and feathery branches giving a n even foliage distribution with minimal leaf-to-leaf shading.
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Moreover, as Bokura (1972) has shown, and Palmer’s (1977b) results have indicated, relative penetration to the lower parts of a tree is influenced by the proportion of direct to diffuse radiation and solar altitude, so always must be measured in appropriate conditions. C. Patterns of Light Penetration into Trees and Their Effects on Growth and Cropping Because of the effects of tree form on the pattern of within-tree light distribution, it is useful to consider separately results on “round-headed” trees and hedgerow trees of triangular or rectangular cross section. 1. Light Relations in Round-Headed Trees.-Studies on light distribution in bush trees with a spherical or hemispherical tree head form generally have shown that only a limited outer zone of such trees receives enough light to produce fruits of good quality. Heinicke (196313, 1964, 1966) found that the average light intensity in a very large ‘Red Delicious’ apple tree fell to 42% of full sunlight a t a depth of about 2 m from the top of the tree, that fruits growing under this level of shade were appreciably smaller than those growing a t the top of the tree, and that they usually did not develop enough color to be placed in the top quality grade. In general, he found fruit skin color of both ‘Red Delicious’ and ‘McIntosh’ to be related directly to exposure. T h e best color was associated with exposure to more than 70% of full sunlight, adequate color with from 40 to 7076, and inadequate color with less than 40%. Fruits receiving less than 50% of full sunlight were small, and the soluble solids content of fruits was higher where they were well exposed to light. T h e photochemical technique used, with its excess sensitivity to blue light, could have led to an overemphasis on the importance of skylight in this study, but Looney (1968) found much the same overall pattern of light penetration in these trees when he measured it using a spectroradiometer. Jackson (1967, 1970) found a more rapid decline when he measured changes in 400 to 640 nm radiation with depth of canopy; light intensity in the center of a 4 m high ‘Cox’ tree fell from 95 to 34% of full sunlight within 1 m. This difference in depth of well illuminated canopy mainly reflected differences in density of leaf arrangement since the decrease in relative light intensity per unit LA1 was similar in England and Canada. Fruit color diminished with depth from the outside of the canopy; fruits under the shade of an LA1 of more than 0.75 had less than 25% of their surface red colored. In separate observations on ‘Laxton’s Superb’ he found that the main cropping zone of the tree received a minimum of 35% of full daylight, while the more shaded areas produced relatively few
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fruits, which were small and green. Anthocyanin content in the most exposed part of the fruit skin increased with light intensity up to a t least 50‘h of full sunlight. Jacyna (1978) observed similar patterns in ‘McIntosh’ trees with round crowns in which light intensity varied primarily with distance from the upper surface. The best colored apples were found in parts of the crown receiving 60 to 70% of full sunlight. There was a high positive correlation between the amount of direct sunlight received and both the intensity and extent of red coloration of the individual fruit surfaces. In contrast to Heinicke, he found the light penetration to be better in the southern and western parts of the crown than in the northern and eastern, although he used the same uranyl-oxalate technique of light measurement. H e attributed the greater irradiation of the eastern side to stronger radiation in the morning under Polish climatic conditions. Lakso and Musselman (1976) studied diffuse light penetration into apple trees. Much experimental data and theoretical analysis, reviewed by Saeki (1975), show that the fraction of diffuse sky radiation transmitted by a forest or a crop is higher than that of direct solar radiation, and that increasing the percentage of diffuse skylight in total sunlight will increase canopy photosynthesis. Lakso and Musselman found that interior canopy readings of P.A.R., measured to avoid sunflecks, were greater on a partially cloudy day than either on a dull day or a clear day, in agreement with expectation. However, if sunflecks had occupied 10% of the horizontal surface area a t the appropriate level in the interior of the ‘Golden Delicious’ tree (or 5% in the case of the ‘Wayne’ tree), total P.A.R. in the tree interior would have been higher on the bright sunny day. No estimate of sunfleck pattern is given in the paper so, unfortunately for fruit growing in cloudy areas such as New York state and England, the argument that a higher proportion of diffuse light can more than compensate for lower total radiation remains to be proved. In considering canopy productivity in relation to light penetration, the fact that fruit bud formation and fruit color development appear to be more sensitive to light intensity than does photosynthesis also must be considered. Lakso and Musselman’s data show the maximum P.A.R. (minus sunflecks) in the interior shaded part of the tree to be only about 15% of full sunlight for ‘Golden Delicious’ and 7% for ‘Wayne’. Unless sunflecks also made a major contribution, which would be a t its greatest under sunny conditions, this tree zone would not be capable of contributing to economic fruit production although capable of growth. In other work Lakso (in press) studied the distribution of light within large ‘McIntosh’ trees using both a Lambda meter to measure P.A.R. and fisheye photography to measure the percentage of sky visible from different points in the canopy. H e found the two measurements to be closely correlated.
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For continued flowering, the spurs had to be exposed to a t least 25 to 30% of above-canopy P.A.R., and optimal fruit color development did not take place where the “fisheye” reading was less than “30% sky,” corresponding to about 40% of above-canopy P.A.R. Mika and Antoszewski (1972) measured illuminance and net photosynthesis in the outer and inner zones of round-headed trees of ‘Jonathan’ and ‘Bancroft’ on M 7 rootstock using a luxmeter of unspecified directional and wavelength response. These trees, with a maximum height of 2.5 m and spread of 3 m, were smaller than those studied by Heinicke, Jackson, Lakso, and Lakso and Musselman. Even so the inner zone of the trees (the part more than 1 m from the upper surface and the outer sides of the trees) received only 9 to 16 klx a t noon, while the outer zone received 70 to 90 klx. The mean rate of net photosynthesis was about three times higher in the outer zone than in the inner zone. The daily course of net photosynthesis reached its peak earlier than the daily course of illuminance. Mika and Antoszewski suggested that this was because the plants suffered from water stress later in the day, which lowered photosynthetic rates because of stomata1 closure. They also studied younger ‘Bancroft’ trees pruned to give either “compact” or “loose” crowns, and found both illuminance and net photosynthesis to be much higher in the inner zone of the loose-crowned than the compactcrowned trees. This indicates the importance of pruning to ensure good light penetration and also shows that defining “inner” and “outer” zones without quantifying depth of canopy in terms of LA1 can be very misleading. A number of authors (Heinicke 1964; Jackson 1970; Markov 1973) have shown that a greater proportion of the volume of a round-headed bush tree on a dwarfing rootstock is well illuminated than is the case with the larger tree on a vigorous rootstock. This has been correlated with differences in fruit size, color, and photosynthesis by the above authors and also with production efficiency (Forshey and McKee 1970). While the smaller size and lower LA1 of trees on dwarfing rootstocks undoubtedly lead to better light penetration and direct effects of this, recent work a t East Malling Research Station (Blasco 1976) has shown that there are direct rootstock effects on fruit size, with M 9 producing larger fruits even after the effects of light have been adjusted for. 2. Light Relations in Hedgerow and Center-Leader Trees.-These trees differ from the round-headed forms in that their most important surfaces for receiving solar radiation are their vertical or sloping sides rather than horizontal, umbrella, or cup-shaped upper surfaces, except in very special cases. Unlike with the horizontal upper surface, the incident radiation a t any point on this sloping or vertical surface is not 100% of
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full daylight. Instead, as shown in Fig. 5.2 (p. 223), the diffuse light at any point on the surface will be reduced since the segment of sky which can be “seen” from that point is less in area and brightness than the whole sky. The total incident direct light is also less because of prior interception by the other side of the hedge, or by an adjoining hedgerow, a t some times of the day. The results obtained in field studies on hedgerow trees must be considered in the context (1) of height-spacing relationships of the type considered in “solid model” computer studies (see p. 220) and (2) of whether the trees actually consisted simply of vertical cropping surfaces, in which case considerations of surface irradiation only are dominant, or had a large interior cropping volume also. Trees of the former type are exemplified by Italian palmettes, which can be up to 4 m high and only 1 m thick and, especially when severely and regularly hedged to retain these dimensions, appear so dense as to be virtually non-transmitting. Actual dimensions of hedgerow orchards used for detailed light studies are given in Table 5.4. From these dimensions and the computer studies referred to earlier it would be expected that the hedgerow trees studied by Jackson (1970) and those by Verheij and Verwer (particularly on M 2) would be shaded appreciably a t the base even on the outside. In contrast, those studied by Mika and Antoszewski and by Cain should have been less so, especially as those of the latter sloped back a t an angle of 20” to be only 1.25 m wide a t the top. Mika and Antoszewski (1974) used trees combining a height to clearalley width ratio of only 1.36 for ‘Jonathan’ and 1.59 for ‘Starking’ with a thickness of only 1.5 m and a reasonably high LA1 (1.8 for ‘Jonathan’, 2.2 for ‘Starking’). Their results seem much as expected. For the ‘Jonathan’ trees the illumination of the lower part of these trees was similar to illumination of the upper part only when this illumination was a t its peak and, presumably, the whole surface was in full sun (8 to 8:30 AM on the east side of the hedges, 2 to 2:30 PM on the west side). For the taller ‘Starking’ trees the differences between illumination of the upper and lower parts were greater. The diurnal pattern of relative illuminance of the east and the west sides remained, but illumination on the west side of the hedgerow was a t its maximum a t 12 to 12:30 PM. No details of the angular response of the sensor nor of the way in which it was used are given, i.e., to measure irradiation on a horizontal surface, in the plane of the hedgerow, or as total “spherical” irradiation. This could influence the numerical values obtained but hardly enough to change the overall patterns shown. Average photosynthesis showed a similar diurnal pattern, peaking a t 8 AM on the east side and 1 2 to 12:30 PM on the west side, indicating a strong dependence on direct light. The effects of hedge
Authork) Cain 1971,1973 Cain 1971,1973 Jackson 1970 Verheij and Verwer 1973 Verheij and Verwer 1973 Mika and Antoszewski 1974 Mika and Antoszewski 1974
Key to reference numbers: 1.McIntosh/M 9/M 7. 2. Macoun/M 2, MacounlMulus sikkimensis. 3. Laxton's Superb/M 26. 4. Golden Delicious/M 9. 5. Golden Delicious/M 2. 6. Jonathan/MM 106. 7. Starking Delicious/MM 106.
Experiment Reference Number 1 2 3 4 5 6 7
Tree Height (m) 3.00 3.66 2.50 2.75 3.25 3.00 3.50
Thickness a t Base (m) 3.66 3.66 2.00 1.75 2.35 1.50 1.50
Width of Clear Alley (m) 2.44 2.44 1.05 1.25 1.15 2.20 2.20
Within-Row Spacing (m) 3.05 3.05 2.45 1.oo 1.25 3.00 3.00
TABLE 5.4. DIMENSIONS OF HEDGEROW ORCHARDS USED IN SOME RECENT STUDIES ON LIGHT INTERCEPTION
U
z
>
T:X
0
4
m
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height on rate of photosynthesis were much less marked than those on light, which is in keeping with the relatively low level a t which photosynthesis is light-saturated. Mika and Antoszewski concluded th a t light distribution and rates of photosynthesis in these hedgerow trees were much more uniform than in the bush apple trees which they had studied earlier (Mika and Antoszewski 1972). Th e very early timing of peak irradiation and photosynthesis on the west side may reflect the climatic pattern of diurnal variation of light intensity in Poland referred to by Jacyna (1978). I t may, however, indicate th a t internal controls influence the rate of photosynthesis since the data of Landsberg et al. (1975) could be interpreted as showing higher actual photosynthesis rates in the morning than those expected from photon flux density. Chekrygin (1976) noted better light penetration and fruit color in trees of ‘Jonathan’ and ‘Snow Calville’ planted as palmettes (5.5 m X 5.5 m) than when grown as large round-crown trees a t 11 m X 5.5 m. T he closeness of the hedgerows studied by Jackson (1970) resulted in a very pronounced vertical profile in light intensity. Even in the center of the alley, where there was no foliage, the light intensity (measured with hemispherical sensors) was only 38% of full daylight a t 0.5 m above the ground whereas it was 64% of full daylight a t a height of 1.5 m. At the edge of the canopy, 1 m from the row center, light intensity a t 1 m and 1.5 m above the ground was the same as a t the same height in the center of the alley, but dropped to 23.5% of full daylight a t 0.5 m high. In the center of the hedgerow, light intensities a t below 1 m in height averaged less than 15% of full daylight. Verheij and Verwer’s (1973) trees showed a similar but slightly less extreme pattern; light intensity decreased sharply towards the lower part of the trees a s well a s with increasing distance from the outer surface. As a result of the overall orchard geometry, surface irradiation in the lower 1.5 m was consistently poorer on their trees on M 2 than on those on M 9. T h e trees on M 2 also had a greater depth and thickness of canopy. As a result of this greater withintree a s well as between-tree shading, they had a greater volume of inadequately illuminated canopy than those on M 9. In general fruit size and color followed the pattern of light distribution, although there were discrepancies attributed to differences in pruning. Rud’ et al. (1977) also mapped the light regime and flowering and fruiting pattern in palmette trees.
D. The Interaction Between Light Interception and Water Use T he possible failure of well-irradiated leaves to reach their photosynthetic potential because of stomata1 closure has been touched on briefly, but its detailed consideration is outside the scope of this review. T h e
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effects of radiant energy which is not intercepted by the trees are, however, an important but often neglected part of the study of orchard light interception, as is the interaction between total tree light interception and water requirement. In the older-style orchard with large trees virtually roofing over the alleyways and intercepting about 80% of available light a t maturity, the energy available for transpiration by grass was obviously low. T h e sheltered conditions tended to reduce windspeed (Preston 1975), which also would influence water use by grass. Th e move towards hedgerow orchards on dwarfing rootstocks, intercepting only 55 to 60% of available radiation even a t maturity, makes more energy available for evapotranspiration from the grassed alleys as well as improving ventilation. Under these circumstances water use by grass can be considerable and this gives scope for appreciable water conservation by appropriate soil management techniques. For example, Atkinson (1976) showed th a t total water loss from the upper 750 mm of soil, by trees and ground cover, in a dwarf hedgerow orchard was 0.43 m3/m2where grass grew right up to the tree trunks, 0.36 m:1/m2 where there was a herbicide strip/grassed alley system, and only 0.23 rn:j/m2 where overall herbicide was used to maintain a grass-and-weed-free orchard floor. Yields were greatest in the overall herbicided and least in the fully grassed plot mainly a s a consequence of this competition for water. Th e potential water use by the grass is a function of the energy transmitted to it, i.e., of Tf T,, so that, for example, a very dense, summer pruned hedgerow system with a large value for Tf might permit much more severe competition by grass for water than a system with a lower LA1 distributed more evenly over the orchard so t hat total transmission was lower. T he water use by the trees themselves is also a function of their energy interception. In an experiment in which overall herbicide treatment maintained a weed-free soil surface, Atkinson (1978) found th a t total water use was directly dependent on density of planting. This result was obtained in a spacing trial using dwarfing rootstocks planted in square arrangements so th at ground cover was directly proportional to tree population.
+
E. Management Practices Which Influence Light Interception a n d Distribution Ligh interception and distribution can be controlled by the choice of tree size and arrangement, by pruning to obtain the desired tree shape and structure, and by using artificial reflectors. 1. Choice of Rootstock.-The vigor control achieved by the use of dwarfing rootstocks makes it much easier to maintain a shallow canopy
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or thin hedgerow which can be adequately illuminated throughout its volume. This is clearly shown by the results of Heinicke (19641, Markov (1973), and Verheij and Verwer (1973). 2. Pruning.-Summer pruning, by removing the growing shoots, increases light intensity in the cropping zone and red coloration of the fruits, while also stimulating fruit bud formation. Its effects were reviewed by Utermark (1976). Normal winter pruning of large trees is designed to ensure adequate light penetration, although this is seldom quantified. Mika and Antoszewski (1972) showed a large effect of pruning, to ensure a “loose” crown, on light penetration. Rud’ et al. (1976) showed that within-tree illumination increased with increased distance between framework branches, while Kudryavets and Trusov (1975) showed that moderate thinning and opening up the crowns of trees planted a t 8 m X 3 m and 8 m X 2 m increased light penetration so that photosynthesis within the crown was increased by 4.5 times compared with the controls. Lakso et al. (1978) found that removing the central leader of eight-year-old semi-standard ‘McIntosh’ apple trees, which made the canopy much more open (although from their photographs it did not appear to affect tree height or spread), increased light intensity in the fruiting zone without reducing total interception and increased fruit size and color. The effect of mechanical trimming on light climate in the fruiting zone depends primarily on the amount and type of regrowth which it stimulates. Cain (1971) found that when he used a cutter-bar for mechanical hedging and topping, light intensity was reduced by 50% within 0.6 m of the top because of the vigorous growth of annual shoots. With ‘McIntosh’, ‘Greening’, and ‘Macoun’, 30% of full sunlight was found to be needed for some flower formation on spurs and 60% to maximize this, so flowering of the cutter-bar-pruned trees was greatly reduced. Where a slotting saw was used instead of a cutter-bar, light intensity in the inner part of the trees was much higher and fruit bud formation correspondingly improved-40% of the spurs bore fruits whereas only 16% of those in the cutter-bar-pruned trees did. Experience in Holland and Denmark confirms the effect of mechanical hedging in increasing shading. In France Hevin’s (1977) results suggest that mechanical pruning, while leading to excess shoot production if practiced a t the top of trees, increased yields if applied to the sides. In Italy (Sansavini 1978) the main problem with mechanized pruning is that it gives excessive numbers of well-illuminated one-year shoots which, in the cultivars used, then set too many fruits and lead to greater costs of thinning. Possibly the effects of both absolute light levels and the ability to crop on one-year-old wood are involved.
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Perhaps the greatest effect of pruning on light interception and distribution in orchards in recent years followed the realization that a relatively shallow depth (c 1%m) of fruiting canopy was capable of intercepting most of the available light, and t h a t only the upper and outer parts of conventional round-headed large trees received enough light to produce good quality fruits and fruit buds. Jackson and Blanco (1973, 1974) reported that conventional, large (4 m tall) round-headed trees had been lowered successfully over a period of 2 years, without any loss of crop, to a height where all pruning could be done without the use of ladders, i.e., to a permanent framework reaching to little over 2 m high. This treatment, frequently with the use of NAA paint on the pruning cuts to prevent vigorous re-growth and shading, is now very widely used in England. Turnbull (1978) observed that 75% of the orchards suitable for re-structuring in this way have been so treated. Fruit size and color have generally improved. Groza (1972) compared several methods of modifying the crowns of mature apple trees. The best results were obtained by removing the leader and inner main branches and by shortening the laterals on the remaining scaffold branches to 25 to 30 cm. Light intensity inside the tree was increased by two or three times and the yields were doubled. Annual shoot growth also was increased. Terekhova (1976) reduced the height of the crowns of three apple cultivars and measured effects on crown light regime. The best results were obtained by lowering ‘Renet Simirenko’, ‘Snow Calville’, and ‘Jonathan’ crowns to 4.0, 3.5, and 3.0 m, respectively. Khamukov (1977) reduced tree height by 20 to 30% and found that this increased leaf surface area. Il’inskii (1978) found that shortening palmette apple trees from 4 to 3 m increased fruit size without diminishing yields. Tolstoguzova (1975), after noting that poor light in the center of crowns gave rise to biennial bearing, found reduction in crown width to 2 m in palmettes increased yield per unit crown area. These positive results from lowering trees and reducing crown volume probably stem from maintaining (or dmost maintaining) light interception while reducing respiratory load. Alternatively, productivity may be raised as a result of better exposure of the spur leaves, which “feed” the fruits, and of increased irradiance of the fruits themselves increasing their temperatures, sink strength, and growth rates. These latter mechanisms may explain the high yields of summer-pruned trees and other dwarf-tree systems in which annual shoot growth is removed or checked. In spite of the fact t h a t orchards of very dwarfed trees do not generally intercept as much light as large-tree orchards, their yields can be very high. McKenzie and Rae (1978) reported maximum yields in New Zealand to be from summer pruned dwarf-pyramid trees (180 M T / h a of ‘Golden Delicious’), while Westwood (1970) recorded 128 M T / h a in Ore-
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gon from hard-pruned trees of ‘Golden Delicious’/M 9, and Preston (1978) obtained the equivalent of 121 M T / h a from trees of Grieve/M 27 a t East Malling Research Station which are so pruned that virtually all the fruits are well exposed to light. 3. Reflection of Light from the Orchard Floor.-Bokura (1972) found that placing an aluminum sheet under the canopy of a large, fairly flat-topped tree increased the level of radiation within the canopy. Moreshet et al. (1975) found t h a t covering the ground between hedgerows in an orchard of tall, dense apple trees with reflective aluminum-coated plastic significantly increased the average weight, diameter, color, and sugar content of fruits harvested from the lower half of the canopy. T h e total weight of fruit harvested per tree was not affected until the following season when a large increase was recorded as a result of improved flowering and fruit set. This again emphasizes the importance of these aspects, rather than only direct photosynthetic effects, in fruit tree response to light. For maximum gain the reflectors should be placed over the entire orchard surface, including the alley, since the greater part of transmitted light falls there. T h e gain from any specific under-tree or within-alley arrangement obviously will depend on overall canopy geometry and density and may be very low in dense orchards.
4.Row Orientation and Between- and Within-Row Spacing.-There is relatively little experimental evidence on the effects of row orientation, probably because of the management problems involved in replicating comparisons of trials with tractor alleyways running in different directions. Theoretical studies discussed earlier suggest t h a t N-S hedgerows are to be preferred, especially because of the poor illumination; fruit quality observations on the northern side of E-W rows also bear this out. With low open-pruned trees these differences can be expected to be very slight and to increase with hedge height/thickness ratio and density. T h e effect of orientation on total interception, hence potential yield, varies with orchard geometry, length of growing season, and latitude. Christensen (1979) found a significant reduction in apple yields in Denmark when hedgerows of dwarf trees were oriented E-W instead of N-S. Devyatov (1976, 1977) and Devyatov and Gorny (19781, who worked with taller trees a t a similar latitude (Minsk), reported better light regimes accompanied by higher photosynthesis and yield in E-W rather than in N-S palmettes. Lombard and Westwood (1977), working a t 42”N, found appreciably higher pear yields where tall “tree-walls” were oriented N-Srather than E-W. They found very low light intensities on the northern side of the E-W rows and also more radiation reaching the middle of the alleys with E-W rather than N-S orientation (i.e., less total light being intercepted by the trees).
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Rosati (1978) commented that early plantings of palmettes in Italy often were planted too closely without regard for their sunlight requirement. The result was excess shading in the lower part of the canopy so that the orchards ceased to have the desired cropping characteristics. Further experience (Rosati 1978) led to the choice of tree heights ranging from 3.5 to 4.5 m, thickness from 1 to 2 m, and between-row spacings of 3.5 to 5 m with, in all cases, a clear alleyway of about 2.5 m. Northsouth row orientation is preferred because it gives the best light exposure on both sides of the hedgerow. Sansavini (1978) quotes rather lower mechanically pruned trees (topped a t 3 to 3.5 m) with a minimum clear alleyway of 1.5 to 2 m, again stressing the importance of light penetration as a determining factor. Rud’ et al. (1977) studied palmette trees of ‘Jonathan’/M 4 grown in Moldavia (USSR) a t 4 m X 5 m, 4 m X 4 m, or 4 m X 3 m, and trees on M 9 grown a t 4 m X 3 m, 4 m X 2.5 m, and 4 m X 2 m in N-S rows. They concluded that the optimum light regime per unit orchard area was obtained with trees 3 to 3.5 m tall spaced a t 4 m X 3 m with a 2 m wide crown base. In northwestern Europe high density planting with slender-spindle bush orchards on M 9 rootstock is widely practiced because of the speed with which they attain maximum yields and the low cost of picking and pruning the dwarf trees (Wertheim 1978). Tree height is usually restricted to 2 to 2.5 m, reaching 3 m as an absolute maximum to permit operations to be carried out without expensive ladder work. From theoretical studies it is clear that even if such trees were so dense as to approximate “solid models,” they would not shade each other unduly if the rows were separated by clear alleyways of only 1 to 1.5 m. Wider spacing, to allow large tractors and conventional orchard machinery access, reduces light interception to below the optimal level. In a spacing trial with hedgerows of ‘Golden Delicious’/M 9a spaced a t 2.9 m, 3.35 m, 3.8 m, and 4.25 m from row center to row center, Palmer and Jackson (1978) reported that in only 1 of 8 cropping years had there been a depression in yield per unit length of row as a result of the closest between-row spacing. This indicates that the extra space given a t the other distances had contributed nothing to cropping. There is, however, ample evidence that close within-row spacing can lead to excess shade, depressing yield per tree as well as fruit size and color (Palmer and Jackson 1975; Parry 1978). This problem is made worse by the tendency for continued vigorous growth of vegetative shoots a t the top of the hedge under close planted conditions, and yield per hectare can be reduced a t very high densities (Verheij 1972). These effects of between- and within-row spacing are to be expected on the general theoretical grounds that the more evenly a given LA1 is
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distributed the greater will be its light interception and potential productivity. A consequence is that light interception and yield from any given number of trees are maximized by narrowing the distance between rows and increasing that within rows to approach a square-planted arrangement. Jackson and Palmer (1973) showed that 3-year-old ‘Golden Delicious’/M 9a planted a t 2.9 m X 2.7 m (1277 trees/ha) intercepted 18% more light than did slightly more trees (1307/ha) planted a t 4.24 m X 1.8 m. T h e trees also yielded 17% more, and the effect has increased rather than diminished over the years (Palmer 1976). With such small trees even 2.9 m between row centers is, however, too wide for high light interception especially in the early years after planting. Since it would be impossible to manage closer spaced rows with conventional machinery, the necessary move towards still more rapid and efficient attainment of high light interception is being attempted in a number of novel orchard designs described in the next section.
IV. CURRENT CONCEPTS IN CANOPY DESIGN TO OPTIMIZE LIGHT INTERCEPTION AND DISTRIBUTION A. General Objectives
T h e general objective of the different experimental high density orchards is to minimize the number of alleyways and cover as much of the ground surface as is possible with a cropping canopy of not more than 1.5 m to 2 m depth. This, as was shown earlier, is all that is capable of producing good quality fruits given conventional leaf area densities.
B. Multi-Row and Bed Systems Ferguson (1960) used solid conical models and a photographic technique to compare the potential light interception by equal numbers of trees arranged in single row systems, with very close spacing within the rows, and a system with staggered double rows separated by alleyways. In the latter system, which also has been referred to as a zig-zag arrangement (Parry 1978) or as a triangular row system by its initiators, each pair of rows forms a row of triangles in plan so that the net effect is to distribute the trees more evenly over the orchard surface. This was calculated to give a total interception gain of only about 1.3% over the season. It should be noted, however, that Ferguson assumed the single row trees to be 4.5 m high and 3 m wide a t the base when spaced a t 4.5 m X 3 m, i.e., a height to minimum alley width ratio of 3, and the average diffuse-light interception by these single rows calculated to be 85% of that available.
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Under these circumstances the potential advantage of more even arrangement of the trees is much less than would be the case with smaller trees intercepting less of the “alleyway” light. Verheij and de Vries (1966) suggested that optimal levels of light interception would be higher with “bed system” orchards than with single-row orchards. Attempts to attain such higher light interception, hence yield, by planting 2-, 3-, 4-, 5-, or 6-row beds separated by tractor alleyways but with only walking paths within the beds have been rather disappointing. Frequently, light penetration into the center of the bed and, consequently, fruit quality have become poor (Wertheim 1978). An alternative system not yet adequately evaluated is the “full-field’’ method of growing trees in rows which are only 1.5 to 2 m apart and are managed by the use of over-row (straddle) tractors. A difficulty with both multi-row and full-field systems on M 9 rootstock (or any which are more vigorous) is the shading effect of the annual shoot growth which, in such a near-continuous-canopy system, forms a vegetative shading layer above the fruit bud- and fruit-producing zone. Jackson (1978) calculated that an orchard of otherwise optimal density with 4773 evenly spaced trees/ha of ‘Golden Delicious’/M 9 would have an LA1 of 0.43 above the uppermost fruits. This would intercept about 18% of available light before it reached the cropping zone. Techniques to remove or prevent the growth of unwanted shoots a t the top of the canopy are needed to ensure that the high light interception which can be achieved by full-field systems is accompanied by satisfactory light distribution. Summer pruning is a t present practiced in such systems; chemical means of growth control would be advantageous. Use of genetic material especially adapted to “full-field’’ systems may become important in the future. Tip-bearing and spur-type cultivars have obvious advantages in that they naturally present their fruits in the upper unshaded parts of such a canopy. Alternatively, very dwarfing rootstocks can be used to minimize unwanted shoot growth. T h e bedsystem orchard on M 27 rootstock (Palmer and Jackson 1977; Preston 1978) is the first example of such an orchard managed to give a shallow canopy no more than 1.5 m high. In this the tractor alleyways are separated by 14 rows of very dwarf, flat-topped trees, the rows being only 1.5 m apart to enable pickers to walk through them and load fruits on to an overbed conveyor. This system has achieved some objectives in that it reaches its ceiling light interception in the second year after planting, has the majority of its fruits well exposed to the light so giving good color, has consistently given more than 50 M T / h a of ‘Golden Delicious’ apples from the second year onward, and has not presented any problems of shoot growth control. The ceiling light interception of 60% is suboptimal and suggests that a deeper canopy is needed. Even so, over a
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15-year life its present total interception would compare favorably with most other systems.
C. Meadow Orchards The most revolutionary approach is that of the meadow orchard (Hudson 1970,1971;Luckwill 1978) with a tree density of 70,00O/ha in which the “trees” are mown off every second year and the fruits then combed off mechanically. Yields of ‘Golden Delicious’ apples have approached 100 MT/ha in the cropping year. The light values a t the base of the canopy in the first year are well within the accepted limit for fruit bud formation (Bennett and Turner 1978), but in the cropping year there is, with some cultivars, a tendency for fruit size and fruit color to be reduced in the center of the plots due to lower light conditions (Child and Atkins 1978; Bennett and Turner 1978). Reduced light penetration with some cultivars was attributed to the production of long “feather” shoots. This interference of vegetative growth with light penetrating to the cropping zone illustrates the general problem in very high density plantings which was discussed by Jackson (1978). A more serious problem of energy use efficiency in the meadow orchard is that it is a biennial cropping system, so that even if performing as a continuous canopy its effective light interception per cropping year could not exceed 50%. If it could be adapted to be an annual system, as with peaches in Israel (Erez 1978), then its energy interception and distribution efficiency should be very high. D. Horizontal and V Trellis Systems
A high degree of ground cover combined with a shallow canopy may be attained also by growing relatively vigorous trees in hedgerows with their branches trained in the form of an open V or T . The horizontal or V arms of the trellis then may be mechanically pruned to keep them to a prescribed depth. This concept has been developed in the Tatura trellis (Chalmers and Van Den Ende 1976) and in the Lincoln canopy (McKenzie et al. 1978). If these can be successfully harvested mechanically with under-canopy catchers, orchards with wide shallow canopies and very narrow alleyways are clearly probable, thus minimizing Tf and ensuring high light interception with uniform irradiation of a large cropping surface. Peach yields of 65 MT/ha in the third season after planting have been reported from Tatura trellis systems (McKenzie et al. 1978). V. CONCLUSIONS The yields quoted in the last section indicate the potential productivity of shallow-canopy fruit trees intercepting a high proportion of the avail-
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able radiation. In the past, many years after planting were required to achieve such levels of production. Now plant breeders, pomologists, growth regulator physiologists, and engineers together are working toward early achievement and easy maintenance of canopies designed to optimize light interception and distribution. A major weakness in the work to date has been inadequate methodology. Many of the studies have described canopies simply in terms of number of trees per hectare and general type of pruning; a number have defined leaf area distribution in space; and very few have measured the underlying limiting factors of light interception and distribution. Many more studies using appropriate instrumentation and computer models are needed to put this branch of horticultural science on sound scientific footing. Until this is done the results of the many very vigorous research programs on canopy management, currently one of the most exciting and promising areas in fruit research, will be much less applied than they could be.
VI. LITERATURE CITED ABRAMOV, N.A. and V.N. KUTNETZOV. 1973. Coefficients for calculating the leaf area in certain apricot and peach cultivars by N.K.Polyakov’s method. Byulleten Gosudarstvennogo Nikitskogo Botanicheskogo Sada 1(20):35-37. ANALYTIS, S., J. KRANZ, and A. STUMPF. 1971. A method of calculating leaf surface area. Angewandte Botanik 45:lll-114. ANDERSON, M.C. 1971. Radiation and crop structure. p. 412-466. I n Z. Sestak, J. Catsky, and P.G. Jarvis (eds.) Plant photosynthetic production, manual of methods. W. Junk N.V., The Hague. ATKINSON, D. 1976. British Crop Protection Conference-Weeds (13th British Weed Control Conference) Proceedings. Nov. 15-18, 1976, Brighton, England. British Crop Protection Council, Ombersley, Droitwich, U.K. 3:873-884. ATKINSON, D. 1978. Use of soil resources in high density planting systems. Acta Hort. 65:79-89. AUCHTER, E.C., A.L. SCHRADER, F.S. LAGASSE, and W.W. ALDRICH. 1926. The effect of shade on the growth, fruit bud formation and chemical composition of apple trees. Proc. Amer. Soc. Hort. Sci. 23:368-382. AVERY, D.J. 1969. Comparisons of fruiting and deblossomed maiden apple trees and of non-fruiting trees on a dwarfing and an invigorating rootstock. Ne w Phytol. 68:323-336. AVERY, D.J. 1975a. Effects of climatic factors on the photosynthetic efficiency of apple leaves. p. 25-31. I n H.C. Pereira (ed.) Climate and the orchard. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, U.K. AVERY, D.J. 1975b. Effects of fruits on photosynthetic efficiency. p. 110-112. I n H.C. Pereira (ed.) Climate and the orchard. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, U.K.
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AVERY, D.J. 1977. Maximum photosynthetic rate, a case study in apple. New Phytol. 7855-63. BARDEN, J.A. 1974. Net photosynthesis, dark respiration, specific leaf weight, and growth of young apple trees as influenced by light regime. J. Amer. Soc. Hort. Sci. 99:547-551. BARDEN, J.A. 1975. Specific leaf weight of apple as influenced by several factors. HortScience 10:331. (Abstr.) BARDEN, J.A. 1977. Apple tree growth, net photosynthesis, dark respiration, and specific leaf weight as affected by continuous and intermittent shade. J. Amer. SOC.Hort. Sci. 102:391-394. BARDEN, J.A. 1978. Apple leaves, their morphology and photosynthetic potential. HortScience 13(6):644-646. BARLOW, H.W.B. 1969. The relation of leaf area to stem cross section. Rpt. East Malling Res. Sta. for 1968, p. 117-119. BARLOW, H.W.B. 1970. Some aspects of morphogenesis in fruit trees. p. 2543. In L.C. Luckwill and C.V. Cutting (eds.) Physiology of tree crops. Academic Press, London. BEGG, J.E. and R.B. CUNNINGHAM. 1974. Penetration of radiation into a Eucalypt woodland. J. Austral. Inst. Agr. Sci. 40(2):160-164. BENNETT, J. and R. TURNER. 1978. Rpt. Long Ashton Res. Sta. for 1977, p. 29. BLASCO, A.B. 1976. Rootstock effects on growth and cropping of apples with special reference to fruit quality. Ph.D. Thesis, University of London. BOKURA, T. 1972. Observations on light transmission through apple trees. Bulletin of the Faculty of Agriculture, Hirosaki University 18:129-133. CAIN, J.C. 1969. A portable economical instrument for measuring light and temperature intensity-time integrals. HortScience 4:123-125. CAIN, J.C. 1971. Effects of mechanical pruning of apple hedgerows with a slotting saw on light penetration and fruiting. J. Amer. SOC.Hort. Sci. 96: 664-667. CAIN, J.C. 1972. Hedgerow orchard design for most efficient interception of solar radiation. Effects of tree size, shape, spacing and row direction. Search Agr. 2:l-14. CAIN, J.C. 1973. Foliage canopy development of McIntosh apple hedgerows in relation to mechanical pruning, the interception of solar radiation and fruiting. J. Amer. SOC.Hort. Sci. 98:357-360. CHALMERS, D.J. and B. VAN DEN ENDE. 1976. The Tatura trellis: a new design in high yielding orchards. J. Agr., Victoria 73:473-475. CHARLES-EDWARDS, D.A. and M.R. THORPE. 1976. Interception of diffuse and direct-beam radiation by a hedgerow apple orchard. Ann. Bot. 40: 603-613. CHEKRYGIN, V.V. 1976. Light regime and fruit quality in differently trained apple trees. Trudy Kuban. S.-Kh. Instituta 131(159):101-107.
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CHILD, R.D. and H. ATKINS. 1978. Crops from the 1972/73 meadow orchard. Rpt. Long Ashton Res. Sta. for 1977, p. 28-29. CHRISTENSEN, J.V. 1979. Effects of density, rectangularity and row orientation on apple trees, measured in a multivariated experimental design. Scien. Hort. 10:155-165. COOPER, J.P. 1964. Climatic variation in forage grasses. J. Appl. Ecol. 1: 45-62. COOPER, J.P. 1976. Photosynthetic efficiency of the whole plant. p. 107126. I n A.N. Duckham, J.G.W. Jones, and E.H. Roberts (eds.) Food production and consumption: the efficiency of human food chains and nutrient cycles. North-Holland Publishing Co., Amsterdam. COX, E.F. 1972. A photoelectric digital scanner for measuring leaf area. New Phytol. 7 1(5):819-823. DE WIT, C.T. 1965. Photosynthesis of leaf canopies. Agr. Res. Rpt. 663. Centre for Agricultural Publications and Documentation, Wageningen. DEVYATOV, A.S. 1976. The light regime of palmette apple orchards. Sudouodstuo 5:3 1-32. DEVYATOV, A.S. 1977. The light regime of differently orientated palmette trees. p. 91-99. I n Plodovodstvo Minsk, Belorussian SSR, Urozhai. DEVYATOV, A.S. and A.V. GORNY. 1978. Effect of hedgerow orientation on light status and cropping of apple trees. Abstract 1542. XXth International Horticultural Congress, Aug. 15-23, 1978, Sydney, Australia. Div. of Hort., Sydney. DOWNS, R.J., H.W. SIEGELMAN, W.L. BUTLER, and S.B. HENDRICKS. 1965. Photoreceptive pigments for anthocyanin synthesis in apple skin. Nuture 205:909-910. DUDNEY, P.J. 1974. An analysis of growth rates in the early life of apple trees. Ann. Bot. 38:647-656. DUNCAN, W.G., D.N. SHAVER, and W.A. WILLIAMS. 1973. Insolation and temperature effects on maize growth and yields. Crop Sci. 13:187-190. EREZ, A. 1978. Adaptation of the peach to the meadow orchard system. Acta Hort. 65:245-250. FEDERER, C.A. 1971. Solar radiation absorption by leafless hardwood forests. Agr. Meteor. 9:3-20. FERGUSON, J.H.A. 1960. A comparison of two planting systems in orchards a s regards the amount of radiation intercepted by the trees. Neth. J. Agr. Sci. 8:271-280. FERGUSON, J.H.A. 1963. Influence of orientation and shape of hedgerows of trees on the quantity of intercepted radiation. Meded. Dir. Tuinb. 26: 240-244. FERREE, D.C. 1978. Cultural factors influencing net photosynthesis of apple trees. HortScience 13:650-652. FORSHEY, C.G. and M. WAYNE MCKEE. 1970. Production efficiency of a large and a small McIntosh apple tree. HortScience 5:164-165.
260
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FREEMAN, G.H. and B.D. BOLAS. 1956. A method for the rapid determination of leaf areas in the field. Rpt. East Malling Res. Sta. for 1955, p. 104-107. FULGA, I.G. 1975. Calculation of fruit tree leaf area using linear parameters. Sadouodstuo, Vinogradarstuo i Vinodelie Moldauii 1:53-54. GABRIELSON, E.K. 1948. The influence of light of different wavelengths on photosynthesis in foliage leaves. Physiol. Plant. 1:113-123. GALLAGHER, J.N. and P.V. BISCOE. 1978. Radiation absorption, growth and yield of cereals. J. Agr. Sci., Camb. 91:47-60. GHOSH, S.P. 1973. Internal structure and photosynthetic activity of different leaves of apple. J. Hort. Sci. 48:l-9. GLADYSEV, N.P. 1969. On methods of determining the area of apple leaves. Bot. Z. 54:1571-1575. GROZA, T . 1972. Results obtained by modifying the crown form of apple trees. Revista de Horticultura si Viticultura 21(10):33-38. GYURO, F. 1978. High density apple planting in Hungary. Acta Hort. 65: 53-60. GYURO, F. and L. MOLNAR. 1974. Determination of apricot leaf area. Gyumolcstermeszt6s 1:143-159. HAMER, P.J.C. and J.E. JACKSON. 1975. The incidence of late spring frosts. p. 63-65. I n H.C. Pereira (ed.) Climate and the orchard. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, U.K. HANSEN, P. 1969. I4C-studies in apple trees. IV. Photosynthate consumption in fruits in relation to the leaf-fruit ratio and the leaf-fruit position. Physiol. Plant. 22:186-198. HANSEN, P. 1970a. 14C-studies in apple trees. V. Translocation of labelled compounds from leaves to fruits and their conversion within the fruit. Physiol. Plant. 23:564-573. HANSEN, P. 1970b. 1%-studies on apple trees. VI. The influence of the fruit on the photosynthesis of the leaves and the relative photosynthetic yields of fruits and leaves. Physiol. Plant. 23:805-810. HANSEN, P. 1971. The effect of cropping on the distribution of growth in apple trees. Tidsskr. Planteaul. 75:119-127. HEINICKE, D.R. 1963a. The microclimate of fruit trees. I. Light measurements with uranyl oxalate actinometers. Can. J. P l a n t Sci. 43:561-568. HEINICKE, D.R. 1963b. The microclimate of fruit trees. 11. Foliage and light distribution patterns in apple trees. Proc. Amer. SOC.Hort. Sci. 83:l-11. HEINICKE, D.R. 1964. The microclimate of fruit trees. 111. The effect of tree size on light penetration and leaf area in Red Delicious apple trees. Proc. Amer. SOC.Hort. Sci. 85:33-41. HEINICKE, D.R. 1966. Characteristics of McIntosh and Red Delicious apples as influenced by exposure to sunlight during the growing season. Proc. Amer. SOC.Hort. Sci. 89:lO-13. HEVIN, R. 1977. MBcaniser la taille du pommier. P6pinie'ristes Horticulteurs Mara;chers 182:41-43, 45-51.
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HOLLAND, D.A. 1968. The estimation of total leaf area on a tree. Rpt. East Malling Res. Sta. for 1967, p. 101-104. HUDSON, J.P. 1970. Maximum intensity orchards, growing fruit without trees. Proc. 18th Intern. Hort. Congr., Mar. 15-25, 1970, Tel-Aviv Intern. SOC. Hort. Sci., Ministry of Agr., Israel. 1:56. HUDSON, J.P. 1971. Meadow orchards. Agriculture 78:157-160. IL’INSKII, A.A. 1978. Lowering the height of palmette trees. Sadovodstoo 2:15-16. INDENKO, I.F. and A.R. RASULOV. 1976. Determination of the apple tree total leaf surface area. Sadovodstvo Vinogradarstvo i Vinodelie Moldavii 4: 17-19. JACKSON, J.E. 1967. Variability in fruit size and colour within individual trees. Rpt. East Malling Res. Sta. for 1966, p. 110-115. JACKSON, J.E. 1970. Aspects of light climate within apple orchards. J Appl. E d . 7:207-216. JACKSON, J.E. 1975a. High density planting of fruit trees. I n R. Antoszewski et al. (eds.) Proc. 19th Intern. Hort. Congr., Warsaw, Sept. 10-18, 1974. Wroclawska Drukarnia Naukowa, Warsaw. 3:137-146. JACKSON, J.E. 1975b. Patterns of distribution of foliage and light. p. 31-40. I n H.C. Pereira (ed.) Climate and the orchard. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, U.K. JACKSON, J.E. 1978. Utilization of light resources by high density planting systems. Acta Hort. 65:61-70. JACKSON, J.E. and A.B. BEAKBANE. 1970. Structure of leaves growing a t different light intensities within mature apple trees. Rpt. East Malling Res. Sta. for 1969, p. 87-89. JACKSON, J.E. and A.B. BLANCO. 1973. EMRS tackles problem of containment pruning. Grower 80:1200-1201. JACKSON, J.E. and A.B. BLANCO. 1974. Containment pruning and the use of NAA paints. Rpt. East Malling Res. Sta. for 1973, p. 177-179. JACKSON, J.E. and J . LANDSBERG. 1972. The value of research in orchard climatology. Spun 15(2):63-65. JACKSON, J.E. and J.W. PALMER. 1971. Light distribution within hedgerow orchards. Rpt. East Malling Res. Sta. for 1970, p. 33-35. JACKSON, J.E. and J.W. PALMER. 1972. Interception of light by model hedgerow orchards in relation to latitude, time of year and hedgerow configuration and orientation. J Appl. Ecol. 9:341-357. JACKSON, J.E. and J.W. PALMER. 1973. Rpt. East Malling Res. Sta. for 1972, p. 54-55. JACKSON, J.E. and J.W. PALMER. 1977a. Effects of shade on the growth and cropping of apple trees. I. Experimental details and effects on vegetative growth. J. Hort. Sci. 52:245-252. JACKSON, J.E. and J.W. PALMER. 1977b. Effects of shade on the growth and cropping of apple trees. 11. Effects on components of yield. J. Hort. Sci. 52:253-266.
262
HORTICULTURAL REVIEWS
JACKSON, J.E. and J.W. PALMER. 1979. A simple model of light transmission and interception by discontinuous canopies. A n n . Bot. 44:381-383. .JACKSON, .J.E., J.W. PALMER, M.A. PERRING, and R.O. SHARPLES. 1977. Effects of shade on the growth and cropping on apple trees. 111. Effects on fruit growth, chemical composition and quality a t harvest and after storage. J. Hrrt. Sci. 5 2 :2 6 7 - 2 82. ?JACKSON, .J.E., cJ.D.QUINLAN, and A.P. PRESTON. 1978. Chemical pruning and pruning aids. Acta Hort. 65:199-207. .JACKSON, J.E. and C.H.W. SLATER. 1967. An integrating photometer for outdoor use particularly in trees. J. Appl. Ecol. 4:421-424. .JACYNA, T . 1978. Influence of light penetration on the quality of McIntosh apple fruits. Fruit Science Rpt., Skierniewice, Poland 5(1):7-17. KHAMUKOV, V.B. 1977. Pruning to reduce apple tree crown volume. Trudy Ka bard ino-Ba 1 kar. Opyt St. Sadovodstvo 1:283- 292. KUDRYAVETS, R.P. and V.P. TRUSOV. 1975. T h e effect of different pruning methods on the light regime and photosynthesis in densely planted apple trees. Sbornik Nauch. Rabot N.-1. Zonal’n. In-t Sadovodstvo Nechernozem. Polo,s~8:153- 160. KUMAR, R. and R.P. SRIVASTAVA. 1974. Use of linear measurements in the estimation of leaf area of apple varieties. Progressive Hort. 6(1):63-70. KUMAR, R., R.P. SRIVASTAVA, A.K. SINGH, and D.S. BANA. 1977. Use of linear measurement in the estimation of leaf area of some apricot, peach, plum, pear and guava varieties. Indian J. Hort. 34(3):229-236. LAKSO, A.N. 1976. Characterizing apple tree canopies by fisheye photography. HortScience 11:404-405. LAKSO, A.N. (in press). Correlations of fisheye photography to structure, light, climate and biological responses to light in apple tree canopies. J. Arner. SOC. Hort. Sci. LAKSO, A.N., W.F. MILLER, R.A. PELLERIN, and S.G. CARPENTER. 1978. Conversion of center leader apple trees for improved mechanical harvest. J. Amer. Soc. Hort. Sci. 103:284-287. LAKSO, A.N. and R.C. MUSSELMAN. 1976. Effects of cloudiness on interior diffuse light in apple trees. J. Amer. SOC.Hort. Sci. 101:642-644. LAKSO, A.N. and E.J. SEELEY. 1978. Environmentally induced responses of apple tree photosynthesis. HortScience 13:646-650. LANDSBERG, J.J., C.L. BEADLE, P.V. BISCOE, D.R. BUTLER, B. DAVIDSON, L.D. INCOLL, G.B. JAMES, P.G. JARVIS, P.J. MARTIN, R.E. NEILSON, D.B.B. POWELL, E.M. SLACK, M.R. THORPE, N.C. TURNER, B. WARRIT, and W.R. WATTS. 1975. Diurnal energy, water and CO:! exchanges in an apple (Malus Pumila) orchard. J. Appl. Ecol. 12:659-684. LANG, A.R.G. 1978. Note on the cosine response of cylindrical net radiometers. Agr. Meteor. 19:391-397. LOMBARD, P.B. and M.N. WESTWOOD. 1977. Effect of hedgerow orientation on pear fruiting. Acta Hort. 69:175-179.
L I G H T INTERCEPTION & UTILIZATION BY ORCHARD SYSTEMS
263
LOOMIS, R.S. and P.A. GERAKIS. 1975. Productivity of agricultural ecosystems. p. 145-172. In J.P. Cooper (ed.) Photosynthesis and productivity in different environments. Cambridge Univ. Press, London. LOOMIS, R.S., W.A. WILLIAMS, and A.E. HALL. 1971. Agricultural productivity. A n n u . Reu. Plant Physiol. 22:431-468. LOONEY, N.E. 1968. Light regimes within standard size apple trees as determined spectrophotometrically. Proc. Amer. SOC.Hort. Sci. 93:l-6. LUCKWILL, L.C. 1978. Meadow orchards and fruit walls. Acta Hort. 65: 237-243. MAGGS, D.H. 1960. T h e stability of the growth pattern of young apple trees under four levels of illumination. A n n . Bot. 24:434-450. MAGGS, D.H. 1963. The reduction in growth of young apple trees brought about by fruiting. J. Hort. Sci. 38:119-128. MAGGS, D.H. 1967. Measuring light in orchard canopies by the photolysis of uranyl oxalate. Austral. J. Instrumn. Control 23:58-59. MAGGS, D.H. and D.MCE. ALEXANDER. 1970. Tests of a uranyl oxalate light integrator for use in fruit tree canopies. J. Appl. Ecol. 7:639-646. MAGGS, D.H. and D.MCE. ALEXANDER. 1973. T h e foliage light product, a measure for assessing orchard canopies and its relation to the yields of three apple varieties trained to three forms. J. Appl. Ecol. 10:501-511. MARKOV, I.E. 1973. Characteristics of the radiation regime in the crown of apple trees on dwarfing rootstocks. Fiziologiya i Biokhimiya Kul’turnykh Rastenii 5(1):71-74. MARSHALL, J.K. 1968. The photographic-photoelectric planimeter combination method for leaf area measurement. Photosynthetica 2:l-9. MCKENZIE, D.W., J.S. DUNN, M. STOLP, and R.J. HUTTON. 1978. Horizontal canopy orchards for mechanical harvesting. Acta Hort. 65:267-276. MCKENZIE, D.W. and A.N. RAE. 1978. Economics of high density apple production in New Zealand. Acta Hort. 65:41-46. MCPHERSON, H.G. 1969. Photocell-filter combinations for measuring photosynthetically active radiation. Agr. Meteor. 6:347-356. MIKA, A. and R. ANTOSZEWSKI. 1972. The effect of leaf position and tree shape on the rate of photosynthesis in the apple tree. Photosynthetica 6: 381-386. MIKA, A. and R. ANTOSZEWSKI. 1974. Photosynthesis efficiency of apple trees trained as hedgerows. Fruit Science Rpt., Skierniewice, Poland 1 (1): 10-17. MOLNAR, L. and Z. SZAKALL. 1971. A preliminary communication on the foliage area of apricots. Szolo-es Gyumolcstermesztes 6:129-132. MONSI, M. and T. SAEKI. 1953. Uber den lichtfaktor in den pflanzengesellschaften und seine bedentung, fur die stoffproduktion. Japan. J. Bot. 14: 22-52. MONSI, M., Z. UCHIJIMA, and T . OIKAWA. 1973. Structure of foliage canopies and photosynthesis. A n n u . Rev. Ecol. System. 4:301-327.
264
HORTICULTURAL REVIEWS
MONTEITH, J.L. 1969. Light interception and radiative exchange in crop stands. p. 89-111. I n J.D. Eastin, F.A Haskins, C.Y. Sullivan, C.H.M. Van Bavel (eds.) Physiological aspects of crop yield. Amer. SOC.Agron. and Crop Sci. Soc. Amer., Madison, Wisc. MONTEITH, J.L. 1973. Principles of environmental physics. Arnold, London. MONTEITH, J.L. 1977. Climate and the efficiency of crop production in Britain. Phil. Trans. R. SOC.Lond. B. 281:277-294. MORESHET, S., G. STANHILL, and M. FUCHS. 1975. Aluminum mulch increases quality and yield of 'Orleans' apples. HortScience 10:390-391. NEUTEBOOM, D.I. 1978. Cox production in England. Grower Books, London. ODIER, G. 1978a. Rble du rayonnement solaire en arboriculture fruitiere. A r boriculture Fruitiere 295:23-29. ODIER, G. 197813. R6le du rayonnement solaire en arboriculture fruitiere. 2" partie. Arboriculture Fruitiere 296:31-35. OIKAWA, T . 1977a. Light-regime in relation to plant population geometry. 11. Light penetration in a square-planted population. Bot. Mag. Tokyo 9O:ll-22. OIKAWA, T . 1977b. Light regime in relation to plant population geometry. 111. Ecological implications of a square-planted population from the viewpoint of utilization efficiency of solar energy. Bot. Mug. Tokyo 90:301-311. OIKAWA, T . and T . SAEKI. 1977. Light regime in relation to plant population geometry. I. A Monte-Carlo simulation of light microclimates within a random distribution foliage. Bot. Mag. Tokyo 9O:l-10. OLANIRAN, Y.A.O. 1974. Some environmental and physiological factors affecting the growth, flowering and fruiting of intensively grown apple trees. PhD. Thesis, University of Reading, U.K. OVSYANNIKOV, A S . 1972. A method for determining the photosynthetic activity of pear and plum leaves during fruit formation. Sel 'skokhozyu&tuennaya Biologiya 7:605-611. PALMER, J.W. 1976. Interception and utilisation of light by apple orchards. PhD. Thesis, University of Nottingham, Nottingham, U.K. PALMER, J.W. 1977a. Light transmittance by apple leaves and canopies. J. Appl. E d . 14:505-513. PALMER, J.W. 1977b. Diurnal light interception and a computer model of light interception by hedgerow apple orchards. J. Appl. Ecol. 14:601-614. PALMER, J.W. .1980. T h e measurement of visible irradiance using filtered and unfiltered tube solarimeters. J. Appl. Ecol. PALMER, J.W. and J.E. JACKSON. 1975. Rpt. East Malling Res. Sta. for 1974, p. 52. PALMER, J.W. and J.E. JACKSON. 1977. Seasonal light interception a n d canopy development in hedgerow and bed system apple orchards. J. Appl. E d . 14:539-549. PALMER, J.W. and J.E. JACKSON. 1978. Rpt. East Malling Res. Sta. for 1977, p. 55.
L I G H T INTERCEPTION & UTILIZATION BY ORCHARD SYSTEMS
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PARRY, M.S. 1978. Integrated effects of planting density on growth and cropping. Acta Hort. 65:91-100. PRESTON, A.P. 1958. Apple rootstock studies: thirty five years’ results with Lane’s Prince Albert on clonal rootstocks. J. Hort. Sci. 33:29-38. PRESTON, A.P. 1975. Wind exposure and crop yield. p. 95-97. In H.C. Pereira (ed.) Climate and the orchard. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, U.K. PRESTON, A.P. 1978. A bed system for planting apples on the dwarfing rootstock M.27. Acta Hort. 65:229-235. PRIESTLEY, C.A. 1969. Some aspects of the physiology of apple rootstock varieties under reduced illumination. Ann. Bot. 33:967-980. PROCTOR, J.T.A. 1978. Apple photosynthesis: microclimate of the tree and orchard. HortScience 13:641-643. PROCTOR, J.T.A. and L.L. CREASY. 1971. Effect of supplementary light on anthocyanin synthesis in McIntosh apples. J Amer. SOC.Hort. Sci. 96: 523-526. PROCTOR, J.T.A., W.J. KYLE, and J.A. DAVIES. 1972. The radiation balance of an apple tree. Can. J. Bot. 50:1731-1740. PROCTOR, J.T.A., W.J. KYLE, and J.A. DAVIES. 1975. The penetration of Hort. Sci. 100:40-44. global solar radiation into apple trees. J. Amer. SOC. QUINLAN, J.D. 1978. Chemical induction of lateral branches (feathers). Acta Hort. 65:129-138. ROSATI, P. 1978. Tall hedgerow systems. Acta Hort. 65:255-260. RUD’, G. YA., V.K. TANAS’EV, and V.V. BALAN. 1977. Light regime of palmette trained young apple trees. Sadouodstuo, Vinogradarstuo i Vinodelie Moldauii (1):12-15. RUD’, G. YA., V.K. TANAS’EV, and G.P. CHIMPOESH. 1976. Light relations in apple trees with palmette crowns in relation to rootstocks and spacing. Trudy Kishinewkoga S. Kh. Instituta 154:31-35. RUD’, G. YA., V.K. TANAS’EV, V.V. MARCHENKO, and G.P. CHIMPOESH. 1977. Light regime in palmette apple trees. Sadouodstuo, Vinogradarstuo i Vinodelie Moldavii (11):16-18. SAEKI, T . 1975. Distribution of radiant energy and C 0 2 in terrestrial communities. p. 297-322. I n J. P. Cooper (ed.) Photosynthesis and productivity in different environments. Cambridge Univ. Press, London. SANSAVINI, S. 1978. Mechanical pruning of fruit trees. Acta Hort. 65: 183-197. SCEICZ, G. 1974. Solar radiation in crop canopies. J Appl. Ecol. 11:11171156. SCEICZ, G., J.L. MONTEITH, and J.M. DOS SANTOS. 1964. Tube solarimeter to measure radiation among plants. J. Appl. Ecol. 1:169-174. SCHURER, K. 1971. Direct reading optical leaf area planimeter. Acta Bot. Neerl. 20:132-140.
266
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SEELEY, E.J. 1978. Apple tree photosynthesis: an introduction. HortScience 13:640-641. SERAFIMOVA, R. 1974. Leaf area coefficient determination in apricots. Gradinarska i Lozarska Nauka 11(2):17-22. SHUL’GIN, I.A., A.F. KLESHNIN, M.I. VERBOLOVA, and V.Z. PODOL’NYI. 1960. An investigation of the optical properties of leaves of woody plants using the SF-4 spectrophotometer. Souiet Plant Physiol. 7(3):247-252. SIBMA, L. 1977. Maximization of arable crop yields in the Netherlands. Neth. J. Agr. Sci. 25:278-287. SIROIS, D.L. and G.R. COOPER. 1964. The influence of light intensity, temperature and atmospheric carbon dioxide concentration on the rate of apparent photosynthesis of a mature apple tree. Maine Agr. Expt. Sta. Bul. 626. SKENE, D.S. 1974. Chloroplast structure in mature apple leaves grown under different levels of illumination and their responses to changed illumination. Proc. R. Soc. London, L3. 186:75-78. SMART, R.E. 1975. Implications of the radiation microclimate for the productivity of vineyards. PhD. Dissertation, Cornell University, Ithaca, N.Y. SUCKLING, P.W., J.A. DAVIES, and J.T.A. PROCTOR. 1975. The transmission of global and photosynthetically active radiation within a dwarf apple orchard. Can. J. Bot. 53:1428-1441. TEREKHOVA, A S . 1976. Changes in the light regime after lowering apple crowns. Trudy Kuban. S.-Kh. Instituta 131(159):98-100. THORPE, M.R. 1974. Radiant heating of apples. J. Appl. Ecol. 11:755-760. TOLSTOGUZOVA, V.G. 1975. Effect of the light regime on shoot growth and leaf and fruit distribution in round and palmette apple tree crowns. Sbornih Nauch. Rabot N.-1 Zonal’n In-t. Sadouodstuo Nechernozem. Polosy 8:161-167. TUKEY, L.D. 1978. The thin-wall trellis hedgerow system. Acta Hort. 65: 261-266. TURNBULL, J . 1978. The Grower Dec. 7, 1978, p. 1084. TYDEMAN, H.M. 1964. The relation between time of leaf break and of flowering in seedling apples. Rpt. East Malling Res. Sta. for 1963, p. 70-72. UTERMARK, H. 1976. Summer pruning. Mitteilungen des Obstbauuersuchsringes des Alten Landes 31:95-102. VAN OOSTEN, H.J. 1978. Effect of initial tree quality on yield. Acta Hort. 65:123-128. VERHEIJ, E.W.M. 1968. Yield-density relationships in apple; results of a planting system experiment in Hungary. I.T.T. Wageningen. Publikatie Nr 37. VERHEIJ, E.W.M. 1972. Competition in apple, as influenced by alar sprays, fruiting, pruning and tree spacing. Meded. Landbouwhogeschool Wageningen. p. 72-74. VERHEIJ, E.W.M. and F.L.J.A.W. VERWER. 1973. Light studies in a spacing trial with apple on a dwarfing and a semi-dwarfing rootstock. Scien. Hort. 1:25-42.
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VERHEIJ, E.W.M. and H.C.P. DE VRIES. 1966. Is there scope for a bed system in fruit growing. Meded Dir. Tuinb. 29(8):338-343. WATSON, D.J. 1947. Comparative physiological studies in the growth of field crops. I. Variation in net assimilation rate and leaf area between species and varieties, and within and between years. Ann. Bot. NS 11(41):41-76. WATSON, D.J. 1952. The physiological basis of variation in yield. Adu. Agron. 4:101-145. WERTH, K. 1978. Economics of high density planting in South Tyrol. Acta Hort. 65:47-52. WERTHEIM, S.J. 1978. Intensive apple orchards with slender spindles. Acta Hor t. 65 :2 09- 2 16. WESTWOOD, M.N. 1970. Tree size control as it relates to high density orchard systems. Proc. 65th Annual Meeting, Washington State Horticultural Association. YIM, Y.J., H. OGAWA, and T. KIRA. 1969. Light interception by stems in plant communities. Japan. J. Ecol. Sendai 19:233-238.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
6 The Physiology of In Vitro Asexual Embryogenesis W. R. S h a r p L Pioneer Research Laboratory, Campbell Institute for Agricultural Research, 261 1 Branch Pike, Cinnaminson, New Jersey 08077 M. R. Sondahl Departmento de Genetica, Instituto Agronomica, Caixa Postal 28, 13.100 Campinas, S.P., Brazil L. S. Caldas Departmento de Botanica, Universidade de Brasilia, Brasilia, DF, Brazil S. B. M a r a f f a Department of Horticulture, Ohio State University, Columbus, Ohio 43210 I. Introduction 269 A. Concept of in vivo and in vitro Embryogenesis 271 B. Patterns of in vitro Embryogenesis C. Determination of Embryogenic Precursor Cells 11. Physiology 273 A. Nitrogen Effects 273 B. Other Mineral Salts 275 276 C. Defined and Undefined Organics D. Growth Regulator Effects 277 1.Auxins 277 2. Cytokinin and Cytokinin/Auxin Interactions 3. Gibberellin and Abscisic Acid 280 4.Embryogenic Inhibition Factor 280 111. Developmental and Molecular Aspects 281 A. Callus Initiation 281 B. Polarity 282
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IWe thank Joyce J. Albert, Helen C. Greth, and Karen M. Selover for their help in preparing the manuscript, and Bruce E. Ogden for preparing the photographic plates.
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C. Theories of Embryogenesis 283 1.Dedifferentiation Theory 283 2. Cell Isolation Theory 284 3. Explant Physiology and Culture Environment Theory 285 286 4. Intercellular Communication and Cytodifferentiation 5 . Predetermination Theory 286 287 6. Pre- and Induced Embryogenic Determined Cell Theory D. Pre-Embryogenic Determined Cells (PEDC) 287 1.Citrus Nucellus 287 288 2. Other Examples of PEDC E. Induced-Embryogenic Determined Cells (IEDC) 288 F. The Mitotic Cell Cycle and Embryo Determination 290 G. RNA and Protein Synthesis in Carrot 296 IV. Conclusions 300 V. Literature Cited 301
I. INTRODUCTION
Apomixis, asexual reproduction, and vegetative propagation are general terms used to define plant development from either sporophytic or gametophytic tissues in the absence of fertilization. Diploid plants are obtainable from sporophytic tissues, whereas haploid plants may be obtained from tissues of gametophytic origin. Organogenesis and embryogenesis are included in a definition of these terms and have been observed both in vivo and in uitro. Organogenesis is limited to the initiation of organ primordia, while an embryo, an initial stage in plant development, is characterized by a bipolar structure bearing shoot and root poles following a series of developmental sequences, e.g., globular, heart, and torpedo stages of dicotyledenous plants. Several types of embryogenesis may be defined: androgenesis implies that the embryos are of miscrospore origin, parthenogenesis pertains to embryos of oospore or ovum origin, gynogenesis is restricted to embryos derived from incompletely fertilized oospores, and finally apometry describes the origin of embryos from either synergids or antipodals. Although both in vitro organogenesis and embryogenesis are practical propagation methods, in vitro embryogenesis offers greater potential in crop improvement programs since it allows for the coupling of efficient cloning and genetic modification. Thus, a limited amount of genetically modified germ plasm may be utilized to obtain a uniform population of genetically modified plantlets. A. Concept of in vivo and in vitro Embryogenesis
Although three extensive reviews of embryogenesis have been made, the concepts of in vivo and in vitro embryogenesis are not entirely clear
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(Street 1979; Tisserat et al. 1979; Kohlenbach 197810). While the concept of in vivo embryogenesis is most often characterized by embryo development following fertilization, it also encompasses the formation of embryos from the intact plant by means other than fertilization, i.e., in situ development from gametophytic tissues, stems, or leaves. In vitro embryogenesis has been defined as the developmental process producing a perfect embryo from a single cell, all the derivatives from which become part of a structure which achieves bipolarity a t as early a stage as occurs in zygotic embryogenesis (Street and Withers 1974). Kohlenbach (1978a) views the induction of embryogenesis as the previous transformation of vacuolated parenchymatical cells into densely cytoplasmic cells with an embryogenic determination. Embryo initials (embryogenic cells) can be recognized by their conspicuous starch contents (Halperin 1970; Halperin and Jensen 1967; Konar et al. 1972a) and their close morphological and cytological resemblance to the apical meristem or zygotic embryo cells, i.e., they are small, relatively isodiametric, rich in cytoplasm, prominent of nuclei, thinwalled, and minimally vacuolated. Although suspensor development occurs during somatic embryogenesis (Sondahl and Sharp 1977; Sondahl, Spahlinger and Sharp 1979; Pence et al. 1979), this is not true for all taxa. In the latter situation, the developing embryo apparently is nurtured by neighboring cells through protoplasmic connections (Halperin and Jensen 1967; Konar et al. 1972a; Wochok 1973). Examples of in vivo and in vitro embryogenesis are reviewed by Tisserat et al. (1979). I t should be noted that the cellular phenotypes undergoing embryogenesis in vitro are more numerous than those occurring in vivo. A comparison of in vivo and in vitro embryogenesis indicates a common series of developmental events. T h e normal development of the Daucus carota embryo in vivo was studied by Borthwick (1931), and demonstrates characteristics consistent with development in many other species. After fertilization, the zygote elongates and divides, and these daughter cells then divide synchronously two more times to form a filamentous grouping of cells. At this stage, variable patterns of development among embryos are observed. Daughters of the distal and sub-distal cells of the four-celled filaments begin to divide periclinically and delineate the plerome, periblem, and dermatogen of the embryo. T h e suspensor develops from the proximal remaining cells. In vitro embryogenesis is characterized by this same pattern of development (Backs-Husemann and Reinert 1970). After an initial unequal division of the zygote, continued division of these daughter cells to form a filamentous grouping may (Backs-Husemann and Reinert 1970; Kato 1968) or may not (Nakajima and Yamaguchi 1967) occur. According to
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Backs-Husemann and Reinert ( 19701, “Adventive embryos have a development of a more or less proembryonic cell complex, and then follow a normal embryogenesis with the preformed suspensor as in the zygotic embryo.” T h e globular, heart-shaped, and torpedo stages of embryo development are usually seen, with the heart-shaped stage often lacking due to retarded cotyledon development (Halperin 1966; Nakajima and Yamaguchi 1967). Tisserat e t al. (1979) compiled a comprehensive list of plants capable of undergoing complete or incomplete in uitro embryogenesis. However, a distinction must be made between complete and incomplete embryogenesis. Incomplete embryogenesis implies arrestment during early stages of development, usually a t the globular stage. Reports quoting instances of complete embryogenesis should employ the term embryo, in accordance with the suggestions made in the Proceedings of the First International Symposium on Haploids in Higher Plants (Fossard 1974). T h e terms arrested embryos, proembryos, or embryoids cannot be confused with de facto embryogenesis.
B. Patterns of in vitro Embryogenesis This review will place emphasis on the physiological events th a t determine in vitro embryogenesis. In the hope of furthering our understanding of embryogenesis, an attempt will be made to integrate current research pertaining to the determination of embryogenic cells and their subsequent development into plantlets. Two general patterns of embryogenic development of in uitro embryogenesis are discernible: (1) direct embryogenesis: embryos originate directly from tissues in the absence of callus proliferation (i.e., nucellar cells of polyembryonic varieties of citrus, epidermal cells of hypocotyl in wild carrot and Ran u n cu lu s sceleratus); (2) indirect embryogenesis: callus proliferation is prerequisite to embryo development (i.e., secondary phloem of domestic carrot; inner hypocotyl tissues of wild carrot; leaf tissue explants of coffee; pollen of rice and some other Gramineae, etc.). An understanding of these two different patterns of development depends upon consideration of the determinative events of cytodifferentiation during the mitotic cell cycle. It is well known th a t the fate of determined daughter cells following mitosis occurs a t least one mitotic cell cycle prior to differentiation (Yeoman 1970). Cells which will undergo embryogenesis directly are the daughters of a prior determinative cell division. Such determined cells may undergo a post-mitotic arrestment until environmental conditions are favorable for commencement of the mitotic developmental sequence characteristic of embryogenesis.
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C. Determination of Embryogenic Precursor Cells Street and Withers (1974), in their ultrastructural analysis of carrot somatic embryogenesis, were unable to identify embryogenic cells in callus cultures. However, callus cells, embryogenic cells, and globular embryos are clearly distinguishable in tissue cultures of Coffea ara bica (Sondahl, Salisbury and Sharp 1979). Identification of the embryogenic mother cells or the stem cells of the embryogenic event will allow a better understanding of the early determinative events in embryogenesis. As discussed previously, two general patterns of in vitro embryogenic development, direct and indirect, may be recognized and may be further characterized by their relative times of determination and differentiation into embryogenic cells. Direct embryogenesis proceeds from preembryogenic determined cells (PEDC) (Kato and Takeuchi 1966; Konar and Nataraja 19651, while indirect embryogenesis requires the redetermination of differentiated cells, callus proliferation, and differentiation of embryogenic determined cells (IEDC). Apparently, PEDC’s await either synthesis of an inducer substance or removal of an inhibitory substance, requisite to resumption of mitotic activity and embryogenic development. Conversely, cells undergoing IEDC differentiation require a mitogenic substance to reenter the mitotic cell cycle and/or exposure to specific concentrations of growth regulators. Cyto-differentiation and the emergence of multicellular organization are multi-step processes in which each step leads to the establishment of a particular pattern of gene activation, allowing transition to the next essential state of development (Street 1978). Arrestment may occur a t any step in this process. T he view that external applications of growth regulators can be permissive or inhibitive of differentiation but not determinative (Street 1978) has been evolved. Tisserat et al. (1979) concur th a t the explant and certain of its associated physiological qualities are the most significant determinants of embryo initiation, while the in uitro environment acts primarily to enhance or repress the embryogenic process. T h a t is, the cells t ha t undergo embryo initiation are predetermined, and their subsequent exposure to exogenous growth regulators simply allows embryogenesis to occur (Tisserat et al. 1979). Street (1978) believes th a t growth regulators may be regarded best as activating agents toward previously induced cells which are preconditioned to respond in specific ways. We are in agreement with Street (1978) and Tisserat et al. (1979) if their definition is restricted to PEDC. However, these investigators have not recognized the occurrence of two distinct patterns of development, i.e., PEDC and IEDC. Their concept of embryogenesis is limited to predetermined embryogenic cells, where growth regulators serve only to ini-
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tiate embryo development from PEDCs and/or the cloning of these PEDCs. However, an alternative concept must be developed to explain how induced embryogenic determined cells (IEDCs) become committed to embryogenic development, since the occurrence of such cells requires redetermination and commitment to embryogenesis. 11. PHYSIOLOGY
A. Nitrogen Effects
In uitro studies to determine the effects of different nitrogen sources in the culture medium have been conducted on primary explants, callus, and developing embryos. These investigations focus on the effects of ammonium and nitrate on carrot suspension cultures. Once established, callus cells replicate less frequently in the presence of NH,+ and develop into multicellular clumps, while cells exposed to Nosseldom give rise to these structures. The requirement for ammonium, or a t least some source of reduced nitrogen, i.e., glycine, glutamine, or yeast extract, in carrot embryogenesis has been documented in the literature (Halperin 1966; Beccari et al. 1967; Kato and Takeuchi 1966; Norreel and Nitsch 1968). I t is apparent that this requirement for reduced nitrogen must be met during a critical time of development since secondary culture of callus grown on ammonium following primary culture on NO3- fails to develop multicellular structures and embryos (Halperin and Wetherell 1965).Explants cultured on medium containing NH4+ usually are characterized by a higher frequency of embryogenesis than those on NO,- a t the same nitrogen concentration. At a total nitrogen concentration of 44.4 mM, 49% of the cultures on NH4NO:i undergo embryogenesis, while 40% of those on KNO:1 become embryogenic (Reinert, Tazawa, and Semenoff 1967). Strong evidence that ammonium is not required for embryogenesis and can be replaced by nitrate in the medium (Reinert 1968; Tazawa and Reinert 1969) also exists. Occasionally, embryogenesis in the presence of NOti- even will surpass that in the presence of NH4+; embryo development occurs in 40% of the cultures on White's medium supplemented with KN03, while a medium containing the same total amount of nitrogen supplied as NH4N03 was associated with embryogenesis in 27% of the cultures (Reinert 1968). The distinct conflict with the effects of nitrogen source on embryogenesis can be understood better after studying other components of the respective culture media, especially 2,4-D (Caldas 1971). Experiments demonstrating an ammonium requirement for obtainment of embryos used concentrations of 2,4-D from 2.5 to 25 times higher than
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those without the ammonium requirement. Apparently, the ammonium requirement is associated with the specific concentration of 2,4-D in the culture medium. Additional evidence in support of this concept is found in the fact th at Halperin and Wetherell did not find an ammonium requirement in the medium in which the embryos were developing, but only in the primary culture medium (Halperin 1966; Halperin and Wethere11 1965). Th e only difference between the two media is th a t the medium of the original explant contains 4.5 X 10 M 2,4-D, and the medium in which the embryos develop includes 4.5 X 10 -‘M 2,4-D. White’s medium, which contains a low nitrogen concentration (3.2mM), allows for embryo determination unless 2,4-D ( 2 X 10 -’) is added (Reinert and Backs 1968). Thus, it appears that ammonium is required for embryo formation in the presence of 2,4-D above certain concentrations. Although a relationship between ammonium requirement and 2,4-D concentrations is evident, a complete characterization of the relationship between the two factors as well as their effect on embryo determination cannot be made a t this time. Moreover, work accomplished by Kamada and Harada (197913) suggests the requirement for reduced nitrogen to be not for the embryogenic determination of cells cultured on 2,4-D-containing medium. Instead of determination, the role of reduced nitrogen pertains to the development of the embryogenic determined cells into multicellular embryos on the 2,4-D-containing medium. With regard to the nitrogen source, Tazawa and Reinert (1969) noted that, “Although the occurrence of NH,+ in the medium is not necessary for embryo formation in uitro, it appears th a t a certain level of intracellular N H 4+ is a prerequisite for this process.” Their data indicate th a t there may be a positive correlation between intracellular NH4+ concentration and embryo development, but they do not support the idea th a t a threshold level must be attained as a prerequisite (Tazawa and Reinert 1969). Intracellular NH4+ concentrations below 10 mM per kg of fresh weight correlate with embryo development in 30% of the cultures, and as little as 1 to 2 mM NH4+ was associated with embryogenesis in 22 to 28% of the cultures. These figures do not differ markedly from the percentages of embryogenesis a t NH4+ concentrations of 20 to 40 mM per kg of fresh weight. Other investigations with nitrogen sources have dealt with amino acids rather than ammonium or nitrate. Among these, glutamate (Reinert et al. 1967; Tazawa and Reinert 1969) as well asglutamine (Halperin 1964, 1966; Nitsch and Nitsch 1969) has been partially or completely successful in replacing ammonium. In carrot, neither lysine, leucine (Norreel and Nitsch 1968), nor aspartic acid (Halperin 1966) was effective in the absence of NH,+, while asparagine was inhibitory (Mahler and Cordes 1966). None of these latter amino acids are derived biosynthetically from
-‘
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glutamine (Mahler and Cordes 1966). Since it already has been shown (Caldas 1971) th at carrot cells have a high glutamine synthetase activity allowing glutamine to be synthesized with just N H 4 + in the medium, the conclusion can be drawn th at glutamine or one of its products is critical in embryo determination. Other experiments pertain to the effects of various amino acids added to -2,4-D secondary culture medium consisting of basal medium a n d 20 mM KNO:I to determine the effects of amino nitrogen on the development of embryogenic determined cells (Kamada and Harada 197910). Five to ten mM concentrations of a-alanine proved to be especially effective toward increasing the frequency of embryo development. Stimulation of embryo development to a somewhat lesser degree occurred when either glutamine, aspartic acid, glutamic acid, arginine, or proline was added to the culture medium. Lysine, valine, histidine, leucine, and methionine had no effect on embryo development. 6-alanine was found to have no effect on embryo development, and pyruvic acid counteracted the stimulatory effect of glutamic acid on embryo development. Glutamine was the most effective amino acid to promote embryo development when added to -2,4-D medium devoid of other nitrogenous compounds. Glutamic acid and a-alanine added to the same medium also enhanced the frequency of embryo development a t the 10 to 30 mM concentrations. Arginine, asparagine, aspartic acid, threonine, and proline had no effect on the stimulation of embryo formation when added to the nitrogenous free culture medium (Kamada and Harada 197913).
B. Other Mineral Salts White’s medium supplemented with nitrogen a t a concentration of 17.0
mM does not promote embryo formation, although a concentration of 1 5
mM nitrogen in Murashige and Skoog’s medium (Murashige and Skoog 1962) promotes embryogenesis (Reinert et al. 1967). (Both of these media included 2,4-D a t low concentrations.) While there are many differences between the two media which could account for these differing results, it is apparent th at the potassium ion may be one of the most important. At low nitrogen concentrations, there is a stimulation of embryo formation by potassium (Reinert et al. 1967; Tazawa and Reinert 1969); a n increase of from 3 to 20 mM in K concentration promotes a n increase in the percentage of cultures forming embryos of from 5 to 45%. T h e difference in K t concentration between White’s medium and Murashige and Skoog’s medium is substantial, with only 0.06 mM K+ in White’s and 20 mM in Murashige and Skoog’s. In the section dealing with the ammonium requirement, an example was mentioned in which the percentage of cultures forming embryos on White’s medium supplemented +
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with KNOs was greater than the percentage on White's medium supplemented with NH4NO:j (Reinert 1968). In this case, it may be that K' was actually the limiting factor. In wild carrot suspension cultures, optimal embryogenesis requires potassium in the concentration of 20 m ~whereas , optimal callus proliferation will be supported by a concentrationof 1mM (Konar and Nataraja 1965b). Studies have demonstrated a possible inhibition of embryo formation when phosphate concentration is increased from 1.25 to 20 mM (Tazawa and Reinert 1969) with a simultaneous decrease in the frequency of embryogenesis from 32 to 20%. A decrease in the frequency of carrot embryogenesis from 100% to 10 to 20% results when either NaCl or Na2S04is used to increase osmotic pressure of the culture medium for 0.7 to 6.9 a t m (Butenko et al. 1967). C. Defined and Undefined Organics Different types and concentrations of sugars have been employed as energy sources. Elongation of asparagus embryos was inhibited a t sucrose concentrations between 2% and 10% (Wilmar and Hellendoorn 1968). Glucose concentrations ranging from 6 to 10% led to an increase in embryo production in carrot cultures, while 10% glucose correlated with optimum embryo formation (Homes 1967). Higher sucrose concentrations (18%)promoted plantlet formation in anthers of tobacco (Sharp et al. 1971), independent of the hormone treatments. It is also interesting that excised embryos of Capsella bursapastoris do not demonstrate the usual requirement for IAA, kinetin, and adenine sulfate when the sucrose concentration is increased to 12 to 18% (Raghavari and Torrey 1963). T h e stimulatory effect of higher glucose and sucrose concentrations is probably not due to the resulting increase in osmotic pressure, since Butenko et al. (1967) noted a steady decline in the percentage of cultures forming embryos as the osmotic pressure was increased from 0.35 to 6.9 atm with either NaCl or Na2S04. Coconut milk has been used often as an organic supplement to the culture media. Steward et al. (1964) once claimed that coconut milk included in the culture medium was required for cell division and embryo formation in carrot cell cultures. However, by using defined media it was demonstrated that coconut milk is not essential for embryo formation (Halperin 1964; Reinert and Backs 1968), and that 10% coconut milk even reduces the percentage of embryo formation by 50% (Reinert 1968). Other systems, such as Ranunculus sceleratus, are not sensitive to the influence of coconut milk and will form embryos in its presence or absence (Konar and Nataraja 1965a,b).
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D. Growth Regulator Effects 1. Auxins.-The early experiments of Wetmore and Rier (1963) with Syringa vulgaris and the later studies of Jeffs and Northcote (1967) with Phaseolus vulgaris demonstrated the formation of vascular elements in callus masses in response to concentration gradients of auxin (IAA) and sucrose. A requirement for both exogenous auxin and cytokinin for tracheary element formation and for callus induction in various species has been reported by various workers. Trewavas (1976) concluded that the primary mode of action of the known natural growth regulating substances is probably their action on membrane systems, particularly their control of ion fluxes. This in turn could lead to many of the biochemical changes which they are known to induce. Thus, natural regulators may perhaps best be regarded as activating agents for cells pre-conditioned to respond in specific ways. The contention also has been made that natural growth regulators, depending on their absolute and relative concentrations, may suppress, permit or modify under permissive conditions morphogenesis or cytodifferentiation in cells previously rendered totipotent or capable of following a pattern of differentiation (Street 1976). Widely varying results regarding hormone effects on embryogenesis in vitro have been obtained. Employment of different auxins in various systems has led to the conclusion that either: (1) auxin is essential for embryo formation (Kato and Takeuchi 1966; Sussex and Frei 1968) or (2) auxin inhibits embryo formation (Halperin 1966; Petru 1970). With carrot cultures, a comparison of growth and relative embryo formation a t different 2,4-D concentrations indicates that the concentrations associated with the greatest degree of growth are not the same as those associated with high frequency embryogenesis (Kato and Takeuchi 1966). This same observation was noted in studies of embryogenesis in coffee leaf callus cultures; highest frequencies of embryo formation were observed when explants were cultured on a primary medium with kinetin/2,4-D concentration ratios of 18.4/4.5 p M (60%), 18.4/18 (50%), and 36.8/4.5 (60%), whereas optimal callus proliferation occurred a t kinetin/2,4-D concentration ratios of 10/5 to 18/9 pM (Sondahl and Sharp 1977, 1979; Sondahl, Spahlinger, and Sharp 1979; Sondahl, Salisbury, and Sharp 1979). The qualitative and quantitative aspects of growth regulators in the microenvironment of embryogenic determined cells are important in the mitotic arrestment or release from arrestment (Tisserat and Murashige 1977a,b; Caldas 1971). Furthermore, the normalcy of embryo development from these determined embryogenic cells as well as mitotic arrestment is regulated by growth regulators in a t least one instance (Am-
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mirato 1977), i.e., Carraway. General conclusions may be drawn after considering somewhat anomalous systems in which 2,4-D was used (Kato 1968; Kato and Takeuchi 1966). Carrot hypocotyl segments cultured on White’s Medium containing 5 X 10 -RM 2,4-D do not develop embryos, while callus originating from hypocotyl segments grown on medium containing higher concentrations of 2,4-D and subcultured onto -2,4-D medium develops embryos (Halperin 1964). Globular embryos develop on medium containing 10 - 6 to 10 2,4-D, but further development is restricted unless tissues are transferred to medium containing only 5 X 2,4-D (Kato 1968). This general pattern is in agreement with 10 other investigators who have employed 2,4-D. T o some extent, the overlap between permissive and non-permissive ranges of 2,4-D concentration can be explained by other differences in the media. As was mentioned in the discussion on nitrogen sources, there is an interaction between 2,4-D and nitrogen concentrations which affects embryo development. White’s medium, supplemented with 2 X 10 -7M 2,4-D, is not permissive to embryo development, but with additional nitrogen or Murashige and Skoog’s medium supplemented with the same 2,4-D concentration embryos develop (Reinert et al. 1967; Tazawa and Reinert 1969). Some effects of auxins on the morphology and behavior of cells in culture have been demonstrated. Carrot cells grown in the presence of 5 2,4-D lose their chlorophyll, and become aneuploid X 10 -7 to 5 X 10 on solid media (Halperin 1966).Cells in clumps tend to break off because of the disappearance of the fibers in the middle lamella and surrounding cell wall when cultured in the presence of 2,4-D (Halperin and Jensen 1967). Even the growth pattern within the first five days reportedly changes with alteration in the growth regulator concentration. Carrot cells tend to form tetrads on 5 X 10 -6M 2,4-D, but have a filamentous form of growth in the absence of 2,4-D or on 6 X 10 - 7 M IAA (Nishi and Sugano 1970). Caldas (1971) studied the time course of somatic embryo formation after the transfer of cells from primary 2,4-D containing medium to a secondary medium lacking this auxin. A logarithmic plot of average numbers of embryos per milliliter versus number of days on a medium without 2,4-D revealed a sigmoidal relationship. T h e logarithmic phase of embryo formation extended from approximately 7 to 11 days, and after a 25-day growth period a dense culture of embryos was observed. In contrast, inhibition of carrot embryo formation in secondary culture in the presence of 2,4-D has been demonstrated (Caldas 1971).A primary culture of carrot cells was subjected to a 16- to 17-day passage on 50 ml of a liquid medium containing 0.5 mg/liter 2,4-D (approximately 2.25 pM). Cells were harvested by centrifugation (150 g, 5 minutes), washed twice for 30 minutes, a third time for 2 to 2.5 hours, and
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sieved through a silk screen (approximately 100 pM pore size). T h e optimum density of the inoculum for secondary cultures was found to be 1:200 dilution (packed cell volume: final cell suspension volume). Using a gradient of 2,4-D concentrations for these washed cells in secondary culture, Caldas (1971) observed a decrease in the number of embryos a t the higher concentrations with complete inhibition a t 2 pM 2,4-D. A two-stage production of somatic embryos is common among systems using 2,4-D as the auxin: carrot (Halperin 1966), asparagus (Wilmar and Hellendoorn 1968),Zarnia intergrifolia (Norstog and Rhamstine 1967), and coffee (Sondahl and Sharp 1977). Callus growing on media with relatively high 2,4-D concentrations does not produce embryos until after transfer to a medium lacking 2,4-D, or to one with a substantially lower 2,4-D concentration, or to one with low concentrations of IAA or NAA. Similarly treated tissue grown on an IAA-containing medium and later transferred to a medium without IAA will not form embryos (Sussex and Frei 1968), although it does form embryos in the presence of IAA. Another point of difference between 2,4-D and IAA is that roots form a t 10 -W IAA and NAA, but not a t similar concentrations of 2,4-D (Norreel and Nitsch 1968). When 2,4-D is the auxin, only concentrations ranging from 5 X 10 -9M to 2 X 10 -iM are permissive to root development (Kato and Takeuchi 1966; Reinert 1968). T h e question of whether or not an auxin is required in the culture medium for embryo determination now appears to be resolved. Auxin is required for determination if IEDCs, but the PEDCs which were determined during a prior mitotic event in situ before their transfer to a cell culture environment either have no auxin requirement or require auxin only for the onset of mitosis. Upon initiation of mitotic activity, these cells then are able to fulfill their commitment to the embryogenic pattern of development. Determination of embryogenic cells during IEDC, according to all evidence in the literature, is only possible in the presence of an auxin or auxin plus cytokinin. 2. Cytokinin and CytokinidAuxin Interactions.-Cytokinins have been tested also for their effects on embryo initiation and development, and have been reported to be inhibitory in some instances. Toxicity was reported (Halperin 1964) with kinetin concentrations of 5 X 10 -6M and 9 X 10 -iM. Nitsch and Nitsch (1969) observed a reduction of androgenesis a t these same kinetin concentrations. Other than these effects, kinetin is effective in maintaining the embryo-forming potential in solid cultures of carrot for a longer period (Halperin 1966), and allows differentiation of asparagus embryos a t concentrations above 5 X 10 -7 M (Wilmar and Hellendoorn 1968). Zeatin, a t a concentration of 0.1 pM, stimulates embryogenesis in carrot suspension cultures during subculture
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onto an auxin-free medium, whereas kinetin or BAP inhibits the process (Kato and Takeuchi 1963). In Apium, kinetin a t a concentration of 0.1 mg/liter promotes embryogenesis (Halperin and Jensen 1967). Leaf explant cultures of Coffea arabica require a high kinetin to auxin ratio for high frequency embryo induction on both the “conditioning medium” with high kinetin and 2,4-D concentrations (e.g., 18.4/4.5 pM), as well as on the “induction medium” with reduced concentrations of kinetin and NAA (2.5/0.5 p M ) which is later followed by a growth-regulator-free medium for further development (Sondahl and Sharp 1977; Sondahl, Spahlinger, and Sharp 1979). 3. Gibberellin and Abscisic Acid.-Gibberellin affects the rate of embryo development, but has no effect on the frequency of embryogenesis (Nitsch and Nitsch 1969). Abscisic acid has been reported to affect either the initiation of embryo development (Norreel and Nitsch 1968) or to lower the rate of embryo development (Nitsch and Nitsch 1969). Ammirato (1977) studied the effects of abscisic acid, zeatin, and gibberellic acid on the development of somatic embryos from cultured cells of caraway (Carum carui). Here the concentration balance between abscisic acid and gibberellic acid can effectively control somatic embryo development and either disrupt or ensure normal maturation. 4. Embryogenic Inhibition Factor.-Studies to elucidate the basis for monoembryonic and polyembryonic cultivars of Citrus are important to understand the release of embryogenic determined cells (PEDCs) in the commencement of the embryogenic developmental process. This will result in an increase in the frequency of embryo yield. Esan (1973) proposed that the nucellus of Citrus contained a graft-transmissible and diffusable embryogenic inhibitor, the “Citrus factor.” The concentration of this inhibition factor was the lowest in the most polyembryonic cultivar. Furthermore, the Citrus factor was effective in suppressing asexual embryogenesis in Daucus carota, implicating a possible general significance. Subsequent studies pertain to the possible identity of the substances in Citrus that repress asexual embryogenesis (Tisserat and Murashige 1977a). The inhibition could be attributed to both volatile and nonvolatile components. Monitoring of gases produced by citron ovule sections under conditions simulating bioassays disclosed significant evolution of carbon oxide, ethylene, and ethanol. Repression of embryogenesis in nucellar tissues was not averted by trapping ethylene. However, ethanol in concentrations equivalent to those released by citron ovules dramatically suppressed asexual embryogenesis in carrot. The adverse effects of ethanol were reversed immediately upon transfer to ethanol-free medium. Other work concerning the anti-embryogenic effects of auxin, abscisic acid, and gibberellin (Tisserat and Murashige 1977b) was dis-
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closed. Analysis of Citrus ovules excised from young fruits revealed that those of monoembryonic citron contain concentrations of IAA, ABA, and GA, several times higher than those of polyembryonic Ponkan Mandarin. I t was concluded that the nonvolatile components of the inhibition might be identified with these hormone substances. Tisserat and Murashige (1977b) investigated the repression of asexual embryogenesis in uitro by 2,4-D, abscisic acid, ethephon, IAA, kinetin, and gibberellic acid. Test tissues consisted of Citrus reticulata Blanco Ponkan mandarin nucellus explants and Daucus carota callus. Embryo initiation and growth of both test tissues were markedly depressed by 2,4-D, abscisic acid, and ethephon. Slight inhibitions were obtained with IAA, kinetin, and gibberellic acid. Recovery from repressor did not occur readily in Citrus nucellus following reculture in citron-ovule-free medium. The researchers concluded that repression by natural sources apparently involved the combined action of some or all natural hormones that are generically related to the above. A further study pertaining to the effects of ethephon, ethylene, and 2,4-D on asexual embryogenesis in Daucus carota callus cells (Tisserat and Murashige 197713) was made. Ethephon inhibition of asexual embryogenesis was attributed primarily to a relatively large concentration generated by the ethephon. However, some of the repression was found to be associated with a non-volatile component. 111. DEVELOPMENTAL AND MOLECULAR ASPECTS
A. Callus Initiation A general view of callus proliferation was presented by Yeoman (1974); Hill (1967) pointed out the need for wounding explant tissue, after which cell division proceeds. Not all cells in the explant divide, and mainly those in the outer layers of tissues contribute to the developing callus. Cell division activity is dependent on growth regulator concentration, as well as the source of explant material. Yeoman recognizes four categories of explants separated on the basis of their growth regulator requirements: (1)auxin, (2) cytokinin, (3) auxin and cytokinin, and (4) absence of hormones. Callus cultures can be maintained on solid or liquid media and growth may differ under these two conditions. It is more difficult to study biochemical or developmental processes in solid cultures than in liquid cultures, because a smaller portion of the tissue is actually in direct contact with the medium and the remainder of the cells are receiving a censored version of the medium’s components. Gradients of growth regulators, nutrients, and physical parameters can exist within the mass of cells,
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making it difficult to characterize the conditions a t the location of embryo formation. Within a callus mass, it is always possible to distinguish several distinct cell populations, attributable to genetic and/or epigenetic differences. Atropa belladonna (Konar et al. 1972b) and Coffea arabica (Sondahl and Sharp 1977) are examples of mixed phenotypic populations in which cells differ in morphogenetic potential for shoot and embryo formation. Cell division in explants of carrot storage roots is induced by exogenous growth regulators. The rate of division can be increased if both kinetin and auxin are utilized, rather than with auxin alone (Linser and Neumann 1968). Protein synthesis has been detected in the freshly cut explants (AP Rees and Bryant 1971), with net RNA synthesis beginning after eight hours and continuing for four days in a simple buffer (phosphate). However, the same workers found that net DNA synthesis was not evident until 48 to 72 hours after cutting (Bryant and A P Rees 1971). This lag in DNA synthesis was not decreased by use of a nutrient medium in which carrot cells were able to divide and grow. Increases in the DNA content of explants were observed on enriched medium over a 13-day culture period. Differences in RNA concentrations between the two treatments were even more striking, since the addition of kinetin doubled the content of RNA. But the rate of 32Pincorporation by the auxin-treated tissue was still six times greater than the rate of incorporation into RNA in the kinetin plus auxin treatment. It appears that there is more stable RNA in the presence of kinetin than in its absence, when the synthesis of short-lived RNA must be relatively high. A comparison of treatments plus and minus coconut milk indicates that total nucleic acid content increased until the sixth day without coconut milk, but continued to increase up to 14 days in culture with coconut milk (Steward et al. 1964). Expressed on a “per cell” basis, the increase in DNA per cell stopped after two to four days with coconut milk and the level was constant a t three or four times the initial value. With coconut milk, there was an initial doubling or tripling in DNA per cell by the fourth day, after which the amount of DNA dropped to the initial level or lower.
B. Polarity Whether developing from single cells or cell clumps in liquid culture, carrot embryos show polarity from the very beginning of their development. An unequal division of the single cell partitions off a larger, more vacuolate cell which will remain as a suspensor-like element. T h e root of the developing embryo is always attached to the remnants of the initial cell (Backs-Husemann and Reinert 1970). Similarly, embryos may develop from multicellular clumps, which are polarized already because
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the inner cells are larger, more vacuolate, and contain more starch than the peripheral eumeristematic cells (Halperin 1967). The inner cells appear to remain associated with the suspensor, as the root end of the embryo is always attached to this clump. This becomes clearer in cases where several embryos arise from a single clump and all have their roots attached to the clump. This uniformity extends to embryos arising from epidermal cells in s i t u on the stem of R a n u n c u l u s plants (Konar and Nataraja 1965a,b),in which all the embryos are attached to the plant by their roots. The fact that both zygotic embryos and in uitro embryos develop by the same basic pattern suggests that the pattern is intrinsically controlled, with one stage providing the changed conditions which initiate the next stage. There are, of course, the very first steps of differentiation which are obvious as visible differences in ultrastructure between the two daughter cells of the first zygotic division (e.g., in cotton) (Jensen 1963), which are not explained by preexisting differences in in uitro conditions as easily as they may be in uiuo. Even after embryogenesis has been initiated, the external medium continues to influence development. For example, cell density of the carrot suspension cultures affects the stage of morphological development attained by the embryo, with progressively more dilute cultures lacking the formation of cotyledons, the elongation of the embryos, and the development of polarity (Halperin 1967).
C. Theories of Embryogenesis 1. Dedifferentiation Theory.-One of the most frequently mentioned theories is that a cell must undergo “dedifferentiation” prior to embryogenesis (Halperin 1970; Neumann 1969). Instead of dedifferentiation, we prefer the use of the terms redifferentiation or differentiation. The problem with the term dedifferentiation is that it implies a reversal of the sequence of states leading to the existing state of cytodifferentiation, while the terms redifferentiation and differentiation do not impose this restriction. Steward et al. (1958) state, “No single parenchyma cell can directly recapitulate the familiar facts of embryology, but, must go through the formation first of an unorganized tissue culture.” Halperin has expressed the need for “dedifferentiation” as a prerequisite to reaching the “embryogenic” state (Halperin 1970), the state of a cell in which it is specialized for embryo formation and will not differentiate in any other way. However, the case for dedifferentiation is not without its drawbacks (Caldas 1971). For example, two systems in which embryos are formed directly from epidermal cells of the stem or hypocotyl (Kato and Takeu-
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chi 1966; Konar and Nataraja 1965a) indicate that the epidermal cells need not dedifferentiate prior to embryo formation. It is our contention that these cells were restricted in their cytodifferentiation options during an earlier mitotic division. Moreover, it should be pointed out that in these systems probably only a subpopulation of the epidermal cells is committed to embryogenic development. These committed cells undergo a periclinal mitotic division a t the onset of embryogenesis rather than the characteristic anticlinal mitotic division typical of epidermal cells. This change in the orientation of the spindle apparatus is indicative of a commitment to embryogenesis during a previous mitotic cell cycle. Differences between epidermal cells and cortical cells of some hypocotyl explants (Kato and Takeuchi 1966) have been noted: “The cells of root or of inner tissues of hypocotyls of carrots demand a certain period of time in 2,4-D containing medium before embryogenic determination.” The need for dedifferentiation depends on the explant material used during primary culture. Epidermal cells of the stem, hypocotyl, and embryo may begin embryo development without going through a callus stage, while cortical cells and cells of xylem and phloem explants do require such a passage (Caldas 1971). Obviously, the requirement is not for dedifferentiation or redifferentiation per se, but for the obtainment of a developmental state or a sequence of such states in differentiation which are permissive to embryo formation. Cells which are capable of embryo formation have been termed embryogenic cells (Halperin 1970), with the additional restriction that embryogenic cells are specialized for, or restricted to, embryo formation. Is this actually a state of differentiation in that all the cells which are embryogenic are phenotypically similar (in the same state), or is it a group of different states, from any one of which embryos can form under appropriate conditions? The main reason for asking this question is that a single state of embryogenesis suggests that the embryogenic cell is differentiated, while in the other case, there is not particular specialization for embryo formation. There is evidence for more than one state permitting embryo formation, since embryos can arise from epidermal cells, which are already differentiated, as well as from callus cells, which even if they are differentiated are a t least different from epidermal cells. Thus it is possible that a cell without a special predisposition for embryo formation will produce an embryo if it is not influenced to follow some other path of differentiation (Caldas 1971). 2. Cell Isolation Theory.-There are several points which support the idea that embryogenesis is the path of differentiation followed when all environmental inducers and co-repressors are absent. One is the classical idea of cell isolation before embryo formation may proceed (Steward
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et al. 1964). In this case, the constraints of the neighboring cells are thought to limit the expression of the cell’s potential to a small part of the genome. Thus, the chemical products of a cell’s metabolism will influence its neighbor cell and stimulate it to a particular type of differentiation, and it is the loss of this type of communication that permits embryo formation. (There is a tendency toward isolation of the embryo sac in vivo as plasmodesmata are disrupted during expansion (Halperin 1970), which is suggestive of the same mechanism operating naturally.) This theory requires that differentiation of a specialized cell type results from either particular inductive compounds which force the differentiation, or from combinations of various conditions and compounds, such as sucrose concentrations, growth regulators, and physical factors (Sharp et al. 1971; Wetmore and Rier 1963; Brown and Sax 1962). At any rate, there is some additional factor which limits the expression of totipotency. I t is appropriate also to point out that a single cell forming an embryo will demonstrate totipotency in the sense that it contains all the genetic material for production of a new plant, but the initial cell has not, in fact, demonstrated a very wide range of differentiation potential. The initial cell in uitro, as is true for the zygote also, merely divides to form a filament or group of cells. The organization which gradually arises from repeated cell division is itself the controlling factor in differentiation of specialized cell types such as stomata, tracheids, and sieve elements. Gradients of nutrients and growth regulators arise within the developing structure and, as a result of different environments, the cells differentiate. Thus, the initial steps of embryo formation are merely cell division, not a complicated process of differentiation. 3. Explant Physiology and Culture Environment Theory.-Street (1976, 1978) has developed the concept that the induction of division (leading to callus initiation from tissue explants) does not in itself reveal the totipotency of the cells, and that this latter change depends upon the physiological state of the cells in the explant and the conditions operating during culture initiation. The importance of the physiological state of cells in the explant is strongly supported by the many instances where embryogenic cultures are most readily obtained from flower buds, embryos (particularly immature embryos), or plantlets derived from somatic embryos. Similarly, morphogenic cultures often can be obtained readily from seedling tissues, but not from those of the mature plant. Further, totipotency is not dependent upon conditions which permit its expression; highly embryogenic carrot cultures can be maintained in an auxin-containing medium which suppresses embryo development and then, a t will, embryogenesis can be initiated by transfer to an auxinfree medium (Smith and Street 1974). Similarly, cells well advanced
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upon a pathway of cytodifferentiation can spontaneously demonstrate their totipotency, as when epidermal cells of the hypocotyl of culture-derived plantlets of Ranunculus sceleratus give rise to embryos (Konar et al. 1972a). 4. Intercellular Communication and Cytodifferentiati0n.-Cytodifferentiation in uiuo takes place in the microenvironment of the cell a t its particular (and changing) location within the developing plant organ. Within this environment, cytodifferentiation is regulated by diffusion gradients of nutrients, endogenous plant growth regulators, and gaseous factors (02,COz, and ethylene and other volatile products of metabolism). Cytodifferentiation arises within the organ as the end-product of a sequence of cell divisions which may progressively alter the nuclear-cytoplasmic relationship and surface:volume ratio of the cell. A differentiating cell also must be viewed as part of a symplast being in communication with adjacent cells via plasmodesmata. Since tissue and cell cultures range from large symplastic callus masses to free cells suspended in liquid medium, they may tell us something of the importance of cell association in cytodifferentiation. However, it is impossible to establish that symplastic cell association is critical to the initiation of cytodifferentiation, because the cellular aggregate itself establishes gradients of both endogenous and exogenous growth regulators, as well as of gases comparable with those in a developing organ. One aspect of this is that the aggregate establishes a different surface: volume ratio, and hence may allow the development of higher cellular levels of critical metabolites. This is, in fact, probably combined with some degree of cell differentiation in uitro, i.e., the basis of the “nurse effect” demonstrated to be of importance in the induction of division in isolated cells (Street 1973) and in the nutrition of pre-globular embryos in systems like carrot embryogenic cultures (Street 1976). In uitro studies, such as the carrot system, have led to the concept that the cytodifferentiation is the outcome of its changing (not static) microenvironment, that the separate steps in the cytodifferentiation process have different “environmental” requirements for their completion.
5. Predetermination Theory.-Perhaps the explant and certain physiological qualities associated with it are most significant in determining whether embryo initiation can be observed. Nutrient media and other in uitro conditions serve primarily to enhance or repress the embryogenic process. This theory focuses on the idea that cells that undergo embryo initiation are embryogenetic to begin with, and that their culture in uitro simply provides the opportunity for embryogenesis to occur (Tisserat et al. 1979).
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6. Pre- and Induced Embryogenic Determined Cell Theory.-As proposed earlier, embryogenic cells can be divided into two categories: (1) pre-embryogenic determined cells (PEDC) in which the cells were determined during prior mitotic divisions, and (2) induced embryogenic determined cells (IEDC), wherein cells reenter the mitotic cell cycle and redifferentiate to embryogenic precursor cells or embryogenic mother cells (EMC) which then develop into embryogenic cells. The latter lead to embryo development by polarized cell divisions typical of the embryogenic developmental sequence (globular, heart, and torpedo stages).
D. Pre-Embryogenic Determined Cells (PEDC) 1. Citrus Nucellus.-The natural occurrence of polyembryony in many species of Citrus (Bacchi 1943; Webber 1940) and its economic importance have long been realized (Webber 1931). Thus, not only a zygotic embryo, but also several adventive embryos may be found within a single seed. These adventive embryos have been shown to originate in single cells of the nucellus, near the micropyle of the ovule, and appear to be initiated after fertilization, soon before or after the first zygotic division (Bacchi 1943). In addition to the natural occurrence of nucellar polyembryony, in uitro cultures of nucellar explants may give rise to embryos and eventually to fully developed plants (Ranga Swamy 1958, 1961; Kochba et al. 1972). Nucellar tissues from both unfertilized as well as fertilized ovules may undergo embryogenesis in uitro (Button and Bornman 1971; Mitra and Chaturvedi 1972). Cultures of monoembryonic cultivars like ‘Shamouti’ also have been shown to be embryogenic (Rangan et al. 1968, 1969; Button et al. 1974). Early characterization of embryogenesis in nucellar cultures consists of an initial proliferation of callus and subsequent development of “pseudobulbils” in the absence of exogenous plant growth regulators (Ranga Swamy 1958). Some of these pseudobulbils continue embryogenic development and eventually become entire plantlets. However, in other experiments with several cultivars of normally monoembryonic species, callus and pseudobulbil formation were not prerequisite to embryo development, and embryos arose directly from nucellar tissue (Button and Bornman 1971). Mitra and Chaturvedi (1972) reported that embryos may arise directly from the nucellus, or indirectly from nucellar callus. Many of these experiments include growth regulators such as NAA and kinetin, as well as complex addenda like malt or yeast extract and coconut milk. These may be beneficial in increasing the frequency of observed embryos. However, it must be stressed that embryogenesis may be observed in the absence of these components. Button et al. (1974) characterized embryogenesis in habituated nucellar callus cultures. This callus was found to be composed not of unor-
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ganized parenchymatous tissue, but solely of numerous proembryos. Embryogenesis has been observed to occur from single cells in the periphery of the callus, as well as from existing proembryos. Some of these developing embryos may enlarge only to a globular stage, commonly referred to as “pseudobulbils.” These rarely develop into plants. Other proembryos follow the developmental sequence characteristic of zygotic embryogenesis and eventually develop into plants. The fact that this callus was habituated, i.e., autonomous for exogenous growth regulators, in no way decreased its embryogenic potential. That the presence of exogenous growth regulators actually depressed embryogenesis lends further support to the concept that exogenous growth regulators may be viewed best as inductive agents for determination. It is our view that embryogenesis from nucellar tissues, both in uiuo and in uitro, may be considered best as cases of PEDC-mediated embryogenesis. The cells of the nucellus are actually preembryogenic determined cells (PEDCs), and their proliferation as a callus mass and subsequent embryogenesis may be viewed best as simply the cloning of these PEDCs. Thus, it appears that embryogenesis in the nucellus is autonomous and may be observed even in the absence of exogenous growth regulators. Although low concentrations of kinetin and NAA have been shown to be beneficial, they are not absolute requirements for embryogenic determination. Exogenous growth regulators probably contribute to the cloning of these PEDCs, thus increasing the relative number of embryogenic cells. Of course, it is also possible that an additional population of induced cells (PEDCs) further contribute to the relative number of embryos. Other Examples of PEDC.-Spontaneous origin of viable embryos from the superficial cells of plantlets arising in culture uia embryogenesis has been reported where somatic embryos originate in uitro without an intervening callus stage. This now has been observed in Atropa belladonna (Rashid and Street 19731, carrot (McWilliam et al. 1974),Datura innoxia (Geier and Kohlenbach 1973), Ranunculus scelaratus (Konar et al. 1972b), and Brassica napus (Tomas et al. 1976). In Ranunculus scelaratus and Brassica napus it has been established that these embryos arise from single cells of the shoot-axis epidermis. Here, as in the natural or rare origin of embryos from synergids and antipodal cells of the embryo sac, the competence for embryogenesis is retained in cells of specialized function. This raises the possibility that differentiation-or a t least some pathways of differentiation-and competence to embark upon morphogenesis are not necessarily incompatible (Street 1979). 2.
E. Induced-Embryogenic Determined Cells (IEDC) The concept of IEDC explains the redetermination of differentiated cells to the embryogenic pattern of development. Evidence exists that
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the auxin or auxinlcytokinin concentration in the primary culture medium or conditioning medium is critical not only to the onset of mitotic activity in non-mitotic differentiated cells but to the epigenetic redetermination of these cells to the embryogenic state of development. A statement characterizing the role of growth regulators in gene expression as direct or indirect cannot be made. Regardless of how growth regulators control gene expression, evidence exists that the auxin, 2,4-D, elicits a response a t the transcriptional and translational levels during primary culture. Subsequently, an additional response a t the transcriptional and translational levels occurs shortly after subculture onto a secondary or induction medium (Sengupta 1978; Sengupta and Raghavan 1979). Numerous examples of IEDC have been reported in the literature in which embryogenic cells, resulting from cellular redetermination, proceed through the various stages of embryo development and form plants. Development of the embryogenic determined cells is usually restricted during culture on the primary or conditioning medium. Thereafter cells need to be subcultured onto a secondary culture medium for induction or continuation of development in the embryogenic determined cells. The latter medium is usually referred to as an induction medium. Documented examples of IEDC have been reported in the literature for the following taxa: Macleaya cordata, Kohlenbach (1965,1966); Cichorium endiuia L., Vasil and Hildebrandt (1966); Daucus carota, Halperin (1969), Reinert, Bajaj, and Zbell (1967), Kamada and Harada (1979a); Atropa belladonna L., Konar, Thomas and Street (1972b); Petunia hybridia, Rao, Handro, and Harda (1973); Cucurbita pep0 L., Jelaska (1974); Corylus auellana L., Radojevic, Vujicic and Neskovic (1975); A p i u m graueolens, Williams and Collin (1976); Nigella satiua L., Banerjee and Gupta (1976); Vitis uinipera L., Krul and Worley (1977); A s paragus officinalis, Reuther (1977); Iris spp., Reuther (1977); Carum carui L., Ammirato (1977); A p i u m graueolens L., Zee and Wu (1979); Gossypium klotzschianum, Anderss, Price and Smith (1979); Theobrom a cacao L., Pence, Hasegawa, and Janick (1979); Solanum melongena L., Matsuoka and Hinata (1979); Phoenix dactylifera, Reynolds and Murashige (1979); Coffea arabica, Sondahl, Spahlinger, and Sharp (1979). Androgenesis and gynogenesis involve the development of IEDCs, although it is beyond the scope of this review to present a detailed account of embryogenesis in haploid cells. In these instances, either the microspore or megaspore must undergo a quantal mitotic division, resulting in an embryogenic determined cell. In the former, a quantal mitotic division results in a generative cell and a vegetative cell. The vegetative cell, or in some instances the generative cell (Raghavan 19761,or a fusion
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cell is determined as an embryogenic mother cell (Sunderland 1974, 1977; Sunderland and Dunwell 1977; Nitsch 1975). F. The Mitotic Cell Cycle and Embryo Determination
Each phase of the cell cycle (G1,S, GP, and M) contains a specific synthetic machinery which is under regulatory control. The time duration of S and M are fairly constant in a given tissue system while G1 and Gz are variable. The principle control points of the mitotic cell cycle are situated in G1 and GP.GI generally is considered to be the control point for S, while GPis the control point for M. Determinative events preceding cytodifferentiation generally are thought to occur during either G1or S, although GPmay be important in some systems. We postulate that specific exogenous growth regulator concentration(s) or concentration ratios in the culture medium have a dual role in the onset of embryogenesis. First, growth regulators are responsible for the initiation of cell division, i.e., reentry of cells into the mitotic cell cycle from Go (a special nonoperational state of the cell cycle) or either the GI or GPprincipal control points (Van’t Hof and Kovacs 1972; Van’t Hof 1974). Second, growth regulators have either a direct or indirect role in the control of cytoplasmic factodd synthesis during GI and GP. These factors are probably responsible for the basic histones and acid nuclear proteins during S phase, resulting in a differential masking or unmasking of genes of the daughter DNA strands. These daughter strands would have different DNA template sequence availabilities for the synthesis of RNA and during the M period, a t the time of cytokinesis. a quantal mitotic division would occur resulting in two phenotypically unlike daughters committed to different developmental patterns. Histone synthesis doubles during the S period of the mitotic cell cycle and generally is thought to be restricted to S, although there are exceptions to this (Mitchison 1971). The restriction of histone synthesis to the S period is consistent with a different hypothesis, i.e., that histones are synthesized continuously through the cycle in the cytoplasm but are incorporated into the nucleus and onto the chromosomes when the new DNA is being synthesized during S. Chromatin of low template activity is rich in histones (Bonner 1965); chromatin of high activity is rich in acidic chromatin proteins. This would accord with the hypothesis that the histones are non-specific repressors and that the acid chromatin proteins (of which there are a large number) are specific derepressors of gene expression. Here then is raised the possibility that major changes in DNA template activity could be affected as well as could interactions of cytoplasm, and nucleus during the S phase could exercise a determinative influence on subsequent gene expression and hence on the course of cytodif f erentia tion.
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The changing patterns of enzyme activity observed during the cell cycle of higher plant cells (Yeoman 1974; King et al. 1974) are due to the operation of feedback controls and changes in the translation of functional structural genes. I t may, therefore, be postulated that the availability of the genome for transcription is under the control of regulatory genes and that the critical events in S-phase relative to cytodifferentiation relate to the activation or suppression of such regulatory genes. This a t present is pure hypothesis (Street 1978). I t should be understood that preceding cell divisions may influence subsequent differentiation (Fosket 1970, 1972; Sussex et al. 1972; Meins 1975): events in cycling cells may determine or limit the subsequent pathways of cytodifferentiation upon which the cells can embark. There may be a long time interval separating a regulatory cell division and the appearance of visible signs of cytodifferentiation. The presumption is that during a quanta1 cell division one of the daughter cells remains meristematic, whereas the other is determined under a proper set of environmental conditions to become an embryogenic mother cell. Examples of cytodifferentiation without any further cell division cited against the involvement of the cell cycle in differentiation (tracheary elements, immature parenchyma cells of leaves of Camellia japonica, etc.) are not justified since these cells obviously were determined during an earlier mitosis. In such studies it is necessary to be aware of the fact that differentiated cells may in fact not be arrested a t a point in the operational cell cycle, but in a special state of cytodifferentiation which has been termed Go (Lajtha 1967), the release from which may involve different stimuli from those which release cells in GI or Gz arrest. Here it is important to develop the concept of multiple phenotypic populations in plant tissue cultures. Explant materials used for the establishment of primary cultures usually consist of an array of phenotypic cellular populations which can be characterized on the basis of cellular morphology, biochemical characteristics, and mitotic cell cycle time. These cells have different developmental destinies imposed upon them because of their different DNA template sequence availabilities. Furthermore, some of these cell populations are actively dividing while others are in mitotic arrest (Go, GI, or G2). Using 3H labeling and autoradiography, Webster and Davidson (1968) identified the presence of 3 cell populations in root meristems of Vicia faba: (1)a rapidly dividing population with a cell cycle time of 14 hours (approximately 50% of meristem); (2) a second population with a cell cycle time of 30 hours (27 to 43% of the meristematic cells); and (3) a remaining cell fraction that divides rarely or not a t all (the quiescent center cell). Although the authors do not identify the position of the different populations, the quantitative heterogeneity with respect to
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mitotic activity contributes to our understanding of the functional organization of the meristem. The differences in mitotic cycle times existing within a meristem and the localization of different cycle times provide evidence, if not of differentiation, then of closely controlled programming of the columns of cells in the meristem. In an elegant experiment presented by Friedberg and Davidson (1971), two subpopulations of cells were recognized a t an early stage of lateral root formation. Root tips of Vicia faba were treated with colchicine (0.003%)for 3 hours and only the dividing cells became polyploid. Using polyploidy as a marker, they found that a t an early stage of lateral root differentiation, the central core of cells divided actively (polyploid cells) and the peripheral core cells were arrested (diploid cells). The central core remained mitotically active almost up to the time of lateral root primordium emergence from the primary root, thus contributing to the early growth of the primordium. A t the time of primordium emergence (approximately 5 days), the central core of cells stopped dividing (arrested in G1 phase) and the peripheral cells divided actively for approximately 48 hours; a t day 8, the central cells resumed mitotic activity again, and most of the peripheral cells became arrested. The authors point out the importance of this temporary shift in mitotic cell populations: (1) adjacent cells behave differently a t the course of lateral root primordium development with a reverse in mitotic activity; (2) the peripheral cells are the ones that contribute to the development of root cap; and (3) changes in the mitotic cycle probably precede biochemical or morphological specialization. Experimentation with root tips of eight different species further links cellular differentiation with events in the mitotic cell cycle (Van’t Hof 1974). The meristematic cells of root tips become arrested following carbohydrate starvation either in G1 or Gz, in different proportions, but never in S or M. Cellular meristem populations of different species have a different comportment upon mitotic arrest; Helianthus sp. differs from Vicia faba in having 77% cells arrested in G1 and 21%in Gz. This finding is in agreement with the tendency for cells to be arrested during dormancy (radicle of seeds) and in mature cells’ tissues. At a distance of 20 mm above root tip, mature cells of Helianthus arrested in G1(91%)and GP (2%)and for V. faba, 22% in G1 and 63% in Gz. Two principal control points in the mitotic cell have been postulated with one in G1 and another in Gz (Van’t Hof 1974). DNA synthesis and mitosis do not take place until the requirements of the control points are met. In other words, a cell arrested in G1or GZis not necessarily prepared to enter S or M. Apparently, the principal control points involve a “. . . sequential enzyme synthesis or activation,” but this needs to be corroborated. Experimental work indicates that protein inhibitors impede
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the progression of cells to S or M, and it is entirely possible that multiple arrest points exist in both GI and Gz. The time delay for entry into S and M has been measured and found to be variable in four different species (Van’t Hof 1974). I t is not certain as to what extent cell arrest a t specific points of the cell cycle is species specific or population specific or both. From the studies presented so far it is possible to conclude that GI and GZ are the most critical phases in the division process of cells. These two phases are the most variable phases of the mitotic cell cycle and evidence has been presented that “critical commitments” to differentiation are made during GI and Gz which will affect the next round of the division cycle (Mitchison 1971). The decision to proliferate and the fate of daughter cells following mitosis have been suggested to occur a t these critical points, but conclusive data still are not available. We would be naive to expect a specific growth regulator concentration to necessarily have a uniform effect on assorted phenotypic populations of cells. Rather, we would expect a particular growth regulator concentration or concentration ratio to affect mitosis and/or redetermination of a particular phenotypic cellular population. Therefore, it is suggested that the embryogenic mother cells of IEDCs are descendants of a population of cells receptive to a critical embryogenic-inducing growth regulator concentration or a concentration ratio of growth regulator substances (auxin/cytokinin). Such cells are redetermined as to their developmental commitments during a quanta1 mitotic division in uitro which results in two daughters, one of which is probably the embryogenic mother cell. The determinative events for PEDCs, of course, occur in sito prior to the transfer to a tissue culture environment. It appears that growth regulators (in particular 2,4-D or 2,4-D and kinetin) have two functions in the conditioning culture medium (primary culture medium): (1) determination of the embryogenic mother cells (EMC) and (2) synchronization of EMCs. Thereafter, this cellular population most likely resides in a state of mitotic arrest until subculture to an embryogenic induction medium, where 2,4-D is removed from the culture medium. This probably allows for the release of the EMC from mitotic arrest and subsequent embryo development. Instances of embryogenic development during primary culture on the conditioning medium have been reported (Sondahl and Sharp 1977), and this is referred to as low frequency embryogenesis (LFSE) (Sondahl and Sharp 1977; Sondahl, Spahlinger, and Sharp 1979). LFSE is explained on the basis of the existence of a “leaky” population of EMC being released from mitotic arrest and the commencement of embryogenesis in the presence of 2,4-D (Fig. 6.1). This also applies to embryogenesis in carrot growing on 0.05 pM of 2,4-D. The existence of low frequency embryogenesis and the probable existence of a population of “leaky” embryogenic cells are offered as
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L
COFFEE LEAF EXPLANTS
+2.4-0
RELEASE OF BLOCKAGE
1
+2,40
CELLULAR SUBPOPULATION ”LEAKY”
-
further support for the hypothesis that determination of EMC occurs during primary culture on a conditioning medium. The characterization of “leaky” cells of root meristematic tissues during the mitotic cell cycle arrest resulting from sugar starvation has been well corroborated by Van’t Hof (1974). Development of the somatic embryos in clumps of HFSE in Coffea is asynchronous. Perhaps the formation of these clusters of somatic embryos can be explained on the basis of an altered pattern of cell segmentation in the committed cells of the callus mass on “induction medium” in the absence of 2,4-D, as discussed by Street and Withers (1974) in the induction of embryogenesis in Daucus carota. Clusters of embryos characteristically are released from the callus mass a t the early globular stage of development and are readily observed developing in the surrounding
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medium. Staritsky (1970) reported similar observations pertaining to cultured orthotropic shoot tissues of C. canephora. T h e fact that HFSE is so effectively triggered in 60% of the cultures by 2,4-D in combination with kinetin during primary culture is striking (Sondahl and Sharp 1977). Other sources of auxin (IBA and NAA) in combination with kinetin are not as effective in the induction of HFSE (10 to 20%). However, NAA in combination with kinetin induces LFSE in up to 60% of the cultures. The removal of 2,4-D, addition of NAA, and reduction of kinetin concentration in the induction medium during secondary culture were essential to the development of HFSE somatic embryos in Coffea spp. T h e effective and preferential role of 2,4-D in triggering the developmental sequences leading to HFSE cannot be fully explained a t present. However, it is possible that 2,4-D induces differentiation of a distinct population of cells according to one of the following phenomena: (1)proliferation of a unique phenotypic population from the original explant (cambium, secondary phloem, etc.); (2) lengthening of the mitotic cell cycle time of a particular cell population by interference with one or more control points and redetermination; (3) determination and arrest of a distinct population of cells in the cell cycle with a blockage of GI or G2 or Go. More experimental work is needed to explain the effective physiological difference between 2,4-D and NAA in the determination of somatic cells in coffee leaf tissues. There is little information in the literature relating growth regulators to activities of the cell cycle. MacLeod (1968) reported that kinetin causes a blockage a t the G1/S interface and suggested that kinetin may affect the oxidation of carbohydrates by inhibiting glycolysis and consequently increase carbohydrate oxidation through the pentose shunt. Neumann (1968) came to similar conclusions when he observed t h a t carrot tissues with active cell division promoted by kinetin had a lower oxygen consumption rate than tissues growing without kinetin. H e suggested that kinetin was an inhibitor of aerobic respiration in the carrot tissues. Differentiated cells from carrot explants can redifferentiate after a period of cell division into embryo-competent cells (Linser and Neumann 1968). High rates of mitotic activity in carrot can be achieved by addition of inositol, IAA, and kinetin (Linser and Neumann 19681, or 2,4-D (Halperin 1964), or coconut milk (Steward et al. 1963; Reinert 1959) to the nutrient medium. The rate of cell proliferation decreases following subculture onto a 2,4-D-free medium. T h e transcription and translation processes of the different cellular populations comprising the callus tissues are obviously differentially affected in regard to their cell cycle phase intervals on different culture media. Linser and Neumann (1968) suggest that growth regulators added to the culture medium probably control morphogenesis indirectly or non-
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specifically through the control of cell division and cell aging. I t is interesting to note that aging of callus, omission of sucrose from medium, or gamma irradiation are reported to stimulate embryogenesis in unfertilized ovule tissues of Citrus sinensis ‘Shamouti’ (Kochba and Button 1974; Spiegel-Roy and Kochba 1973). Bayliss (1977) reported a positive correlation between increasing 2,4-D concentration and increasing the mean generation time in carrot cell suspension. I t also was found that the mitotic duration increased and the mitotic index decreased with increasing 2,4-D concentrations (0.5 to 70 pM). These results were partially interpreted as a blockage or lengthening of G1 and Gz and the lengthening of prophase and metaphase relative to anaphase and telephase. I t is interesting that in carrot somatic embryogenesis occurs only after removal of 2,4-D and that concentrations as low as 0.1 pM inhibit embryo development (Bayliss 1977). Peaks in peroxidase activity are associated with the appearance of somatic embryos in orange ovular tissues. An isoenzyme analysis of these tissues reveals a cathodic band to be distinctly associated with the embryogenic process (Kochba et al. 1977). Shortening of GI and an increase in peroxidase activity were described by Gupta and Stebbins (1969) in association with development of hooded barley primordia. It is possible that HFSE in Coffea leaf callus is induced by a resetting of enzyme patterns (peroxidases, etc.) during blockage of a certain population of cells in GI or Gz by 2,4-D during the primary culture. After subculture onto the induction medium, the -2,4-D medium, callus proliferation ceases and mitosis occurs in previously arrested embryogenic cells. Another approach is to study enzymes with a characteristic pattern of synthesis during the mitotic cell cycle in conjunction with the process of differentiation by looking for variations in the pattern of enzyme synthesis. This approach is difficult because of the absence of synchrony within cellular populations. Enzyme activity fluctuations during the cell cycle in plant suspension cultures have been discussed by Aitchinson and Yeoman (1974a,b) and Yeoman and Aitchinson (1976). They reported that thymidine kinase, thymidine monophosphate kinase, and DNA polymerase activities increased just a t the onset of S period. On the other hand, glucose-6-phosphate dehydrogenase (G-6PDH) has an increased activity during G1.
G. RNA and Protein Synthesis in Carrot Although the potential for embryogenic induction of carrot cells has been investigated extensively under a variety of experimental conditions (Reinert e t al. 1977), the only detailed investigation thus far undertaken
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pertaining to the biosynthetic pattern of cells during early stages of embryogenic induction is that reported by Sengupta and Raghavan (1979). Reinert et al. (1973) and Matsumoto et al. (1975) observed a difference in template activity of chromatin isolated from carrot cells growing in the presence and absence of 2,4-D. Matsumoto et al. (1975) observed an increase in template activity in carrot cells 14 days following transfer to -2,4-D culture medium. They correlated this observation with the onset of embryogenic determination rather than release from mitotic arrest and subsequent development of previously determined cells because of the elimination of 2,4-D from the culture medium per se. In these studies, while no quantitative nor qualitative differences were observed in the histones extracted from cells cultured on 2,4-D- and -2,4-D-containing medium, differences in the non-histone proteins were evident as early as 2 days following auxin omission. These changes in the non-histone proteins were due presumably to changes in template activity. Correlations between template activity of chromatin, the capacity of non-histone proteins to restore histone-inhibited RNA synthesis, and tissue specificity in the promotion of transcription have been noted also in animal systems (Wang 1968a, 1971; Spelsberg and Hnilica 1969.) So it is reasonable to think that changes in the non-histone proteins are due presumably to changes in template activity. These non-histone proteins appear to be important in the regulation of transcription during the carrot embryogenic process. Electrophoretic variations have been reported for glutamate dehydrogenase and other isoenzymes isolated from carrot cells grown in the presence or absence of 2,4-D (Lee and Dougall 1973). These changes of isoenzyme pattern are best understood by assuming a hormonal effect on terminal gene expression. Based on this previous work, a detailed biochemical analysis of the early stages of embryogenic induction in carrot cell suspensions was pursued by Sengupta and Raghaven (1980a,b). Questions posed during the course of this research were as follows: What changes in the macromolecule synthetic pattern occur during the transition of nonembryogenic carrot cells to embryos? Can these changes be related to the time of embryogenic induction? Is embryogenic induction in carrot cell suspensions following the removal of 2,4-D controlled a t the transcriptional or translational level? Answers to these questions would allow for an understanding of whether the presence of 2,4-D in the medium has a role in embryogenic induction, or if the sole function of 2,4-D is initiation of callus proliferation. Results of this study on the macromolecular changes occurring during the induction of somatic embryogenesis in carrot cell suspension culture are summarized as follows (Sengupta 1978; Sengupta and Raghavan 1979, 1980a,b).
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(1) Forty-eight hours following transfer to fresh media, the rate of cell division, as well as total RNA and protein contents, is higher in cells growing in a medium without auxin as compared to cells growing in the presence of auxin. (2) T h e specific activity of :IH in RNA and protein in the embryogenic cells incubated continuously in "-adenosine and "H-leucine, respectively, is lower than in the nonembryogenic counterpart within the first four to six hours of transfer to medium. ( 3 ) During the first 1 2 hours after transfer of cells to media with and without auxin, the rate of RNA synthesis measured by the precursor pool method is higher in the embryogenic cells than in the nonembryogenic cells. T h e specific activity of :'H in the A T P pool in the embryogenic cells was higher than in the nonembryogenic cells by 4 to 10%. (4) RNA synthesized by embryogenic cells during the early hours of transfer to the fresh medium has a higher turnover value than RNA synthesized by nonembryogenic cells of the same age. (5) T h e rate of protein synthesis as measured by pulse labeling with :'H-leucine is higher in the embryogenic cells than in their nonembryogenic counterpart during the first 1 2 hours of growth in the fresh media. (6) T h e rate of DNA synthesis after 24 hours of culture is higher in the embryogenic cells than in nonembryogenic cells of the same age. (7) T h e rate of rRNA synthesis is higher in nonembryogenic cells than in embryogenic cells. ( 8 ) T h e rate of poly(A)+RNA synthesis sharply increases (12 to 40%) upon the transfer of cells to 2,4-D-depleted medium. (9) Using a double labeling technique, it was found that poly(A)+RNA in the range of approximately 1 6 s to 1 2 s is synthesized in a greater amount in embryogenic cells than in nonembryogenic cells as early as 3 to 6 hours following transfer to 2,4-D-depleted medium. By 24 hours the poly(A)+RNA in the entire range of 16A to 5s is synthesized in a greater amount in the embryogenic cells than in the nonembryogenic cells. (10) Actinomycin D, a t a concentration of 100 mg/liter, inhibits protein and RNA synthesis in both embryogenic and nonembryogenic cells by 30 to 40%. Cordycepin, a t a concentration of 25 mg/liter, completely blocks cellular protein synthesis and inhibits embryo formation, while a lower concentration (10 mg/liter) is ineffective in inhibiting protein synthesis and has no inhibitory effect on embryo formation. However, embryos in the latter treatment are arrested in the early stages of development. Cordycepin also is found to effectively inhibit poly(A)+RNA synthesis in carrot cell cultures.
Based on the results of these experiments, a speculative hypothesis to explain control of embryogenic induction in carrot cell suspension is presented in Fig. 6.2. Results obtained in this work lead to the tentative
PHYSIOLOGY OF IN VITRO ASEXUAL EMBRYOGENESIS
+
299
CALLUS CELL SUSPENSION
CALLUSGROWTH,AND REPLICATION
TRANX,RIPTION
RNA FOR
RNA FOR CALLUS GROWTH AND REPLICATION
lNDUCTloN
Inat translated71
1 1
1
TRANSLATION
PROTEIN FOR CALLUS GROWTH AND REPLICATION
I &
MODIFICATION OF PRE TRAN SCRIBED RNA TO
OF RNA
POLY (A1 + RNA SYNTHESIS
1 1 1
TRANSLATION
PROTEINS
1
EARLY STAGES OF EMBRYOGENESIS
PROTEINS
LATER STAGES OF EMBRYOGENESIS
Adapted from Sengupta (1978)
FIG. 6.2. SCHEME FOR THE CONTROL OF SOMATIC EMBRYOGENESIS IN CARROT CELL SUSPENSION CULTURES
conclusion that embryogenic induction in carrot cell suspensions initiated by the removal of 2,4-D from the culture medium is probably controlled a t both the transcriptional and translational levels. Cells growing in the presence of 2,4-D possibly could synthesize RNA involved in embryogenic induction in addition to the synthesis of RNA and protein for cellular maintenance and growth. However, the translation of RNA synthesized in conjunction with embryogenic induction probably does not occur until the removal of 2,4-D. Most likely, the original transcript synthesized in the 2,4-D-containing medium is modified when cells are transferred to -2,4-D medium. Modification of the original transcript (HnRNA) simply may involve cleavage to mRNA, poly-adenylation, or a modification in the 5' terminal CAP. I t also is possible t h a t attachment of the RNA molecules to ribosomes does not take place until the 2,4-D concentration is lowered. Also, it is possible t h a t the RNA necessary for embryogenic induction synthesized in the presence of 2,4-D is masked, and that unmasking occurs only when 2,4-D is removed from the medium. T he initial increase in protein synthesis observed upon removal of 2,4-D from the medium should involve increased ribosome synthesis.
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However, cells are found to have a lower rate of rRNA synthesis compared to nonembryogenic cells. Since 2,4-D is known to have a non-specific stimulatory effect on rRNA synthesis, any increase in rRNA to provide ribosomes for increased protein synthetic activity remains undetected due to the difficulty of distinguishing among ribosomes engaged in the synthesis of different types of proteins. Besides triggering the translational process, removal of 2,4-D from the medium also triggers the transcriptional process. T h e result is an increase in poly(A)+RNA synthesis. Even though it is difficult to determine whether an increase in poly(A)+RNA synthesis is due to the synthesis of new poly(A)+RNA or to a stimulation in the synthesis of an already existing poly(A)+RNA or due to the polyadenylation of preformed RNA, it is reasonable to conclude that changes in the rates of synthesis of poly(A)+RNA might reflect changes in mRNA metabolism. Since blocking poly(A)+RNA synthesis with cordycepin does not inhibit protein synthesis, it seems that the proteins synthesized during the early hours of 2,4-D omission are not products of newly synthesized poly(A)+RNA. Experiments using cordycepin also indicate that translational products of RNA transcribed in the presence of 2,4-D are involved in the early stages of embryo development, while the translational products of the newly synthesized poly(A)+RNA have a role in the later stages of embryo development. IV. CONCLUSIONS
Somatic embryogenesis can be divided into the categories of PEDC and IEDC. PEDC pertains to embryogenic mother cells (EMC) or zygotic equivalents determined during a previous embryogenic mitotic cell cycle, while IEDC pertains to the situation in which cells reenter the mitotic cell cycle and redifferentiate into EMC. Plant growth regulators (auxin or auxin and cytokinin) are regarded to be the primary agents of determination in IEDC, while in PEDC the growth regulators are regarded as activators of development. T h e growth regulators can be important in determination, activation, and cloning, as well as the arrestment of embryogenic determined cells. Although evidence in carrot and coffee clearly points out the importance of growth regulatods) in the embryogenic determination process, the actual induction of embryogenic development occurs only following removal of auxin (2,4-D) from the culture medium. This process probably occurs a t both the transcriptional and translational levels. Further investigation a t the cellular and molecular levels pertaining to determination of embryogenic cells and the induction of embryogenic development is essential to our understanding of the phenomena of somatic embryogenesis and the successful occurrence of high frequency embryogenesis in other crops of economic importance.
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V. LITERATURE CITED AITCHISON, P.A. and M.M. YEOMAN. 1974a. T h e use of 6-MP to investigate the control of glucose-6-phosphate dehydrogenase levels in cultured artichoke tissue. J Expt. Bot. 24:1069-1083. AITCHISON, P.A. and M.M. YEOMAN. 197413. Control of periodic enzyme synthesis in dividing plant cells. p. 251-263. In G.M. Padilla, I.L. Cameron and A. Zimmerman (eds.) Cell cycle controls. Academic Press, New York. AMMIRATO, P.V. 1977. Hormonal control of somatic embryo development from cultured cells of caraway. Plant Physiol. 59579-586. AP REES, T . and J.A. BRYANT. 1971. Effects of cycloheximide on protein synthesis and respiration in disks of carrot storage tissue. Phytochemistry 10:1183-1190. BACCHI, 0. 1943. Cytological observations in Citrus. 111. Megasporogenesis, fertilization, and polyembryony. Bot. Gaz. 105:221-225. BACKS-HUSEMANN, D. and J. REINERT. 1970. Embryobildung durch isolierte einzelzellen aus gewebekulturen von Daucus carota. Protoplasma 70: 49-60. BANERJEE, S.and S. GUPTA. 1976. Embryogenesis and differentiation in Nigella satiua leaf callus in uitro. Physiol. Plant. 38:115-120. BAYLISS, M.W. 1977. T h e effects of 2,4-D on growth and mitosis in suspension cultures of Daucus carota. Plant Sci. Letters 8:99-103. BECCARI, E., G. D’AGNOLO, G. MORPURGO, F. POCCHIARI, and R. RICCI. 1967. Effetto dello ione ammonio sul metabolismo del glucosio in cellule di Daucus carota. Ann. Znst. Super. Sanita 3: 184. BONNER, J . 1965. T h e molecular biology of development. Clarendon Press, Oxford. BORTHWICK, H.A. 1931. Development of the macrogametophyte and embryo of Daucus carota. Bot. Gaz. 92:23-44. BROWN, C.L. and K. SAX. 1962. The influence of pressure on the differentiation of secondary tissues. Amer. J. Bot. 49:683-691. BRYANT, J.A. and T . AP REES. 1971. Nucleic acid synthesis and induced respiration by disks of carrot storage tissue. Phytochemistry 10:1191-1197. BUTENKO, R.G., B.P. STROGONOV, and Z.A. BABAEVA. 1967. Somatic embryogenesis in carrot tissue culture under conditions of high salt concentrations in the medium. Dokl. Akad. Nauk. SSSR 175:1179-1181. BUTTON, J . and C.H. BORNMAN. 1971. Development of nucellar plants from unpollinated and unfertilized ovules of the Washington navel orange in uitro. South Afr. J Bot. 37:127-134. BUTTON, J., J . KOCHBA, and C.H. BORNMAN. 1974. Fine structure of and embryoid development from embryogenic ovular callus of ‘Shamouti’ orange (Citrus sinensis osb.). J. Expt. Bot. 25:446-457. CALDAS, L.S. 1971. Effects of various growth hormones on the production of embryoids from tissues culture of the wild carrot, Daucus carota L. PhD Dissertation, T h e Ohio State University, Columbus.
302
HORTICULTURAL REVIEWS
CALDAS, R.A. 1971. Purification and characterization of glutamine synthetase from suspension culture of wild carrot (Daucus carota L.). PhD Dissertation, The Ohio State University, Columbus. DE FOSSARD, R.A. 1974. Terminology in haploid work. p. 403-410. In K. J. Kasha (ed.) Haploids in higher plants. Univ. of Guelph Press, Guelph. DUNSTAN, D.J., K.C. SHORT, and E. THOMAS. 1978. The anatomy of secondary morphogenesis in cultured scutellum tissues of Sorghum bicolor. Protoplasma 97 1251-260. ESAN, E.B. 1973. A detailed study of adventive embryogenesis in the Rutaceae. PhD Dissertation, University of California, Davis. FOSKET, D.E. 1970. The time course of xylem differentiation and its relation to deoxyribonucleic acid synthesis in cultured Coleus stem segments. Plant Physiol. 46:64-68. FOSKET, D.E. 1972. Meristematic activity in relation to wound xylem differentiation. p. 33-50. In M.W. Miller and C.C. Kuehnert (eds.) The dynamics of meristem cell population. Plenum Press, New York. FRIEDBERG, S.H. and D. DAVIDSON. 1971. Duration of S phase and cell cycles in diploid and tetraploid cells of mixoploid meristems. Expt. Cell Res. 61:216-218. GAUTHERET, R.J. 1966. Factors affecting differentiation of plant tissues grown in uitro. p. 55-71. In W. Beerman (ed.) Cell differentiation and morphogenesis. North Holland Publishing Co., Amsterdam. GEIER, T . and H.W. KOHLENBACH. 1973. Entwicklung von embryonen und embryozem kallus aus pollen kornein von Datura meteloides und Datura innoxia. Protoplasma 78:381-396. GREGOR, D., J. REINERT, and H . MATSUMOTO. 1974. Changes in chromosomal proteins from embryo induced carrot cells. Plant Cell Physiol. 15: 875-881. GUPTA, V. and G.L. STEBBINS. 1969. Peroxidase activity in hooded and awned barley a t successive stages of development. Biochem. Genet. 3:15-34. HALPERIN, W. 1964. Morphogenetic studies with partially synchronized cultures of carrot embryos. Science 147:408-410. HALPERIN, W. 1966. Alternative morphogenetic events in cell suspensions. Amer. J. Bot. 53:443-453. HALPERIN, W. 1967. Population density effects on embryogenesis in carrot cell cultures. Expt. Cell Res. 48:170-173. HALPERIN, W. 1969. Ultrastructural localization of acid phosphatase in cultured cells of Daucus carota. Planta 88:91-102. HALPERIN, W. 1970. Embryos from somatic plant cells. Symp. Intern. SOC. Cell Biol. 9:161-191. HALPERIN, W. and W.A. JENSEN. 1967. Ultrastructural changes during growth and embryogenesis in carrot cell cultures. J Ultrastructure Res. 18: 428-443. HALPERIN, W. and D.F. WETHERELL. 1965. Ammonium requirement for embryogenesis in uitro. Nature 105:519-520.
PHYSIOLOGY OF IN VITRO ASEXUAL EMBRYOGENESIS
303
HILL, G.P. 1967. Multiple budding on carrot embryos arising in tissue culture. N a turc 2 15:1098-1099. HOMES, J.L.A. 1967. Influence de la concetration en glucose sur la developpement et la differenciation d’embryons formes dans des tissus de carotte cultives in uitro. CNRS. p. 49-60, Strasbourg. Les cultures de tissus de plantes. Colloq. Nat. CNRS, Paris. JEFFS, R.A. and D.H. NORTHCOTE. 1967. The influence of indol-3-yl-acetic acid and sugar in the pattern of induced differentiation in plant tissue cultures. J Cell Sci. 2:77-88. JELASKA, S . 1974. Embryogenesis and organogenesis in pumpkin explants. P h ysiol. Plant. 3 1:25 7- 26 1. JENSEN, W.A. 1963. Cell development during plant embryogenesis. p. 179202. I n Meristems and differentiation. Brookhaven Symp. in Biol. 16. JONES, L.E., A.C. HILDEBRANDT, A.J. RIKER, and J.H. WU. 1960. Growth of somatic tobacco cells in microculture. Amer. J. Bot. 47:468-475. KAMADA, H. and H. HARADA. 1979a. Studies on the organogenesis in carrot tissue cultures. I. Effects of growth regulations on somatic embryogenesis and root formation. 2. Pflanzenphysiol. 91:255-266. KAMADA, H. and H. HARADA. 1979b. Studies on the organogenesis in carrot tissues. 11. Effects of amino acids and inorganic nitrogenous compounds on somatic embryogenesis. Z. Pflanzenphysiol. 91:453-463. KATO, H. 1968. The serial observations of the adventive embryogenesis in the microculture of carrot tissue. Sci. Papers College Gen. Educ., Univ. of Tokyo 18:191-197. KATO, H. and M. TAKEUCHI. 1963. Morphogenesis in uitro starting from single cells of carrot root. Plant & Cell Physiol. 4:243-245. KATO, H. and M. TAKEUCHI. 1966. Embryogenesis from the epidermal cells of carrot hypocotyl. Sci. Papers College Gen. Educ. Univ. of Tokyo 16: 245254. KING, P.J., B.J. COX, M.W. FOWLER, and H.E. STREET. 1974. Metabolic events in synchronized cell culture of Acer pseudoplatus L. Planta 117:109122. KOCHBA, J. and J . BUTTON. 1974. The stimulation of embryogenesis and embryoid development in habituated ovular callus from the ‘Shamouti’ orange (Citrus sinensis) as affected by tissue age and sucrose concentration. Z. Pflanzenphysiol. 73:415-421. KOCHBA, J., S. LAVEE, and P. SPIEGEL-ROY. 1977. Differences in peroxidase activity and isoenzymes in embryogenic and non-embryogenic ‘Shamouti’ orange ovular callus lines. Plant & Cell Physiol. 18:463-467. KOCHBA, J., P. SPIEGEL-ROY, and H. SAFRAN. 1972. Adventive plants from ovules and nucelli in citrus. Planta 106:237-245. KOHLENBACH, H.W. 1965. Uber organisierte bildungen aus Macleaya cordata kallus. Planta 64:37-40. KOHLENBACH, H.W. 1966. Die entwicklungspotenzen explantierter und isolierter dauerzellen. I. Das streckungs - und teilungswachstum isolierter meso-
304
HORTICULTURAL REVIEWS
phyllzellen von Macleaya cordata. 2. Pflanzenphysiol. 55:142-157. KOHLENBACH, H.W. 1978a. Regulation of embryogenesis i n uitro. p. 236251. I n H.R. Schutte and D. Gross (eds.) Regulation of developmental processes in plants. VEB Kongress - und Werbedruck, Oberlungwitz. KOHLENBACH, H.W. 1978b. Comparative somatic embryogenesis. p. 59-66. In T.A. Thorpe (ed.) Frontiers of plant tissue culture. Univ. of Calgary Offset Printing Services, Calgary. KOMAMINE, A,, Y. MOROHASHI, and M. SHIMOKORIYAMA. 1969. Changes in respiratory metabolism in tissue cultures of carrot root. Plant & Cell Physiol. 10:411-423. KONAR, R.N. and K. NATARAJA. 1965a. Experimental studies in R a n u n culus sceleratus L. Development of embryos from the stem epidermis. Phytomorphology 15: 132-137. KONAR, R.N. and K. NATARAJA. 1965b. Experimental studies in R a n u n culus sceleratus L. Plantlets from freely suspended cells and cell groups. Phytomorphology 15:206-211. KONAR, R.N., E. THOMAS, and H.E. STREET. 1972a. Origin and structure of embryoids arising from the epidermal cells of R a n u n c u l u s sceleratus L. J. Cell Sci. 11:77-93. KONAR, R.N., E. THOMAS, and H.E. STREET. 1972b. The diversity of morphogenesis in suspension cultures of Atropa belladonna L. A n n . Bot. 36: 249-258. KRUL, W.R. and J.F. WORLEY. 1977. Formation of adventitious embryos in callus cultures of ‘Seyval’, a French hybrid grape. J. Amer. SOC.Hort. Sci. 102:360-363. LAJTHA, L.G. 1967. Proliferation kinetics of steady state cell populations. p. 97-105. I n H. Teir and T . Rytomaa (eds.) Control of cellular growth in adult organisms. Academic Press, London. LEE, D.W. and D.K. DOUGALL. 1973. Electrophoretic variation in glutamate dehydrogenase and other isozymes in wild carrot cells cultured in the presence and absence of 2,4-dichlorophenoxyaceticacid. I n Vitro 8:347-352. LINSER, H. and K.N. NEUMANN. 1968. Untersuchungen uber beziehungen zwischen zellteilung und morphogenese bei gewebekulturen von Daucus carota. I. Rhizogenese und ausbildung ganzer Pflanzen. Physiol. Plant. 21: 487-499. MACLEOD, R.D. 1968. Changes in the mitotic cycle in lateral root meristems of Vicia faba following kinetin in treatment. Chromosoma 24:177-187. MAHLER, H.R. and E.H. CORDES. 1966. Biological chemistry. Harper & Row, Publishers, New York. MATSUMOTO, H., D. GREGOR, and J. REINERT. 1975. Changes in chromatin of Daucus carota cells during embryogenesis. Phytochemistry 14:4147. MATSUOKA, H. and K. HINATA. 1979. NAA-induced organogenesis and embryogenesis in hypocotyl callus of Solanum melongena L. J. Expt. Bot. 116:363-370.
PHYSIOLOGY OF IN VITRO ASEXUAL EMBRYOGENESIS
305
MCWILLIAM, A.A., S.M. SMITH, and H.E. STREET. 1974. The origin and development of embryoids in suspension cultures of carrot (Daucus carota). Ann. Bot. 38:243-250. MEINS, F., JR. 1975. Cell division and the determination phase of cytodifferentiation in plants. p. 151-175. Zn J. Reinert and H. Holzer (eds.) Results and problems in cell differentiation. Springer-Verlag, Berlin. MITCHISON, J. M. 1971. The biology of the cell cycle. Cambridge Univ. Press, Cambridge. MITRA, G.C. and H.C. CHATURVEDI. 1972. Embryoids and complete plants from unpollinated ovaries and from ovules of in uiuo-grown emasculated flower buds of Citrus spp. Bul. Torr. Bot. Club 99:184-189. MURASHIGE, T., N.M. SHADBE, P.M. HASEGAWA, F.H. TAKATORI, and J.B. JONES. 1972. Propagation of asparagus through shoot apex culture. I. Nutrient medium for formation of plantlets. J. Amer. Soc. Hort. Sci. 97: 158-161. MURASHIGE, T. and F. SKOOG. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15:473-497. NAKAJIMA, T. and T. YAMAGUCHI. 1967. On the embryogenesis observed in tissue culture of carrot, Daucus carota L. Bul. Uniu. Osaka Prefecture 19:43-49. NEUMANN, K.H. 1965. Wurzelbildung und nukleinsauregehalt bei phloemgewebekulturen der karottenwurzel auf synthetischen nahrmedium verschiedener hormonkombinationen. In Les phytohormones et l’organogenese. Les Congres et Colloques de’l Universite de Liege 38:Les phytohormones et l’orgenese, p. 95-102. NEUMANN, K.H. 1968. Untersuchungen uber beziehungen zwischen zellteilung und morphogenese bei gewebekulturen von Daucus carota. 11.Respiration von gewebekulturen in abhangigkeit von der zellteilungsintensitat. Physiol. Plant. 2 1:5 19- 5 24. NEUMANN, K.H. 1969. Mikroskopie. Mikroskopische untersuchungen zum wachstumsverlauf von explantaten verschiedener gewebepartien der karottewurzel in gewebekultur. 25:261-27 1. NEUMANN, K.H. and F.C. STEWARD. 1968. Investigations on the growth and metabolism of cultured explants of Daucus carota. I. Effects of iron, molybdenum, and manganese on growth. Planta 81:333-350. NEWCOMB, W. and D.F. WETHERELL. 1970. The effects of 2,4,6-trichlorophenoxyacetic acid on embryogenesis in wild carrot tissue cultures. Bot. Gaz. 131:242-245. NISHI, A. and N. SUGANO. 1970. Growth and division of carrot cells in suspension culture. Plant & Cell Physiol. 11:757-765. NITSCH, C. 1975. Single cell culture of a haploid cell: the microspore. p. 297310. I n L. Ledoux (ed.) Genetic manipulations with plant material. Plenum Press, New York. NITSCH, J.P. and C. NITSCH. 1969. Haploid plants from pollen grains. Science 163:85-87.
306
HORTICULTIJRAL REVIEWS
NORREEL, G. and J.P. NITSCH. 1968. La formation d’ “embryons vegetatifs” chez Daucus carota L. Bul. SOC. Bot. Fr. 115:501-514. NORSTOG, K. and E. RHAMSTINE. 1967. Isolation and culture of haploid and diploid cycad tissues. Phytomorphology 17:374-381. NORTHCRAFT, R.D. 1951. T h e use of oxalate to produce free-living cells from carrot tissue cultures. Science 113:407-408. PENCE, V.C., P.M. HASEGAWA, and J . JANICK. 1979. Asexual embryogenesis in Theobroma cacao L. J. Amer. SOC. Hort. Sci. 104:145-148. P E T R U , E. 1970. Development of embryoids in carrot root callus culture (Daucus carota L.). Biologia Plantarum (Praha) 12:l-3. PRICE, H.J. and R.H. SMITH. 1979. Somatic embryogenesis in suspension i u m klotzchianum Anderss. Planta 145:305-307. RADOJEVIC, L., R. VUJICIC, and M. NESKOVIC. 1975. Embryogenesis in tissue culture of Corylus auellana L. 2. Pflanzenphysiol. 77:33-41. RAGHAVEN, V. 1976. Role of the generative cell in androgenesis in henbane. Science 191:388-389. RAGHAVAN, V. and J.G. TORREY. 1963. Growth and morphogenesis of globular and older embryos of Capsella in culture. Amer. J. Bot. 50:540-551. RANGA SWAMY, N.S. 1958. Culture of nucellar tissue of Citrus i n uitro. Experien tia 14:111-112. RANGA SWAMY, N.S. 1961. Experimental studies on female reproductive structures of Citrus microcarpa Bunge. Phytomorphology 11:101- 127. RANGAN, T.S., T. MURASHIGE, and W.P. BITTERS. 1968. I n uitro initiation of nucellar embryos in monoembryonic Citrus. HortScience 3:226-227. RANGAN, T.S., T. MURASHIGE, and W.P. BITTERS. 1969. In vitro studies of zygotic and nucellar embryogenesis in Citrus. In H.D. Chapmen (ed.) Proc. First Intern. Citrus Symp., Vol. I. May 16-26, 1968. Univ. of Calif., Riverside. RAO, P.S., W. HANDRO, and H. HARADA. 1973. Hormonal control of differentiation of shoots, leaf and stem cultures of Petunia inflata and Petunia hybrida. Physiol. Plant. 28:458-463. RASHID, A. and H.E. S T R E E T . 1973. T h e development of haploid embryoids from anther cultures of Atropa belladonna. Planta 113:263-270. REINERT, J. 1959. Uber die kontrolle der morphogenese an gewebekulturen. Ber. Dtsch. Bot. Ges. 71:15. REINERT, J. 1968. Factors of embryo formation in plant tissues cultivated i n uitro. p. 33-40. I n Les cultures des tissus de plantes. Coll. Nat. CNRS, Paris. REINERT, J. and D. BACKS. 1968. Control of totipotency in plant cells growing i n uitro. Nature 220:1340-1341. REINERT, J., Y.P.S. BAJAJ, and B. ZBELL. 1977. Aspects of organizationorganogenesis, embryogenesis, cytodifferentiation. p. 389-427. I n H.E. Street (ed.) Tissue and cell culture. Blackwell Scientific Publications, Oxford. REINERT, J., D. GREGOR, and H. MATSUMOTO. 1973. Studies on the chromatin of carrot cell cultures growing in the presence and absence of auxin.
PHYSIOLOGY OF IN VITRO ASEXUAL EMBRYOGENESIS
307
p. 539-548. I n Proc. Eighth Intern. Conf. Plant Growth Substances, Tokyo. Hirokawa Publishing Co., Tokyo. REINERT, J., M. TAZAWA, and S. SEMENOFF. 1967. Nitrogen compounds as factors of embryogenesis i n uitro. Nature 216:1215-1216. REIJTHER, G. 1977. Adventitious organ formation and somatic embryogenesis in callus of asparagus and Iris. Acta Hort. 78:217-224. REYNOLDS, J.F. and T. MURASHIGE. 1979. Asexual embryogenesis in callus cultures of palms. I n Vitro 15:383-387. SANGWAN, R.S. and H. HARADA. 1975. Chemical regulation of callus growth, organogenesis, plant regeneration, and somatic embryogenesis in Antirrhinum majus tissue and cell cultures. J. Expt. Bot. 26:868-881. SENGUPTA, C. 1978. Protein and nucleic acid metabolism during somatic embryogenesis in carrot. PhD Dissertation, T h e Ohio State University, Columbus. SENGUPTA, C. and V. RAGHAVAN. 1977. Nucleic acid metabolism during induction of somatic embryogenesis in carrot. Plant Physiol. (Suppl.) 69:160. SENGUPTA, C. and V. RAGHAVAN. 1979. Nucleic acid metabolism during induction of somatic embryogenesis in carrot. p. 841. (Abstr.) I n W.R. Sharp, P.O. Larsen, E.F. Paddock, and V. Raghavan (eds.) Plant cell and tissue culture. Ohio State Univ. Press, Columbus. SENGUPTA, C. and V. RAGHAVAN. 1980a. Somatic embryogenesis in carrot cell suspension. I. Pattern of protein and nucleic acid synthesis. J. Expt. Bot. (in press). SENGUPTA, C. and V. RAGHAVAN. 1980b. Somatic embryogenesis in carrot cell suspension. 11. Synthesis of ribosomal RNA and Poly(A)+ RNA. J. Expt. Bot. (in press). SHARP, W.R., D.K. DOUGALL, and E.F. PADDOCK. 1971. Haploid plantlets and callus from immature pollen grains of Nicotiana and Lycopersicon. Bul. Torr. Bot. Club 98:219-222. SMITH, S.M. and H.E. S T R E E T . 1974. T h e decline of embryogenic potential as callus and suspension callus of carrot (Daucus carota L.) are serially subcultured. Ann. Bot. 38:223-241. SONDAHL, M.R., T.L. SALISBURY, and W.R. SHARP. 1979. Characterization of embryogenesis in coffee callus by scanning electron microscope. 2. Pflanzenphysiol. 94:185-188. SONDAHL, M.R. and W.R. SHARP. 1977. High frequency induction of somatic embryos in cultured leaf explants of Coffea arabica L. 2. Pflanzenphysiol. 81:395-408. SONDAHL, M.R. and W.R. SHARP. 1979. Research in Coffea and applications of tissue culture methods. p. 527-584. I n W.R. Sharp, P.O. Larsen, E.F. Paddock, and V. Raghavan (eds.) Plant cell and tissue culture - principles and application. Ohio State Univ. Press, Columbus. SONDAHL, M.R., D.A. SPAHLINGER, and W.R. SHARP. 1979. A histological study of high frequency induction of somatic embryos in cultured leaf explants of Coffea arabica L. 2. Pflanzenphysiol. 94:lOl-108.
308
HORTICULTURAL REVIEWS
SPELSBERG, T.C. and L.S. HNILICA. 1969. The effect of acidic proteins and RNA on the histone inhibition of the DNA dependent RNA synthesis in uitro. Biochem. Biophys. Acta 195:63-75. SPIEGEL-ROY, P. and J. KOCHBA. 1973. Stimulation of differentiation in orange (Citrus sinensis) ovular callus in relation to irradiation of the media. Radiation Bot. 13:97-103. STARITSKY, G. 1970. Embryoid formation in callus tissues of coffee. Acta Bot. Neerl. 19:509-514. STEWARD, F.C., L.M. BLAKELY, A.E. KENT, and M.O. MAPES. 1963. Growth and organization in free cell cultures. p. 73-88. In Meristems and differentiation. Brookhaven Symp. in Biol. 16. STEWARD, F.C., M.O. MAPES, A.E. KENT, and R.D. HOLSTEN. 1964. Growth and development of cultured plant cells. Science 14390-27. STEWARD, F.C., M.O. MAPES, and K. MEARS. 1958. Growth and organized development of cultured cells. 11. Organization in cultures grown from freely suspended cells. Amer. J Bot. 45:705-708. STREET, H.E. 1973. Plant cell cultures: their potential for metabolic studies. p. 93-125. In B.V. Milborrow (ed.) Biosynthesis and its control in plants. Academic Press, London. STREET, H.E. 1976. Cell cultures: a tool in plant biology. p. 7-38. In D. Dudits, G.L. Farkas, and P. Maliga (eds.) Cell genetics in higher plants. Publ. House Hungarian Academy of Sciences, Budapest. STREET, H.E. 1978. Differentiation in cell and tissue cultures-regulation at the molecular level. p. 192-218.In H.R. Schutte and D. Gross (eds.)Regulation of developmental processes in plants. VEB Kongress - und Werbedruck, Oberlungwitz. STREET, H.E. 1979. Embryogenesis and chemically induced organogenesis. p. 123-154.In W.R. Sharp, P.O. Larsen, E.F. Paddock, and V. Raghavan (eds.) Plant cell and tissue culture. Ohio State Univ. Press, Columbus. STREET, H.E. and L.A. WITHERS. 1974. The anatomy of embryogenesis in culture. p. 71-100. In H.E. Street (ed.) Tissue culture and plant science. Academic Press, London. SUNDERLAND, N. 1974. Anther culture as a means of haploid induction. p. 91-122. In K.J. Kasha (ed.) Haploids in higher plants, advances and potential. Univ. of Guelph, Guelph, Ontario. SUNDERLAND, N. 1977. Observations on anther culture of ornamental plants. In R . Gautheret (ed.) G. Morel Memorial Volume. Masson Lie, Paris. SUNDERLAND, N. and J.M. DUNWELL. 1977. Anther and pollen culture. p. 223-265. In H.E. Street (ed.) Plant tissue and cell culture. Univ. of Calif. Press, Berkeley. SUSSEX, I.M., M.E. CLUTTER, and M.H.M. GOLDSMITH. 1972. Wound recovery by pith cell redifferentiation: structural changes. Amer. J.Bot. 59: 797-804. SUSSEX, I.M. and K.A. FREI. 1968. Embryoid development in long-term tissue cultures of carrot. Phytomorphology 18:339-349.
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309
TAZAWA, M. and J. REINERT. 1969. Extracellular and intracellular chemical environments in relation to embryogenesis in uitro. Protoplasma 68:157173. THOMAS, E., F. HOFFMAN, I. POTRYKUS, and F. WENZEL. 1976. Protoplast regeneration and stem embryogenesis of haploid androgenetic rape. Molec. Gen. Genet. 145:245-247. THOMAS, E., P.J. KING, and I. POTRYKUS. 1977. Shoot and embryo-like structure formation from cultured tissues of Sorghum bicolor. Naturwiss 64: 587. TISSERAT, B., E.B. ESAN, and T. MURASHIGE. 1979. Somatic embryogenesis in angiosperms. p. 1-78.In J. Janick (ed.) Horticultural reviews, volume I. AVI Publishing, Westport, Conn. TISSERAT, B. and T. MURASHIGE. 1977a. Probable identity of substances in Citrus that repress asexual embryogenesis. I n Vitro 13:785-789. TISSERAT, B. and T. MURASHIGE. 1977b. Repression of asexual embryogenesis in uitro by some plant growth regulators. I n Vitro 13:799-805. TORREY, J.G., J. REINERT, and N. MERKEL. 1962. Mitosis in suspension cultures of higher plant cells in a synthetic medium. Amer. J Bot. 49:420425. TREWAVAS, A. J. 1976. Plant growth substances. p. 249-298. I n J.A. Bryant (ed.) Molecular aspects of gene expression in plants. Academic Press, London. VAN'T HOF, J. 1974. Control of the cell cycle in higher plants. p. 77-85. I n G.M. Padila, I.L. Cameron, and A. Zimmerman (eds.) Cell cycle controls. Academic Press, New York. VAN'T HOF, J. and C.J. KOVACS. 1972. Mitotic cycle regulation in the meristem of cultured roots: T h e principal control point hypothesis. p. 13-33. I n M.W. Miller and C.C. Keuhnert (eds.) The dynamics of meristem cell populations. Plenum Press, New York. VASIL, I.K. and A.C. HILDEBRANDT. 1966. Variations of morphogenetic behavior in plant tissue cultures I. Cichorium endiuia. Amer. J. Bot. 53:860869. WANG, T.Y. 1968a. Restoration of histone inhibited DNA dependent RNA synthesis by acid chromatin proteins. Expt. Cell Res. 53:288-291. WANG, T.Y. 1968b. Study of the chromatin acidic proteins of rat liver; heterogenity and complex formation with histones. Arch. Biochem. Biophys. 124: 176-183. WANG, T.Y. 1971. Tissue specificity of non-histone chromosomal proteins. Expt. Cell Res. 69:217-219. WEBBER, H.J. 1931. The economic importance of apogamy in Citrus and Mangifera. Proc. Amer. Soc. Hort. Sci. 28:57-61. WEBBER, J.M. 1970. Polyembryony. Bot. Reu. 6:575-598. WEBSTER, P.L. and D. DAVIDSON. 1968. Evidence from Thymidine-"labeled meristems of Vicia faba of two cell populations. J. Cell Biol. 39:332338.
310
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WETMORE, R.H. and J.P. RIER. 1963. Experimental induction of vascular tissues in callus of angiosperms. Arner. J. Bot. 50:418-430. WILLIAMS, L. and H.A. COLLIN. 1976. Embryogenesis and plantlet formation in tissue cultures of celery. Ann. Bot. 40:325-332. WILMAR, C. and M. HELLENDOORN. 1968. Growth and morphogenesis of asparagus cells cultured in uitro. Nature 217:369-370. WOCHOK, Z.S. 1973. DNA synthesis during development of adventive embryos of wild carrot. Biol. Plant. 15:107-111. YEOMAN, M.M. 1970. Early development in callus cultures. Intern. Reu. Cytol. 29:383-409. YEOMAN, M.M. 1974. Division synchrony in cultured cells. p. 1-17. In H.E. Street (ed.) Tissue culture and plant science. Academic Press, London. YEOMAN, M.M. and P.A. AITCHISON. 1976. Molecular events of the cell cycle: A preparation for division. p. 111-113. In M.M. Yeoman (ed.) Cell division in higher plants. Academic Press, New York. ZEE, S.Y. and S.C. WU. 1979. Embryogenesis in the petiole explants of Chinese celery. 2. Pflanzenphysiol. 93:3 25 - 3 3 5.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
7 Genetics of Vigna Richard L. Fery U.S. Vegetable Laboratory, Agricultural Research, Science and Education Administration, U.S. Department of Agriculture, Charleston, South Carolina 29407 I. 11. 111. IV.
Introduction 314 Taxonomy 314 Gene Nomenclature for Vigna 315 Cowpea 317 A. Cytology 317 B. Plant Characters 324 1. Habit 324 2.Leaves 325 3. Abnormalities 325 327 4. Lethal Factors C. Heterosis 327 D. Color 327 328 1. Seed Coat Color 2. Flower Color 330 331 3. Pod Color 332 4. Foliage Color E. Flowers and Flowering 333 333 1. Compound Inflorescence 2. Photoperiod 333 333 3. Outcrossing Mechanisms 4 . Early Flowering 334 F. Pods 335 335 1. Pod Size 2. Seed Number 337 337 3. Seed Spacing 4. Pod Texture 337 337 5. Pod Shape G. Seeds 338 1. Seed Size 338 338 2. Seed Shape 311
312
HORTICULTURAL REVIEWS
3. Seed Coat Pattern 338 4. Seed Coat Structure 340 5. Hollow Seeds 341 6. Seed Protein 341 H. Yield 341 1.Heritability Estimates and Gene Action 2. Character Association 341 I. Resistance to Fungal and Bacterial Diseases 1.Anthracnose 343 2. Bacterial Canker 343 3. Cercospora Leaf Spot 344 4. Charcoal Rot 344 5. Fusarium Wilt 344 6. Powdery Mildew 344 7. Rust 344 8. Stem Rot 344 9. Target Spot 344 10. Verticillium Wilt 344 J. Resistance to Virus Diseases 345 345 1.Bean Yellow Mosaic Virus 345 2. Cowpea Chlorotic Mottle Virus 3. Cowpea Mottle Virus 345 345 4. Cowpea Yellow Mosaic Virus 5. Cucumber Mosaic Virus 345 345 6. Southern Bean Mosaic Virus 7. Tobacco Ringspot Virus 345 K. Resistance to Root-knot Nematodes 346 L. Resistance to Insects 346 1.Beetle 346 2. Cowpea Curculio 346 3. Pod Borer 347 M. GeneLinkage 347 N. Interspecific Hybridization 347 V. MungBean 348 A. Cytology 351 B. Plant Characters 352 1.Habit 352 2.Leaves 352 3. Pubescence 354 C. Heterosis 354 D. Color 355 1.Plant Color 355 2. Seed Coat Color 355 3. Flower Color 357 4. Pod Color 357 5. Plant Pubescence Color 357 E. Flowers and Flowering 358
341 343
GENETICS OF VIGNA
1.Simple Inflorescence 358 2. Photoperiod 358 3. Outcrossing Mechanisms 358 4. Early Flowering 358 F. Pods 359 1.Pod Length 359 2. Seed Number 359 3. Pod Shattering 360 4. Pod Shape 360 G. Seeds 360 1.Seed Size 360 2. Seed Coat Structure 360 3. Seed Protein 361 H. Yield 361 1.Heritability Estimates and Gene Action 2. Character Association 362 I. Resistance to Fungal and Bacterial Diseases 1.Bacterial Leaf Spot 363 2. Cercospora Leaf Spot 363 3. Powdery Mildew 363 J. Resistance to Virus Diseases 363 363 1.Mung Bean Yellow Mosaic Virus 2 . Cucumber Mosaic Virus 363 K. GeneLinkage 364 L. Interspecific Hybridization 364 VI. UrdBean 364 A. Cytology 364 B. Plant Characters 367 1.Habit 367 2.Leaves 368 C. Color 368 1.Seed Coat Color 368 2. Pod Color 368 3. Plant Color 368 D. Flowers and Flowering 369 1.Flower Mutants 369 2. Early Flowering 369 E. Pods 369 1.Pod Size 369 2. Pod Pubescence 369 F. Seeds 370 1.Seed Size 370 2. Glossy Seed Coat 370 3. Seed Dormancy 370 4. Seed Protein 371 G. Yield 371 1.Heritability Estimates and Gene Action
361 363
371
313
314
HORTICULTURAL REVIEWS
VII. VIII. IX. X.
2. Character Association 371 H. Resistance to Yellow Mosaic Virus I. GeneLinkage 372 J. Interspecific Hybridization 372 Adzuki Bean 373 MothBean 373 RiceBean 375 Literature Cited 376
372
I. INTRODUCTION The genus Vigna, Leguminosae, contains several species that are important in world agriculture. Cowpeas ( V . unguiculata [L.] Walp.), mung beans (V. radiata [L.] Wilczek), and urd beans (V. mungo [L.] Hepper) are grown on more than 10 million ha annually (Rachie and Roberts 1974), and provide a significant portion of the dietary protein for many people. Additionally, several other Vigna species, e.g., adzuki beans ( V. angularis iWilld.3 Ohwi & Ohashi), moth beans ( V . aconitifolia LJacq.1 Marechal), and rice beans (V. umbellata [Thunb.] Ohwi & Ohashi), are important in the diets of some societies. The cultivated Vigna species share desirable features (Rachie and Roberts 1974). They can be grown successfully over a wide range of environmental conditions and all provide inexpensive protein that can be prepared easily in a number of edible forms, such as tender green shoots and leaves, immature pods, and green and dry seeds. The cultivated Vigna species also are valued as fodder, cover, and green manure crops. Except for limited coverage in a general review of grain legumes by Rachie and Roberts (19741, the genetics of the cultivated Vigna species was last reviewed by Yarnell in 1965. The objectives of this review are to (1) present a comprehensive review of the genetics of the cultivated Vigna species and (2) to resolve the numerous discrepancies in the literature with respect to gene symbols, and update or construct gene lists using appropriate gene nomenclature rules. 11. TAXONOMY
There is considerable confusion in the synonymy and names of the cultivated Vigna species. The U.S. Department of Agriculture (USDA) recognizes Verdcourt’s (1970) classification scheme (Gunn 1973). Verdcourt (1970) concluded that cowpea (formerly V. sinensis (L.) Savi ex Hassk.), catjang (formerly V. cylindrica (L.) Skeels), and asparagus bean (formerly V. sesquipedalis (L.) Fruw. and V. sinensis (L.) Savi ex Hassk. subsp. sesquipedalis (L.) van Eseltine) are not to be regarded as distinct
GENETICS OF VIGNA
315
species since they cross freely to form fully fertile hybrids. He treats these three rather distinct taxa as subspecies of V. unguiculata (L.) Walp., i.e., cowpea = V. unguiculata subsp. unguiculata, catjang = V. unguiculata subsp. catjang, and asparagus bean = V. unguiculata subsp. sesquipedalis. Additionally, Verdcourt (1970) lists the following cultivated species as belonging to the genus Vigna and not the genus Phaseolus: adzuki bean, V. angularis (Willd.) Ohwi & Ohashi (formerly P. angularis (Willd.) W.F. Wright); moth bean, V. aconitifolia (Jacq.) Marechal (formerly P. aconitifolius Jacq.); mung bean, V. radiata (L.) Wilczek (formerly P. radiatus L., P. aureus Roxb., and P. sublobatus Roxb.); rice bean, V. umbellata (Thunb.) Ohwi & Ohashi (formerly P. calcaratus Roxb.); urd, V. mungo (L.) Hepper (formerly P. mungo L.). Verdcourt (1970) regards mung bean (V. radiata) and urd (V. mungo) as “scarcely more than variants of one species,” but recommends that the two species be kept distinct until monographed. Unfortunately, this statement has caused some confusion in the recent literature. For example, Rachie and Roberts (1974) consider mung and urd to be botanical varieties of V. radiata, and reviewed the literature for both species together under the single heading “mung beans.” Watt and Marechal (1977), however, suggested that there is ample evidence to justify keeping distinct identities for mung and urd. They point out that the lethality or semi-lethality often observed when mung and urd are crossed is good evidence of an incompatibility barrier separating the species. Also, they cited the chemotaxonomic work of Otoul et al. (19751, who found evidence that the wild V. radiata var. sublobata is a progenitor of V. radiata and not of V. mungo. Since the USDA recognizes V. radiata and V. mungo as separate species, their identities will be kept separate in this review. 111. GENE NOMENCLATURE FOR VIGNA
No recommendations on gene symbols and nomenclature for the genus Vigna have been published. For example, there are instances in which the same symbol has been assigned to different genes, the same gene has been assigned different symbols, or no symbol has been assigned to a gene. Robinson e t al. (1976) recently used the recommendations of both the International Committee on Genetic Symbols and Nomenclature (Tanaka et al. 1957) and the Tomato Genetics Cooperative (Barton et al. 1955; Clayberg e t al. 1960, 1966, 1970) to construct a proposed set of gene nomenclature rules for the Cucurbitaceae. The following set of rules has been adapted from those proposed for Cucurbitaceae and I propose that they be adopted for Vigna:
316
HORTICULTURAL REVIEWS
(1) The name of a gene should be descriptive of the characteristic phenotype conditioned by the gene. The name should be short and in either English or Latin. (2) Genes are symbolized by italicized Roman letters, the first letter being the same as that for the name. A minimum number of additional letters is used to distinguish the symbol from other symbols already assigned to the species. (3) The first letter of the symbol and name is capitalized if the gene is dominant to the normal allele; otherwise, all letters are in lower case. The normal allele is represented by the symbol “+,” or if needed for clarity, the gene symbol followed by the superscript “+.” Except for instances in which a symbol has already been established for the normal allele, the primitive form of each species shall represent the + allele for each gene. (4) A symbol shall not be assigned to a gene that is not firmly established by statistically valid segregation data. (5) Mimics, i.e., different genes that condition similar phenotypes, may be assigned distinctive names and symbols or the symbol of the original gene followed by a hyphen and distinguishing Arabic numeral or Roman letter. The suffix “1” is used, or understood, for the original gene in a mimic series. Allelism tests should be made before a new gene symbol is assigned to a mimic. (6) Multiple alleles are assigned the same symbol, followed by a Roman letter or Arabic number superscript. The allelism test must be made to establish multiple alleles. (7) Indistinguishable alleles, i.e., alleles a t the same locus that condition identical phenotypes, preferably should be given the same symbol. However, an allele that is an apparent recurrence of the same mutation can be given a distinctive symbol by adding to the symbol of the original allele superscript Roman letters or Arabic numbers that are enclosed in parentheses. The superscript “(1)”is understood and not used for the original allele. (8) A modifying gene may be designated using a symbol for an appropriate name, e.g., intensifier, suppressor, or inhibitor, followed by a hyphen and the symbol of the allele affected. Alternatively, a modifying gene may be given a distinctive name and symbol without reference to the gene modified. (9) In instances where the same symbol has been assigned to different genes or the same gene has been assigned different symbols, priority in publication will be the primary criterion for establishing the preferred symbol. Incorrectly assigned symbols will be enclosed in parentheses on gene lists.
GENETICS OF VIGNA
317
IV. COWPEA Cowpea is the most generally recognized common name for all of the cultivated forms of the botanical species V. unguiculata (L.) Walp., and it is the term most commonly used in the scientific literature. The cultivated forms of the V. unguiculata, however, are known by many other common names. Edible types grown in the United States are known as southernpeas, blackeye peas, and blackeye beans. Other common names include niebh, field pea, crowder pea, china pea, kaffir bean, lubiah, ellaich, coupe, and frijole. The names asparagus bean, yard-long bean, sitao, bodi bean, and snake bean are used sometimes for cultivated forms of the subspecies sesquipedalis. Catjang, Jerusalem pea, and marble pea usually denote cultivated forms of the subspecies catjang. Except for limited outcrossing observed occasionally in humid climates (Harland 1919a; Mackie and Smith 1935; Purseglove 1968; Rachie and Silvestre 19771, it is highly self-pollinated. The large flowers and untwisted keels of the cowpea make it one of the easiest legumes to emasculate and artificially pollinate. Detailed hybridization procedures have been published by Oliver (19101, Capinpin (19351, Krishnaswamy et al. (19451, Mackie (19461, Kheradnam and Niknejad (1971a1, Ebong (19721, Pokle and Deshmukh (19721, Moore (1974), Rachie, Rawal, and Franckowiak (19751, and Kumar et al. (1976a). A total of 141 genes has been described for the species (Table 7.1). A. Cytology
Although there have been reports that the haploid chromosome number for V. unguiculata is 12 (Yarnell 19651, the preponderance of published data indicates that the correct number is 11. Faris (1964) exhaustively examined the species and found only diploids of 2n = 2x = 22 chromosomes. Frahm-Leliveld (1965) concluded that n = 11 was normal for the cowpea. Mukherjee (1968) conducted a critical study of pachytene chromosomes of V. unguiculata and described each of 11 bivalents. He found that the complement consisted of 1 short (19 pm), 7 medium (26 to 36 pm), and 3 long (41 to 45 pm) chromosomes. The chromomeres were not distributed uniformly along the chromosome arms. Sen and Hari (1956) and Sen and Bhowal (1960) studied induced tetraploidy in V. unguiculata and found marked cultivar differences in morphological characters, pollen sterility, fruit-setting, and meiotic irregularities. Sen and Bhowal (1960) observed autotetraploid meiotic abnormalities such as quadrivalent, trivalent, and univalent formation and the occurrence of laggards and unequal distributions in the anaphases. Although they con-
318
HORTICULTURAL REVIEWS
TABLE 7.1. LIST OF COWPEA. VIGNA UNGUICULATA. GENES
Preferred Symbol Synonym Character Alfalfa-likepod shape. A
Reference Spillman and Sando 1930
ax
Axillary buds. Active buds in axils of cotyledons.
Krishnaswamy et al. 1945
B
Blue seed coat.
Spillman 1912
*Bc-1
Bacterial canker resistance-1.
Singh and Patel 1977a
*bc-2
Bacterial canker resistance-2.
Singh and Patel 1977a
BCY
Brown calyx color. Dominant to green.
Kolhe 1970
Buff seed coat color.
Harland 1919a,b, 1920
Brown grain color. Dominant to white grain color.
Kolhe 1970
Blackpod color. Dominant to white pod color.
Capinpin 1935
*Bf
(N)
Bg *Bk
*Bl
(B)
(B,Bb),Pb Black seed coat. Also condi-
tions anthocyanin production in the pod tip, calyx and peduncle. Heterozygote produces mottled seeds.
Harland 1919a,b, 1920; Franckowiak and Barker 1974
*El'
(B')
New Era seedcoat pattern.
Franckowiak and Barker 1974
*El'
B'
Blue seed coat (fine speckling) pattern.
Franckowiak and Barker 1974
*Big
(Bg)
Gray on black seed coat color.
Franckowiak and Barker 1974
*El'
(El)
Light spots on black seed coat.
Franckowiak and Barker 1974
*Blp
(BP)
Purple seed coat color.
Franckowiak and Barker 1974
*El8
(B")
Black spots on seed coat.
Franckowiak and Barker 1974
*El'
(B')
Taylor seed coat pattern.
Franckowiak and Barker 1974
*bl"
(b")
Modifier of El'.
Franckowiak and Barker 1974
*BP
(Y)
Brown pod color. Dominant to straw color.
Saunders 1960b
Br
(B)
Brown seed coat color.
Spillman 1912; Spillman and Sando 1930
*Bs
(B)
Basic pigmentation gene for seed coat color.
Capinpin 1935
Buffseed coat color.
Brittingham 1950
Bean yellow mosaic virus resistance.
Reeder et al. 1972
Color factor (general).
Spillman 1912; Harland 1919a,b, 1920; Spillman andSando 1930
Bu *bY C
(R)
GENETICS OF VZGNA TABLE 7.1. (Continued)
Preferred Symbol Synonym Character Cbr Cocoa brown pod color (dry).
Reference Krishnaswamy et al. 1945
*cc
Cowpea chlorotic mottle virus resistance.
Rogersetal. 1973
*Ci
Compound inflorescence.
Sen and Bhowal1961
* Ce
Cerise (reddish)pod color.
Saunders 1960a
*Cls-1
Cercospora leaf spot resistance-1.
Fery et al. 1976; Fery and Dukes 1917
*cls-2
Cercospora leaf spot resistance-2.
Fery et al. 1976; Fery and Dukes 1977
*Cm
Cucumber mosaic virus resistance.
Sinclair and Walker 1955
CO
Thick seed coat
Ojomo 1972
CP
Constricted petal.
Rachie, Rawal, Franckowiak, and Akinpelu 1975
Color rnodifyinggene for seed coat color.
Capinpin 1935
crpt
Crumpled petal.
Appa Rao and Reddy 1976
CY
Cylindrica-length pod
Krishnaswamy et al. 1945
D
Dark flower color.
Harland 1919a
*Db
Dark brown seed coat color.
Franckowiak and Barker 1974
*De
Dense speckling; characteristic of 'New Era'.
Spillman and Sando 1930
df
Dwarf. Slow growth, dark green leaves, and short internodes.
Jones 1965
*Dgd-a
Densegrain deposition-a
Kolhe 1970
'Dgd-b
Dense grain deposition -b.
Kolhe 1970
*Dt
Dotting; converts Holstein spots into numerous small ones.
Spillman and Sando 1930
E
N e w Era seed coat pattern. Also conditions anthocyanin production in the pod tip, calyx and pedunc e
Harland 1920
*Ef-1
Early flowering-1.
Ojomo 1971
*Ef-2
Early flowering-2.
Ojomo 1971
*Er
Erect pod attachment. Dominant to drooping pod attachment.
Singh and Jindla 1971
* Cr
319
320
HORTICULTURAL REVIEWS
TABLE 7.1. (Continued)
Preferred Symbol Synonym Character Fine and dense speckling. F Gives rise to blue seed coat.
G
Reference Spillman and Sando 1930
Tinged flower color
Harland 1920
*Gn
Green pod color. Dominant to gnY and recessive to Grid. Conditions similar color response in leaf, calyx and dorsal surface of standard.
Sen and Bhowall961
*Gnd
Darkgreen pod color. Dominant to Gn andgnY.Conditions similar response in leaf, calyx, and dorsal surface of standard.
Sen and Bhowall961
*gny
Yellowgreen pod color. Recessive to Gn and Grid. Conditions similar color response in leaf, calyx and dorsal surface of standard.
Sen and Bhowall961
*Grip
Green pod color. Dominant to white.
Singh and Jindla 1971
GP
Green pod color. Dominant to cream pod color.
Kolhe 1970
Gr
Green bud color. Dominant to white bud color.
Singh and Jindla 1971
gt
Green testa. Recessive to white seed coat.
Chambliss 1974
h -1
Holstein seed coat pattern-1.
Spillman 1911; Sen and Bhowall961
*h-2
Holstein seed coat pattern-2.
Harland 1919a
Ha
Hastate-leaf.
Ojomo 1977
hs
Hollow seed.
Krishnaswamy et al. 1945
Inhibitor of Taylor seed coat pattern.
Spillman and Sando 1930
k
Drabpod color.
Mortensen and Brittingham 1952
Kh
K h a k i seed coat color.
Krishnaswamy et al. 1945
L
Pale flower color.
Harland 1919a
*La
Lanceola te leaf shape.
Krishnaswamy et al. 1945
*Le-1
Lethal-1. Complementary to Le-2.
Saunders 1952,1960~
*Le-2
Lethal-2. Complementary to Le-1.
Saunders 1952,1960~
*In-T
GENETICS OF VIGNA
321
TABLE 7.1. (Continued)
Preferred Symbol Synonym Character *Le-3 Lethal-3. Complementary to Le-4.
Reference Saunders 1952.1960~
*Le-4
Lethal-4. Complementary to Le-3.
Saunders 1952,1960~
*L f
Longi tudina 1 furrowing on seed coat.
Spillman and Sando 1930
Light green pod color.
Krishnaswamy et al. 1945
*Lgf-1
Lightgreen foliage -1. Complementary to Lgf-2.
Kolhe 1970
*Lgf-2
Lightgreen foliage -2. Complementary to Lgf-I.
Kolhe 1970
Llf
Long leaf
Kolhe 1970
Is
Lea fsize. Small leaf recessive to large leaf.
Krishnaswamy et al. 1945
It
Loose testa.
Krishnaswamy et al. 1945
M
Maroon seed coat.
Harland 1919a,b, 1920
ms-1
Male sterile-1.
Sen and Bhowall962
*ms-2
Male sterile-2.
Rachie, Rawal, Franckowiak, Akinpelu 1975
Mu
Mottled seed coat pattern.
Franckowiak and Barker 1974
N
Anthocyanin pigment factor.
Spillman 1912; Spillman and Sando 1930
*Nu
Narrow eye seed coat pattern.
Spillman and Sando 1930
Nl f
Narrow leaf. Dominant to broad leaf.
Kolhe 1970
0
Hilum ring seed coat pattern.
Saunders 1960a
P
Purple pod color. Dominant to green pod color. Also causes anthocyanin roduction in the calyx and pe8uncle.
Harland 1920
Pb
Red-tip pod.
Mortensen and Brittingham 1952
P8
Purple pod withgreen sutures, and partly colored stem and petioles.
Sen and Bhowall961
PP
Purple pod color.
Mortensen and Brittingham 1952
P'
Purple tip pod and stems with purple spots a t the internodes.
Sen and Bhowall961
k
322
HORTICULTURAL REVIEWS
TABLE 7.1. (Continued)
Preferred Symbol Synonym Character Green pod with purple P' ventral suture. Also conditions the spread of purple color on the calyx.
Reference Sen and Bhowall961
*pa-1
Pod appearance-1. Wrinkled appearance of dry pod recessive to smooth appearance.
Krishnaswamy et al. 1945
*pa-2
Pod appearance-2. Wrinkled appearance of dry pod recessive to smooth appearance.
Krishnaswamy et al. 1945
Pb
Purplepetiole base.
Sen and Bhowall961
Pbr
Purple branch base.
Sen and Bhowall961
Pco t
Purple cotyledon. Dominant to white cotyledon.
Krishnaswamy et al. 1945
Pf
Purple flower.
Kolhe 1970
Palegreen plant color.
Saunders 1960a
Pn
Peduncle length. Long peduncles dominant to short.
Krishnaswamy et al. 1945
*4-1
Purple plant pigmentation-1.
VenugopalandGoud 1977
*4-2
Purple plant pigmentation-2.
Venugopal and Goud 1977
* Pr
Purple seed coat color.
Spillman and Sando 1930
Ps
Purple sutures on greed od Pod tip is purple and smaf; ' purple patches scattered over pod surface.
Sen and Bhowall961
Pu
Purplepod. Stem and petiole are completely purple.
Sen and Bhowall961
R
Red seed coat color.
Spillman 1912
Beetle resistance.
Kolhe 1970
Rk
Root-knot resistance.
Fery and Dukes 1979
*Rs
Reniform-shape seed.
Kolhe 1970
Spottingpattern. Patches of black pigment on certain types of seed coat.
Spillman and Sando 1930
*Sbm
Southern bean mosaic virus resistance.
Brantley and Kuhn 1970
*sh
Spindlygrowth habit. Marked elongation of the main stem and few side branches.
Saunders 1960b
*shp
S h r u n k e n pericarp.
Premsekar and Raman 1972
*Pg
*rh
S
GENETICS OF VZGNA
323
TABLE 7.1. (Continued)
Preferred Symbol Synonym Character Speckled pod. *Sk
Reference Saunders 1960a
Sm
Smokyseed coat pattern.
Krishnaswamy et al. 1945
SP
Sesquipedalis-length pod.
Krishnaswamy et al. 1945
*Spk
Speckled seed coat.
Saunders 1959
*Sr
S t e m rot resistance.
Purss 1958
St
Standard petal exhibits full expression of color.
Krishnaswamy et al. 1945
*stp
Stippling seed coat pattern; characteristic of ‘New Era’.
Saunders 1959
*StX
Sesqui edalis-like texture of podcoft).
Premsekar and Raman 1972
Swollen stem base.
Sen and Bhowall961; Ojomo 1977
*Sy-1
Straw yellowpod color (dry)-1.
Krishnaswamy et al. 1945
*sy-2
Straw yellowpod color (dry)-2.
Krishnaswamy et al. 1945
T
Taylor seed coat pattern; thinly scattered speckling of bluish purple dots.
Spillman and Sando 1930
Th
Thick seed coat.
Ojomo 1972
Tobacco ringspot virus resistance.
deZeeuw and Ballard 1959; deZeeuw and Crum 1963
U
Buff seed coat color.
Spillman 1912; Spillman and Sando 1930
un
Unifoliate leaf. Petiole, all stipellae, and the 2 lateral leaflets with their petioles are missing.
Rawal et al. 1976
V
Seed coat mottling characteristicof ‘Brabham’.
Saunders 1959
Vining-1.
Brittingham 1950; Norton 1961; Kolhe 1970; Singh and Jindla 1971
sw
*Tr
* Vi-1
* Vi-2
( V,V,, T2)
Vining-2.
Norton 1961; Kolhe 1970; Singh and Jindla 1971
* V i-3
(T3)
Vining-3.
Singh and Jindla 1971
Verticillium wilt resistance.
Moore 1974
I, W,D
Watson seed coat pattern; eye with indefinite margin.
Spillman 1911;s illman and Sando 1930; Harfand 1919a; Sen and Bhowall961
(W
Whippoorwill type of seed coat pattern.
Spillman and Sando 1930
*v w W
* Wh
)
324
HORTICULTURAL REVIEWS
TABLE 7.1. (Continued) Preferred Svmbol Svnonvm
Character
Reference
*Wp-a
Wpa
Wrinkledpod-a.
Kolhe 1970
*Wp-b
Wpb
Wrinkledpod-b.
Kolhe 1970
X
Anthocyanin coloration in the vegetative parts.
Harland 1919b, 1920
xn
Xantha seedling. Chlorophyll deficient seedling. Homozygous lethal.
Krishnaswamy et al. 1945
Y
Verysmall eye seedcoat pattern.
Harland 1922
Ymr
Cowpea yellow mosaic virus resistance.
Bliss and Robertson 1971
Ystp
Yellow strip on petals.
Kolhe 1970
* Proposed new symbol.
cluded that the sterility observed in tetraploid cultivars was the most limiting factor to their economic utilization, the researchers noted that one of the autotetraploid cultivars in their study showed comparatively good fertility.
B. Plant Characters 1. Habit.-The data of Brittingham (19501, Premsekar and Raman (19721, and Krutman et al. (1975) indicate that the climbing characteristic is governed by a single dominant gene, which Brittingham (1950), designated T. Norton (1961) and Kolhe (1970) showed that the indeterminate or vining characteristic is conditioned by two duplicate genes. Norton (1961) assumed that one of thesegenes was Brittingham’s (1950) T gene and proposed that the second gene be designated V. Kolhe concluded that his results were in agreement with Norton’s (1961), but he proposed that the genes be designated V-1 and V-2.Since the symbol T was previously assigned by Spillman and Sando (1930) and the symbol V was previously assigned by Saunders (1959), I propose that these vining genes be redesignated Vi-1 and Vi-2. Shortly after Kolhe’s (1970) paper was published, Singh and Jindla (1971) released data suggesting that trailing growth habit is conditioned by two complementary genes and a third gene that is expressed only when both complementary genes are present in the homozygous recessive form. They proposed that these genes be designated T-1, T-2, and T-3, but I suggest that these symbols not be used. The symbol T was assigned earlier and T-1 and T-2 are probably redesignations for the Vi-1 and Vi-2 genes. I propose that the T-3 gene be redesignated Vi-3.
GENETICS OF VIGNA
325
Several authors have studied the genetics of various growth habit characteristics using biometrical techniques, and over 50 broad-sense heritability estimates have been published (Table 7.2). Although there is considerable variation among studies, the results indicate that such characteristics as plant height, vine length, leaf number, branch number, branch length, peduncle length, number pods per node, and stem girth should be considered to be a t least moderately heritable under most conditions. For example, the 19 heritability estimates for plant height ranged from 5.9 to 97.2% and averaged 45.1%. Two genes that control pod position in the foliage canopy have been described. Singh and Jindla (1971) showed that erect pod attachment is dominant to drooping pod attachment and conditioned by a single gene. The symbol they proposed for this gene, E, was used previously by Harland (1920) and I propose that it be redesignated Er. Krishnaswamy et al. (1945) assigned the symbol Pn to a dominant gene that conditions long peduncles. 2. Leaves.-Six genes that affect leaf size and shape have been described in the cowpea. Long leaf, Llf, is dominant to short leaf (Kolhe 19701, small leaf, Is,is recessive to large leaf (Krishnaswamy et al. 19451, and unifoliate leaf, un, is recessive to the normal trifoliate leaf (Rawal et al. 1976). Krishnaswamy et al. (1945) assigned the symbol L to a dominant gene that conditions lanceolate leaf shape, but this symbol was used previously by Harland (1919a). I propose that it be redesignated La. Saunders (1960b) and Kolhe (1970) each reported that a single dominant or partially dominant gene conditions the narrow leaf genotype, and Kolhe (1970) symbolized the gene Nlf. Jindla and Singh (1970) and Ojomo (1977) found that hastate leaf shape is inherited in a dominant manner. Although Jindla and Singh (1970) concluded that the trait is conditioned by four genes, Ojomo (1977) concluded that only one gene was involved. Since Jindla and Singh (1970) examined only a single Fz population, their findings must be interpreted as preliminary. Ojomo (1977) proposed the symbal Ha for hastate leaf.
3. Abnormalities.-The dwarf mutant, df, induced by Jones (1965), is recessive to normal habit and swollen stem base, Sw, is dominant to normal stem base (Sen and Bhowall961; Ojomo 1977).Saunders (1960b) showed that spindly growth habit is conditioned by a single recessive gene, which I propose be symbolized sh. The recessive gene ax activates the usually dormant buds in the axils of cotyledonary leaves, which permits the production of axillary branches not seen in normal plants (Krishnaswamy et al. 1945). Sharma (1969a,b) reported the repeated isolation of a “late giant” type mutation following dry seed treatment with chemical mutagens and he postulated that a wide-range mutator gene was responsible.
Tikka, Jaimini, Asawa and Mathur 1977 Trehan et al. 1970 Veeraswamy et al. 1973a
Lakshmi and Goud 1977 Sohoo et al. 1971
Kheradnam and Niknejad 1974 Kohli et al. 1971
Chandrappa et al. 1974 Erskine and Khan 1978
Reference Bapna and Joshi 1973
~ ~~
-
Branches Main Plant per Plant Peduncle Branch Height (no.) Length Length 45.3 48.8 29.6 38.8 51.0 13.9 5.9 41.8 49.8 15.0 34.6 44.4 58.6 51.3 20.1 47.7 42.8 43.7 43.3 29.6 6.0 38.5 17.5 33.5 41.0 97.2 58.3 61.3 72.5 94.4 67.8 74.2 66.5 40.3 24.2 24.6 22.8 57.9 61.3
~
-
82.0 94.9 77.0 -
-
-
-
Vine Length -
-
48.4 49.6 51.6 43.3 33.6
-
Stem Girth -
Pods per Leaves Cluster per Plant (no.) (no.) 89.5 63.7 30.2 28.9 24.7 33.7 -
TABLE 7.2. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR GROWTH HABIT TRAITS IN COWPEA, VlGNA UNGUICULATA h2 (%)
GENETICS OF VZGNA
327
4. Lethal Factors.-The first lethal gene in the cowpea was reported by Krishnaswamy et al. (1945), who described the gene xantha seedling, xn, as a homozygous lethal. Saunders (1952) showed that each of two lethal conditions was controlled by two complementary genes which, when both are present, bring about a delayed lethal condition in F1 seedlings. He proposed that the genes controlling the first lethal condition be designated L1 and Lz and those controlling the second lethal condition be designated L3 and Lq. Since the symbol L was first used by Harland (1919a), I propose that these four genes be redesignated Le-1, Le-2, Le-3, and Le-4, respectively. Saunders ( 1 9 6 0 ~later ) identified two other distinct lethal conditions, but he speculated that both were modifier gene-induced variants of the Le-3/Le-4 system.
C. Heterosis Some cowpea hybrids exhibit considerable heterosis for yield and most yield components (Agble 1972; Brittingham 1950; Capinpin and Irabagon 1950; Hawthorne 1943; Singh and Jain 1972; Ojomo 1974; Kheradnam et al. 1975; Mak and Yap 1977). Ojomo (1974) demonstrated that much of the heterosis in this species is due probably to the effect of dominance or epistasis. The cowpea also exhibits inbreeding depression, but usually a t a relatively lower level than heterosis (Singh 1975; Kheradnam et al. 1975; Mak and Yap 1977). Kheradnam et al. (1975) concluded that heterosis for seed yield is sufficient to warrant hybrid production if large-scale emasculation and crossing procedures can be developed. Several authors have studied heterosis for characteristics other than yield. Hofmann (1926) reported heterosis for plant height and stem diameter and Premsekar and Raman (1972) found heterosis for length and width of leaf and branch length. Mak and Yap (1977) examined seed protein content, but were unable to demonstrate significant heterosis for the trait. Premsekar and Raman (1972) and Erskine and Khan (1978) reported heterosis for earliness. Tikka, Sharma and Mathur (19761, however, found heterosis for earliness in only 4 of 28 Fl’s tested and concluded that flower initiation was governed by additive gene action.
D. Color Mann (1914) demonstrated that two kinds of sap-soluble pigments, a melanin-like substance and anthocyanin, are responsible for color in the cowpea. The melanin-like pigment is found only in the seed coat and it conditions a basal color ranging from very pale yellow to deep copper red. This pigment is always present in the third cell layer and often in the
328
HORTICULTURAL REVIEWS
palisade or outer cell layer of all colored seed coats, but its amount and location vary. The palisade cell layer of some colored seed coats or variously localized areas in this layer also contains anthocyanin. The anthocyanin pigment produces various shades of purple and rose when the cell sap is acidic and various shades of blue and black when the sap is alkaline. This anthocyanin pigment also is responsible for all color in the petals, seed pods, peduncles, petioles, stems, and leaves of the plant. The colors of various plant organs are correlated. The melanin-like pigment can develop only in the presence of a general color factor, and this factor and an anthocyanin pigment factor must be present before anthocyanin synthesis can occur. The multiple effects of these and several other color genes are discussed below. 1. Seed Coat Color.-Spillman (1912) was the first to attempt an explanation of the complex inheritance of seed coat color in cowpea. He postulated that the general color factor, C, is necessary for color expression and its absence results in white seeds. The C factor in combination with R, U, Br, Br and N, and N a n d B conditions red, buff, brown, black, and blue seed coat colors, respectively. Later, Harland (1919a,b, 1920) proposed a similar model. In this model R conditions red seed coat color and functions as a general color factor with B, N, M, and N a n d M conditioning black, buff, maroon, and brown, respectively. In a relatively comprehensive review, Spillman and Sando (1930) presented a revised version of Spillman’s (1912) model. They redesignated the general color factor as R and described N as an anthocyanin pigment factor. Additionally, they used the symbols B, F, P, and U for brown, fine and dense speckling, purple, and buff, respectively, and showed how the R, N, B, F, P, and Ugenes interacted to produce ten different seed coat colors. Harland’s (1919a,b, 1920) and Spillman and Sando’s (1930) use of the symbol R for the general color factor utilizes the symbol that Spillman (1912) used earlier for red seed coat. I suggest that Spillman’s (1912) original designation for the general color factor, C, be used. Harland’s (1919a,b, 1920) symbols B and N were used previously by Spillman (19121, and I suggest that they be redesignated B1 and Bf, respectively. Similarly, Spillman and Sando’s (1930) symbols B and P were used previously by Spillman (1912) and Harland (1919a,b, 19201, respectively, and I suggest that Spillman’s (1912) original designation for brown seed coat, Br, be used and that the gene for purple seed coat be redesignated Pr. Harland’s (1919a,b, 1920) model appears to be compatible with the more comprehensive model of Spillman and Sando (1930). Harland’s (1919a,b, 1920) Bf and M genes are probably Spillman and Sando’s (1930) U and Br genes, respectively. Harland’s (1919a,b, 1920) B1 gene
GENETICS OF VIGNA
329
functions much as Spillman and Sando’s (1930) N gene, but Harland’s (1919a) conclusion that the B1 gene does not condition anthocyanin production in the flowers, stems, and leaves suggests that B1 is not the anthocyanin pigment factor N . Table 7.3 illustrates the Spillman and Sando (1930) model for seed coat color using the proposed new symbolization. Subsequent to the early work of Spillman (19121, Harland (1919a,b, 1920), and Spillman and Sando (1930), several other studies on the genetics of seed coat color were published. Many of the genes identified in these studies, however, are probably redesignations for genes in the Harland (1920) or Spillman and Sando (1930) models. Capinpin (1935) described two genes, B, a basic pigmentation gene, and C, a color modifying gene. Since the B and C symbols were assigned previously, I suggest TABLE 7.3. INTERACTION OF SPILLMAN AND SANDO’S (1930) PIGMENT FACTORS FOR THE PRODUCTION OF SEED COAT COLOR IN THE COWPEA, VlGNA UNGUICULA TA
Gene Symbol (See Table 7.1)
Color Anthocyanin Purple Black Dull black Blue Red Melanin-like Coffee Maroon Buff or clay Pink White or cream
Necessarv
Permissable
Not Permissable
CNPr CNBrU CNBr CNFU CN
Br U
CBr U C Br CU
Pr Pr Nor Pr Pr
N NU Nand Pr, Br NBr U
N B r Pr U
c
c
Pr Pr U Pr PrBr U
that Capinpin’s (1935) B and Cgenes be redesignated Bs and Cr, respectively. Brittingham (1950) proposed the symbol Bu for a gene conditioning buff seed coat color; Krishnaswamy et al. (1945) proposed the symbol Kh for a gene conditioning khaki seed coat color; and Kolhe (1970) proposed the symbol Bg for a gene conditioning brown grain color. Chambliss (1974) proposed the symbol g t for a recessive gene that conditions a green seed coat. Louis and Sundaram (1975) induced a single gene mutation that removed the anthocyanin pigment from the seed coat of a blackeye cultivar. Saunders (1959) collected data on seed coat colors during the course of extensive breeding experiments and successfully explained his observations using Harland’s (1919a, 1920) model. In an abstract published without supporting data or references to previous work, Franckowiak and Barker (1974) assigned the gene sym-
330
HORTICULTURAL REVIEWS
bols Bh, Bg, BP, V , N,and M for black, black with gray, purple, dark brown, buff, and maroon seed coat colors, respectively. The symbols B, N , and M are apparently those of Harland (1919a,b, 1920). Since I have recommended that Harland’s (1919a,b, 1920) B and N genes be redesignated B1 and Bf, respectively, I suggest that the same symbolization be used for the Franckowiak and Barker (1974) genes. However, I suggest that B1 and not Blh be used for black. The Bl, Blg, and B1P genes are allelic. Since the symbol V was assigned previously, I suggest that dark brown gene be symbolized Db. B f is a dominant inhibitor of red pigmentation; M conditions maroon seed coat color only in Bf Bf genotype plants. Although generally the genetics of seed coat color appear to be understood, there undoubtedly are interactions and modifier genes that are not yet understood. For example, Capinpin and Irabagon (1950) reported that pale purple, drab color seed coat is a simple dominant over dark Corinthian purple. Although either of Spillman and Sando’s (1930) “permissible” factors for purple, Br or U, may account for variation in purple pod color, the exact identification of the gene described by Capinpin and Irabagon (1950) cannot be made by use of the Harland (1920) or the Spillman and Sando (1930) models. +
+
2. Flower Color.-Anthocyanin is the color pigment responsible for the purple or violet flower color that is characteristic of most cultivars. The principal flower colors are dark, pale, tinged, and white. The presence and the extent of development of anthocyanin are associated with seed coat color and pattern (Spillman 1913; Harland 1919a; Saunders 1960a). Dark flowers have much anthocyanin and are characteristic of cultivars with self-colored or Watson-eye seeds. Pale flowers have small amounts of anthocyanin on the wings and are associated with all eye and Holstein seed coat patterns. Tinged flowers have a faint narrow band of violet pigmentation along the outer edge of the standard and are associated with the hilum ring seed coat pattern. White flowers are devoid of anthocyanin and are indicative of white or cream seed coats. Spillman (1912, 1913) noted that the presence of anthocyanin in the flowers is dependent on the presence of the general color factor C and the anthocyanin factor N. Harland (1919a) found that flower color is due to the interaction of two factors which he designated L and D. The L factor conditions pale flower color and the D factor increases the amount of anthocyanin but has no visible effect except in the presence of L. Later, Harland (1920) proposed the symbol G for the gene that conditions tinged flower color. He noted that G produces tinged type flowers in plants with white seeds. Harland (1919a) speculated that dark flower color and Watson seed coat pattern were manifestations of a single factor. Yarnell (1965) suggested that L is likely the general color factor
GENETICS OF VZGNA
331
C. Sen and Bhowal (1961) presented evidence that tinged flower color was a secondary characteristic of the h gene for Holstein seed coat pattern. Saunders (1960a) pointed out that white flowers may be due to either the absence of the general color factor C or the absence of certain complementary genes for seed coat pattern. He noted that dark flower color is epistatic to the pale and tinged colors. Krishnaswamy et al. (1945) proposed the symbol St for a spreading factor that is responsible for full expression of color on the dorsal surface of the standard petal. Kolhe (1970) found yellow strips on the dorsal surface of the standard to be dominant over yellow and conditioned by a gene that he designated Ystp. Kolhe (1970) also proposed the symbol P f for a gene that conditions purple flower color over white, but this gene is probably either the general color factor C or one of the complementary genes for seed coat color or pattern. 3. Pod Color.-Many cultivars bear pods that contain anthocyanin and are partially or wholly purple in color. Harland (1920) showed that wholly purple pods are dominant to green pods and conditioned by a single gene that he designated P. Harland (1920) also noted that both the B1 factor for black seed coat and the E factor for New Era seed coat pattern condition purple pod tips, and he suggested that both factors might be allelic to P. Later, Mortensen and Brittingham (1952) concluded that P is allelic to B1 and they proposed that these genes be redesignated P and P,respectively. They observed that P is dominant to P in pod color but recessive to it in seed coat color and noted that it should be impossible to obtain a true-breeding plant with both purple pod and black seed coat, as such a plant would be of the genotype P P. Sen and Bhowal (1961) described three more P locus alleles, p t , p', and pg, and identified two additional genes, Ps and Pu, that condition anthocyanin pigmentation in the pod. The p t , p', and pg alleles conditioned green pod with purple tip, green pod with purple ventral suture, and purple pod with green sutures, respectively; except for a reversal of dominance in the hybrid p' pg a t unripe and semiripe stages, dominance was in accordance with increasing pigmentation. The gene Ps conditioned green pod with purple sutures, purple tip, and scattered small purple patches. The Pu gene conditioned completely purple pods; the Put allele conditioned green pod with faintly purple suture and tip. Mortensen and Brittingham (1952) considered drab pod color as a distinct color class and proposed the symbol k for a recessive gene that they speculated conditioned the color. Saunders (1960a) proposed the symbol Y for a gene that conditions brown or drab pod color over straw color, the symbol C for a gene that in the absence of P conditions cerise pod color, and the symbol S for a gene that conditions speckled pod. Since
332
HORTICULTURAL REVIEWS
these symbols were assigned previously to other genes, I propose that Saunders’ (1960a) Y, C, and S genes be redesignated Bp, Ce, and Sk, respectively. Capinpin (1935) found that black pods are dominant over white and conditioned by a single gene that he designated B. The symbol B was assigned previously, and I propose that Capinpin’s (1935) B gene be redesignated B k . Hare (1956) reported that yellow pod color is monogenically dominant to golden and red pod colors. Sen and Bhowal (1961) noted that the brownish-straw and amberstraw colors of dry pods are monogenically dominant over straw color. Krishnaswamy et al. (1945) showed that the two complementary factors Il and I2condition the straw yellow color of dry pods and the factor Cbr converts the straw yellow color to cocoa brown color. Since the symbol I was used previously, I propose that Krishnaswamy et al.’s (1945) Il apd I2 genes be redesignated Sy-1 and Sy-2, respectively. Any plant homozygous recessive a t one or more of the Sy-1, Sy-2, or Cbr loci bears ivory yellow pods. Several studies reporting genes that condition different degrees of green pod color have been published. Krishnaswamy et al. (1945) and Premsekar and Raman (1972) found that light green pods are recessive to green pods and are conditioned by a single gene. Krishnaswamy et al. (1945) designated their gene lg. Sen and Bhowal (1961) proposed the symbols GD, G, and g for genes conditioning dark green, green, and yellow green pod colors, respectively. They noted that these genes were allelic and appeared to condition similar color responses in the leaf, calyx, and dorsal surface of the standard. Since the symbol G was used by Harland (1920) for tinged flower color, I propose that Sen and Bhowal’s (1961) GD,G, and g genes be redesignated Gnd,Gn, and gny, respectively. Kolhe (1970) and Singh and Jindla (1971) reported a gene that conditioned green pod color over cream or white pod color. Kolhe (1970) assigned the symbol Gp to his gene and Singh and Jindla (1971)proposed the symbol G. I suggest that the Singh and Jindla’s (1971) G gene be redesignated Gnp. 4. Foliage Color.-If the general color factor C and anthocyanin factor N are present, several green plant parts other than the pods can exhibit purple pigmentation (Spillman 1912). Harland (1919b, 1920) reported that the factor X conditioned anthocyanin production in the vegetative parts. He also noted that P, B1, and E caused development of anthocyanin in the calyx and peduncle. Sen and Bhowal (1961) reported that Pu conditioned completely purple stem and petiole, pg conditioned a partly colored stem having reddish purple patches on the nodes and internodes and purple streaks on the petioles, p i conditioned stems with purple spots a t the internodes, Pb conditioned purple petiole base, Pbr
GENETICS OF VZGNA
333
conditioned purple branch base, and p" conditioned the spread of purple color on the calyx. Venugopal and Goud (1977) found that two independent genes governed the presence of pigmentation in the nodal regions of the main stem and the bases of tertiary branches, peduncles, and stalks of trifoliate leaves. They proposed the symbols PI and P2for these genes, but I suggest that they be redesignated Pp-1 and Pp-2. Krishnaswamy et al. (1945) reported that purple cotyledon is monogenically dominant over white cotyledon, and they proposed that this gene be symbolized Pcot. Saunders (1960a) observed that plants with pale green plant color have a noticeable degree of chlorophyll deficiency. He proposed the symbol g for the recessive gene that conditions this trait, but this symbol was used previously. I suggest that it be redesignatedpg. Kolhe (1970) found that light green foliage color is dominant to green and conditioned by the two complementary genes Lg-a and Lg-b. Since Krishnaswamy et al. (1945) used the symbol lg for light green pod, I propose that Kolhe's (1970) Lg-a and Lg-b genes be redesignated Lgf-1 and Lgf-2. Sen and Bhowal(1961) noted that the allelic series Gnd, Gn, and gnYfor dark green, green, and yellow green pod colors, respectively, appeared to condition similar color responses in the leaf, calyx, and dorsal surface of the standard. Singh and Jindla (1971) proposed the symbol Gr for a factor that conditions green bud color over white. Premsekar and Raman (1972) reported that dark green calyx is dominant to pale green and observed that the segregation pattern of an F2 population suggested monogenic inheritance. Kolhe (1970) proposed the symbol Bcy for a gene that conditions brown calyx color over green.
E. Flowers and Flowering 1. Compound Inflorescence.-Sen and Bhowal(1961) found that compound inflorescence is monogenically recessive to the normal simple inflorescence. They proposed that this gene be designated C, but this is the symbol for the general color factor. I suggest that the gene for compound inflorescence be symbolized Ci. 2. Photoperiod.-Many cowpea cultivars are photosensitive and the expression of the reproductive phase is influenced by varying daylength. Sene (1967) showed that a pair of major genes probably conditioned photoperiod response. Short-day response was dominant over photoperiod-insensitive response. Singh et al. (1974) demonstrated that it is possible to develop photoperiod-insensitive cultivars.
3. Outcrossing Mechanisms.-The development of population improvement breeding schemes for self-pollinated crops has stimulated the
334
HORTICULTURAL REVIEWS
search for male sterility and other outcrossing mechanisms to facilitate hybridization procedures. The high cost of hybrid seed also prohibits commercial exploitation of heterosis. Sen and Bhowal (1962) reported finding a male-sterile mutant in ‘Poona’. The floral parts of this mutant were reduced in size and the anthers aborted. The sporogenous tissue in the anthers was reduced and meiosis did not proceed beyond early diakinesis. A single recessive gene, designated m s , was found to condition the trait. Later, Rachie, Rawal, Franckowiak, and Akinpelu (1975) described another recessive male-sterile gene that they designated ms-2. They also described a type of mechanical male sterility involving petals constructed in such a way as to restrict stamen development, but still allow the stigma and style to emerge a t an early, pre-receptive stage of development. This trait was found to be governed by a single recessive gene that was designated constricted petal and symbolized cp. The gene cp was considered less promising than the ms-2 gene because of extremely poor fruit set. Appa Rao and Reddy (1976) induced a crumpled petal mutant conditioned by the recessive gene crpt, in which self-fertilization was restricted because the anthers were enclosed in the petals. Crumpled petal plants produced very few seeds. Rawal et al. (1978) showed that honey bees (Apis mellifera L.) could be used to pollinate male-sterile (ms-2 ms-2) cowpeas but they noted that flower color preference of the bees could lead to marked shifts in gene frequencies for dark seed coat colors because of pleiotropic association between flower pigmentation and seed coat colors. 4. Early Flowering.-The ability of a cultivar to mature early is a relatively important agronomic characteristic. Typically, earliness is measured by such criteria as days to flowering or days to maturity. Some reports suggest that early maturity is dominant or partially dominant over late maturity (Brittingham 1950; Ojomo 1971; Roy and Richharia 1948), while others suggest that late maturity is dominant or partially dominant over early maturity (Capinpin and Irabagon 1950; Mackie 1939). Roy and Richharia (1948) concluded that days to flowering is probably conditioned by two complementary genes; Ojomo (19711, however, thought that duplicate dominant epistasis between two designated major genes, Ef-1 and Ef-2, in the presence of some minor modifying genes was responsible. Brittingham (1950) postulated that maturity probably was inherited quantitatively. Several biometrical studies of the genetics of earliness parameters have been published (Table 7.4); the 26 computed broad-sense heritability estimates range from 3.8 to 95.1% and average 53.9%.Several authors concluded that the main genetic variation for earliness was due to additive gene action (Kheradnam and Niknejad 1971b; La1 et al. 1976;
GENETICS OF VZGNA
335
TABLE 7.4. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR EARLINESS PARAMETERS IN COWPEA. VlGNA UNGUlCULATA
Reference Bapna and Joshi 1973 Bordia et al. 1973 Erskine and Khan 1978
Kohlietal. 1971
Singh and Mehndiratta 1969 Sohoo et al. 1971 Tikka, Sharma and Mathur 1976 Tikka, Jaimini, Asawa and Mathur 1977 Trehan et al. 1970
Days to Flowering 94.3 84.8 60.5 3.8 14.9 0.0 17.0 0.0 66.8 34.4 26.5 31.6 25.6 88.8 91.9 59.4 91.4 38.8 47.1 95.1 4.4
Days to Pod Maturity 89.5 50.3 56.3 23.0 13.6 0.0 0.0 41.9 78.3 87.3 73.3 89.2 -
19.6
Mak and Yap 1977; Tikka, Sharma and Mathur 1976). Data of other authors, however, suggest that non-additive gene action and genotype by environmental interactions can be important in some instances. Ojomo (1974) found that specific combining ability and not general combining ability was significant, and he postulated that most of the genetic variation for days to flowering was due to dominance or epistasis. Tikka, Jaimini, Asawa and Mathur (1977) and Trehan et al. (1970) noted that the high heritability estimates for earliness were accompanied by comparatively low estimates for genetic advance. This, they pointed out, suggests that earliness is conditioned by effects other than additive gene action. F. Pods 1. Pod Size.-Pod length is moderately to highly heritable under most environmental conditions; published heritability estimates range from 0.0 to 97.5% and average 75.2% (Table 7.5). Much of the variation in pod length is due probably to additive gene action. Tikka, Jaimini, Asawa and Mathur (1977) and Veeraswamy et al. (1973) reported that the high heritability was accompanied by high genetic advance. Singh and Jain (1972), however, found that both general combining ability and specific combining ability were important for pod length, indicating that both
336
HORTICULTURAL REVIEWS
TABLE 7.5. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR POD TRAITS IN COWPEA, VlGNA UNGUlCULATA
h2 Reference Aryeetey and Laing 1973 Bapna and Joshi 1973
Bhowall976 Bliss et al. 1973 Bordia et al. 1973 Chandrappa et al. 1974 Erskine and Khan 1978
Kheradnarn and Niknejad 1974 Lakshrni and Goud 1977 Leleji 1975 Singh and Mehndiratta 1969 Sohooetal. 1971 Tikka, Jaimini, Asawa and Mathur 1977 Trehan et al. 1970 Veeraswarny et al. 1973a
Pod Lenzth 60.7 60.3I -
76.9 -
59.8 7.3 20.9 4.8 33.7 0.0 95.4 54.4' 80.5 94.8 75.9 87.0 95.0 24.6 97.5
Pod Girth -
-
-
95.3 -
-
-
-
-
-
-
-
(96) Pod Seedperpod Breadth (no.) 47.8 37.8l 78.9 52.2
53.0 50.6 94.0 22.1 23.1 44.8 23.9 9.6 64.0 70.1 41.73 64.2 74.3 98.9 68.4 86.3 23.5 33.3
Narrow-sense heritability estimate. Avg of 5 crosses. I Avg of 6 crosses.
I
additive and non-additive gene action can be important in some instances. Generally, long pods are dominant or partially dominant to short pods (Brittingham 1950; Capinpin and Irabagon 1950; Fennell 1948; Jindla and Singh 1970; Roy and Richharia 1948). Bhowal (1976) and Leleji (19751, however, reported that short pods are partially dominant to long pods. Except for Aryeetey and Laing's (19731 estimate of 0.44 effective factors, most of the published data indicate that a t least 2 genes condition pod length. Krishnaswamy et al. (1945) studied pod length in a subspecies sesquipedalis X subspecies cylindrica cross and suggested that two major genes were involved. They proposed the symbols Sp and Cy for genes that condition the long subspecies sesquipedalis-type pod and short subspecies cylindrica-type pod, respectively. Bhowal (19761, Brittingham (19501, and Capinpin and Irabagon (1950) suggested that six, eight, and two genes, respectively, conditioned the pod length. Fennell (19481, Jindla and Singh (19701, and Roy and Richharia (1948) concluded that the trait was conditioned by multiple factors.
GENETICS OF VIGNA
337
Bhowal (1976) found that narrow pod was partially dominant over broad pod. He reported a heritability estimate of 80.5% for pod breadth and suggested that the trait was governed by 10 genes. Chandrappa et al. (1974) reported a heritability estimate of 95.3% for girth of pod. 2. Seed Number.-The number of seeds per pod is moderately heritable; published heritability estimates range from 9.6 to 98.9%, but average only 52.8% (Table 7.5). Non-additive gene action accounts for a significant portion of the variation in this trait. Singh and Jain (1972), for example, found that specific combining ability and not general combining ability was important, and Tikka, Jaimini, Asawa and Mathur (1977) noted that the high heritability of seed number per pod was accompanied by a comparatively low genetic advance. Kheradnam and Niknejad (1971b), however, found that both general combining ability and specific combining were important. Leleji (1975) reported that fewer number of seeds per pod is partially dominant over larger number of seeds per pod. Aryeetey and Laing (1973) estimated that number of seeds per pod is conditioned by a single effective factor.
3. Seed Spacing.-Fennel1 (1948) noted that medium or uncrowded seed spacing within the pod is dominant over the wide spacing that is characteristic of the yard-long bean. He concluded that the trait was multigenic. Kolhe (1970) found that dense grain deposition was dominant to thin grain deposition and was governed by two complementary genes that he symbolized Dgd-a and Dgd-b. 4. Pod Texture.-Krishnaswamy et al. (1945) found that the wrinkled appearance of dry subspecies sesquipedalis-type pods is conditioned by the two complementary recessive genes pa-1 and pa-2. Kolhe (1970) studied similar material but he reported that wrinkled pod appearance was dominant to smooth pod appearance and was governed by 2 complementary genes that he designated Wp-a and Wp-b. Premsekar and Raman (1972) also studied a subspecies unguiculata X subspecies sesquipedalis cross and they found that the tough cowpea-type pod was dominant to the soft subspecies sesquipedalis-type pod and was conditioned by a single gene. The smooth pericarp of dry cowpea pods was dominant to the shrunken pericarp of dry yard-long bean pods and also was found to be governed by a single gene. I propose that Premsekar and Raman’s (1972) genes for soft subspecies sesquipedalis-type pod and shrunken pericarp be designated stx and shp, respectively. 5. Pod Shape.-Spillman and Sando (1930) proposed the symbol A for alfalfa-like curled pod shape. Alfalfa-like pod shape is semi-dominant to normal pod shape.
338
HORTICULTURAL REVIEWS
G. Seeds 1. Seed Size.-Seed size is an important agronomic trait and a major yield component. It is measured usually as 100-seed weights. Seed size is moderately to highly heritable; published heritability estimates range from 3.8 to 97.3% and average 66.2% (Table 7.6). Seed size of F1plants is usually intermediate between parents, but partial dominance for small seeds is sometimes evident (Mackie 1946; Leleji 1975; Bhowal 1976). Singh and Jain (1972) found that both general combining ability and specific combining ability were significant, but the data of Kheradnam and Niknejad (1971b) suggested that general combining ability is the more important. Singh and Mehndiratta (1969) reported that seed size had a high genetic advance. Aryeetey and Laing (19731, Bhowal(19761, and Sene (1968) estimated that ten, four, and six genes, respectively, conditioned seed size.
2. Seed Shape.-The long reniform seed shape that is characteristic of the subspecies sesguipedalis is dominant or partially dominant to the shorter and rounder seeds characteristic of most cowpea cultivars. Fennell(1948) and Brittingham (1950) suggested that multiple factor inheritance was involved, but Kolhe (1970) and Premsekar and Raman (1972) presented data indicating that the trait was monogenic. Kolhe (1970) proposed the symbol Lg for the gene conditioning long grain. However, this symbol was used previously by Krishnaswamy et al. (1945) and I propose that it be redesignated reniform shape seed, symbolized Rs.
3. Seed Coat Pattern.-Seed coat patterns are inherited independently of seed coat color. However, the appearance of any pattern is dependent upon the presence of the general color factor C. Spillman (1911) was one of the earliest to attempt an explanation of the inheritance of the common eye (pigmented area of partially pigmented seed coat) type patterns. He assigned the symbols w and h (Sen and Bhowal (1961) suggested that lower case letters be used) to the genes that condition Watson eye (indefinite eye margin) and Holstein seed coat patterns, respectively. Both patterns are recessive to solid seed color. Ordinary or small eye was w w h h and large eye was the heterozygote between the Holstein and small eye patterns w w h. Spillman and Sando (1930), however, concluded later that the big eye genotype was homozygous a t the h locus and heterozygous a t either or both the w andNu loci. Harland (1919a, 1920, 1922) described three additional seed coat pattern genes: h-2, a duplicate Holstein pattern gene; E, New Era pattern (dark blue irregular dots); and y, very small eye. He also concluded that seed coat mottling is indicative of the presence of the B1 gene in the heterozygous condition. Sasaki (1922) described a recessive gene which conditioned an
+
Narrow-sense heritability estimate. mg per g flour. g per 100 g protein. Avg of 7 crosses.
Tikka. Jaimini. Asawa and Mathur 1977
Kheradnam and Niknejad 1974 Lakshmi and Goud 1977 Leleji 1975 Singh and Mehndiratta 1969 Sohoo et al. 1971
Bordia et al. 1973 Chandrappa et al. 1974 Erskine and Khan 1978
Bhowal1976 Bliss et al. 1973
Bapna and Joshi 1973
Reference Aryeetey and Laing 1973
100-seed wt 63.0 37.4l 80.6 85.3 84.1 84.0 75.4 96.6 9.3 50.4 35.7 54.4 3.8 75.0 93.8 68.34 95.9 97.3 71.8 62.0 -
-
-
-
-
29.0 -
_-
%
Protein -
-
-
%
Cystine 34.02 27.03 -
-
-
54.O2 46.03 -
-
%
Methionine -
-
39.02 4.03 -
-
%
Tryptophan
96.0
-
-
-
-
-
-
-
-
-
-
Test wt -
TABLE 7.6. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR SEED TRAITS IN COWPEA, WGNA UNGUlCULATA
W
w w
340
HORTICULTURAL REVIEWS
eye pattern intermediate in size between large eye and Holstein patterns. Spillman and Sando (1930) described the following seed coat pattern genes: D, dense speckling; E, narrow eye; F, fine and dense speckling (blue color); G, dotting of Holstein seeds; S, spotting (patches of black pigment); T, Taylor pattern (thinly scattered bluish purple dots); W, Whippoorwill mottle pattern (irregular areas of dark shade separated by lighter areas); and X,Taylor inhibitor. The D, E, G, W, and X symbols were used previously and I suggest that Spillman and Sando's (1930) dense speckling, narrow eye, dotting, Whippoorwill, and Taylor inhibitor pattern genes be redesignated De, Na, Dt, Wh, and In-T, respectively. De is epistatic to T. Krishnaswamy et al. (1945) assigned the symbol Sm to the gene conditioning the smoky pattern (minute dots on maroon background). Saunders (1959, 1960b) identified the following seed coat pattern genes: V , mottling; E, stippling; S, speckled; and 0,hilum ring. Since the symbols E and S were assigned previously, I propose that Saunders' (1959, 1960a) genes for stippling and speckled patterns be redesignated Stp and Spk, respectively. The combination of V and Stp results in the mottling and stippling effect characteristic of 'Victor'. Several of the seed coat pattern genes, e.g., E, De, and Stp, may be allelic, but until allelism is proved I suggest that their identities be kept separate. Franckowiak and Barker (1974) concluded that several of the genes that condition seed coat patterns are alleles to the B1 gene (Franckowiak and Barker (1974) used Harland's (1919a,b, 1920) symbol B for the black seed coat gene) for black seed coat color. They assigned the following gene symbols: BL', black with light spots; BP, black spots; Bl', New Era pattern; Bl', Taylor pattern; Blf, blue; and bl", modifier of Blf. (See p. 328 for a discussion of other B1 alleles that condition seed coat color as reported by Franckowiak and Barker (1974).) Mottle seed coat was conditioned by the presence of the dominant factor Mu, mottled pattern. Several of these Bl alleles are probably genes described by earlier workers. However, Franckowiak and Barker (1974) published their work in abstract form and did not present any data or cite previous literature, which makes definitive reconciliation of findings impossible. Until further data are made available I suggest that the identity of Franckowiak and Barker's (1974) B1 alleles be kept separate from the genes described earlier. 4. Seed Coat Structure.-Loose testa is governed by the recessive gene It (Krishnaswamy et al. 1945). Spillman and Sando (1930) proposed the symbol L for a dominant gene that conditions longitudinal furrowing on the seed coat, but this symbol was used earlier by Harland (1919a). I propose that it be symbolized Lf. Ojomo (1972) showed that seed coat thickness is conditioned by the two duplicate genes Th and Co.
GENETICS OF VZGNA
341
5. Hollow Seeds.-Krishnaswamy et al. (1945) proposed the symbol hs for the single recessive gene that conditions hollow seeds.
6. Seed Protein.-Bliss et al. (1973) reported that percentage of protein and the amino acids cystine, methionine, and tryptophan are moderately heritable (Table 7.6). They noted, however, that the genotypic and phenotypic correlations of yield with percentage of protein, yield with methionine content, and 50-seed weight with tryptophan content were negative and relatively high.
H. Yield 1. Heritability Estimates and Gene Action.-The yields of the economically important reproductive and vegetative parts of the cowpea plant are moderately heritable under most environmental conditions (Table 7.7). Published broad-sense heritability estimates for the 2 most frequently measured yield parameters, pod number and grain weight, range from 7.0 to 97.4% and average 54.8% for pod number and 46.1% for grain weight; heritability estimates for fresh and dry fodder yields range from 13.6 to 98.6% and average 46.2%. Singh and Jain (1972) and Kheradnam and Niknejad (1971b) reported that both general combining ability and specific combining ability are important for grain yield, suggesting that both additive and non-additive gene action are important. The high genetic gain estimates for grain and/or pod yields reported by Singh and Mehndiratta (1969), Trehan et al. (19701, Veeraswamy et al. (1973a), and Tikka, Jaimini, Asawa and Mathur (1977) suggest that expression for yield is conditioned largely by additive gene effects. Kohli et al. (1971) reported a high genetic gain for fodder yield. 2. Character Association.-During the past decade there has been considerable interest in developing indirect selection schemes for increasing yield in cowpea. Successful application of such schemes is dependent upon the use of characters or yield components that are highly heritable, strongly correlated with yield, and without strong negative correlations with other yield components. Correlation, multiple regression, discriminant function, coheritability, and path coefficient analyses have been used to determine the potential value of various plant characters for use as indirect selection criteria for yield. A number of such studies have indicated that the principal yield components of pod number, seed number per pod, and seed size may have considerable value, either alone or in combination, in indirect selection schemes for grain yield (Bapna et al. 1972; Bordia et al. 1973; Chandrappa et al. 1974; Kumar et al. 1976b; Lian 1975; Janoria and Ali 1970; Lakshmi and Goud 1977; Premsekar and Raman 1972; Kheradnam and Niknejad 1974; Singh and Mehndir-
Narrow-sense heritability estimate.
Tikka, Jaimini, Asawa and Mathur 1977 Trehan et al. 1970 Veeraswamv et al. 1973a
Lakshmi and Goud 1977 Singh and Mehndiratta 1969 Sohoo et al. 1971
Kheradnam and Niknejad 1974 Kohli et al. 1971
Bliss et al. 1973 Bordia et al. 1973 Chandrappa et al. 1974 Erskine and Khan 1978
Bapna and Joshi 1973
Reference Aryeetey and Laing 1973
47.0 50.5 48.7
-
Clusters Per Plant (no.) -
41.9 56.1 97.4 94.8 83.2 94.5 21.4 62.8
-
Pods Per Plant (no.) 28.2 19.8' 62.6 44.3 7.0 36.8 68.0 44.6 51.5 47.0 62.8 46.8 44.0 -
70.0
-
-
-
86.8 -
-
(wt) -
PEt
Pods
-
-
-
-
-
-
55.3 35.8 -
-
Seeds Per Plant (no.) -
47.5 35.6 70.0 19.6 41.9
-
-
-
26.2 54.0 12.0 23.9 73.0 57.6 57.1 50.5 80.8 53.4 35.0
-
Seeds Per Plant (wt)
-
90.0 98.6 95.6
-
~
28.9 ~. 23.3 32.3 24.6
Fodder Yield (Fresh)
32.0 ~~. 13.6 23.6 14.9
Fodder Yield (Dry)
TABLE 7.7. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR YIELD PARAMETERS IN COWPEA, VlGNA UNGUlCULA TA hZ (%)
(fl
F; 8
c
M
!a
.p N
W
GENETICS OF VZGNA
343
atta 1969, 1970; Tikka and Asawa 1978; Tikka, Jaimini, Asawa and Mathur 1977; and Tikka et al. 1978); secondary characters such as cluster number, plant height, test weight, pod length, and peduncle length also may be of value (Bapna et al. 1972; Bordia et al. 1973; Kumar et al. 1976b; Lakshmi and Goud 1977; Lian 1975; Singh and Mehndiratta 1969; Tikka and Asawa 1978; Tikka, Jaimini, Asawa and Mathur 1977; and Tikka et al. 1978). Leaf number, plant height, branch number, branch length, stem girth, protein content, and digestibility have been shown to be potential indirect selection criteria for fodder yield (Chopra and Singh 1977; Dangi and Paroda 1974; Singh et al. 1977; Tyagi et al. 1978). The question of increased efficiency of indirect selection over direct selection for yield in cowpea appears to be unsettled. Aryeetey and Laing (1973) noted that pod number may be useful as a preliminary selection criterion but they concluded that the best criterion for selection to increase yield should be yield itself. Erskine and Khan (1977) reported that environmental effects accounted for most of the variation in grain yield. They observed that selection for pod number is promising, but expessed doubt about the feasibility of selecting for a high expression of pods per plant in combination with a high stability of pod number. Later, they presented data showing that direct selection for grain yield was more efficient than indirect selection for yield using pod number and seed number per pod as selection criteria (Erskine and Khan 1978). I. Resistance to Fungal and Bacterial Diseases 1. Anthracnose.-Cowpea anthracnose is incited by the fungus Colletotrichum lindemuthianum (Sacc. & Magn.) Bri. & Cav. Three major groups of resistance have been identified: immunity, hypersensitivity, and field resistance (Anon. 1976). There is some evidence that hypersensitivity resistance is conditioned by a single dominant gene.
Bacterial Canker.-Bacterial canker is known also as bacterial pustule, bacterial blight, and bacterial spot.The disease is incited by the bacterium Xanthornonas uignicola Burk. The data of Lefebvre and Sherwin (1950) indicate that resistance is conditioned by a single dominant gene. Singh and Pate1 (1977a) identified two resistance genes. They showed that resistance in an ‘Iron’ accession was governed by a single recessive gene and resistance in the lines P-309, P-426, and P-910 was governed by a single dominant gene. I propose that Singh and Patel’s (1977a) dominant and recessive bacterial canker resistance genes be symbolized Bc-1 and bc-2, respectively. Resistance in some lines appears to be controlled by two genes (Anon. 1976). 2.
344
HORTICULTURAL REVIEWS
3. Cercospora Leaf Spot.-Cercospora leaf spot is incited by Cercospora cruenta Sacc. and C. canescens Ell. & Martin. Both the dominant gene Cls-1 and the recessive gene cls-2 condition a high level of resistance to the leaf spot caused by C. cruenta (Fery et al. 1976). The genes are not allelic or linked (Fery and Dukes 1977). 4. Charcoal Rot.-Charcoal rot is also known as ashy stem blight. The disease is incited by the fungus Macrophomina phaseolina (Tassi) G. Goid. ‘Iron’, ‘Victor’, and ‘Brabham’ are resistant and the resistance is dominant (Mackie 1934, 1939). 5. Fusarium Wilt.-Fusarium wilt is incited by the fungus Fusarium oxysporum Schlecht. f. tracheiphilum (E. F. Sm.) Snyd. & Hans. ‘Iron’ is resistant to all three races of the organism that have been identified (Mackie 1934). Hawthorne (1943) and Hare (1957) presented evidence that resistance to Race 1 is probably conditioned by a single dominant gene. Hare (1957) concluded that resistances to Races 2 and 3 are controlled by two major dominant genes.
0. Powdery Mildew.-Erysiphe polygoni DC. ex St. Amans is the causal organism of powdery mildew. Dundas (1939) reported that resistance in yard-long bean and ‘Blackeye’ is due to a single dominant gene. Fennell (1948) examined the resistance in the yard-long bean and found that it is inherited as a recessive trait. He concluded that resistance is under quantitative control. Fennell (1948) speculated that the existence of E. polygoni strains might explain the difference between his results and those of Dundas (1939). 7. Rust.-Cowpea rust is incited by Uromyces phaseoli (Reben.) Wint. var. uignae (Barcl.) Arth. Resistance has been identified and it is thought to be conditioned by a single dominant gene (Anon. 1976).
8. Stem Rot.-Resistance to cowpea stem rot, a disease incited by the fungus Phytophthora uignae Purss, is governed by a single dominant gene (Purss 1958). The gene, which is present in ‘California Blackeye No. 5’, conditions almost an immunity. I propose that this gene be symbolized Sr. Partridge and Keen (1976) concluded that the basis for the expression of this gene is a specific derepression of kievitone biosynthesis. 9. Target Spot.-‘VITA-3’ contains a single recessive immunity gene to target spot, a disease incited by the fungus Corynespora casiicola (Berk. & Curt.) Wei (Anon. 1976). 10. Verticillium Wilt.-Moore (1974) showed that a single dominant gene conditions resistance to Verticillium wilt, a fungal disease incited by Verticillium albo-atrum Reinke & Berth, in the line M 62. I propose that this gene be designated Vw.
GENETICS OF VIGNA
345
J, Resistance to Virus Diseases 1. Bean Yellow Mosaic Virus.-Reeder et al. (1972) studied the inheritance of bean yellow mosaic virus (BYMV) resistance in Plant Introduction (PI) 297562 and concluded that resistance is governed by a single recessive gene. I propose that this BYMV resistance gene be symbolized by. 2. Cowpea Chlorotic Mottle Virus.-PI 255811 is resistant to cowpea chlorotic mottle virus (CCMV), and the resistance is controlled by a major recessive gene (Rogers et al. 1973). I propose that this CCMV resistance gene be symbolized cc.
3. Cowpea Mottle Virus.-Bliss and Robertson (1971) studied the inheritance of tolerance to cowpea mottle virus. Tolerance is dominant and the observed segregation ratios are indicative of a qualitative inheritance mechanism, probably one or two genes. 4. Cowpea Yellow Mosaic Virus.-Three additive loci are responsible for tolerance to cowpea yellow mosaic virus (CYMV) (Bliss and Robertson 1971). ‘Alabunch’ is probably homozygous resistant for all three genes. ‘Dixielee’ is resistant to CYMV due to the dominant gene Ymr. The Ymr resistance gene segregates independently of the three tolerance genes.
5. Cucumber Mosaic Virus.-Sinclair and Walker (1955) studied cucumber mosaic virus (CMV) resistance in F1, Fz,and F3 progenies and proved that resistance is dominant and governed by a single gene pair. Khalf-Allah et al. (1973) conducted a similar study and their results support the single dominant gene hypothesis. DeZeeuw and Crum (1963) used the symbol C for this gene, but C is the symbol for the general color factor. I propose that the CMV resistance gene be symbolized Cm. 6. Southern Bean Mosaic Virus.-Brantley and Kuhn (1970) studied hypersensitive-type resistance to southern bean mosaic virus (SBMV) and demonstrated that the resistance was conditioned by a single dominant gene. I propose that the SBMV resistance gene be designated Sbm. 7. Tobacco Ringspot Virus.-DeZeeuw and Ballard (1959) showed that a single dominant gene governs a hypersensitivity-type resistance to tobacco ringspot virus (TRSV). Later, deZeeuw and Crum (1963) presented evidence for the existence of an epistatic inhibitor of TRSV susceptibility. They used the previously assigned symbol T for the TRSV resistance gene. I suggest that this symbol be changed to Tr.
346
HORTICULTURAL REVIEWS
K. Resistance to Root-knot Nematodes Root-knot is a severe disease of cowpea caused by several species of the root-knot nematode genus Meloidogyne. M. incognita (Kofoid & White) Chitwood is the most common species pathogenic on cowpeas, but M. javanica (Treub) Chitwood, M. arenaria (Neal) Chitwood, and M. hapla Chitwood also are economically important pests. Webber and Orton (1902) were the first to recognize the existence of naturally resistant ‘Iron’ cowpea plants, and Orton (1913) found that resistance is dominant and can be recovered from progeny generations of crosses between ‘Iron’ and several susceptible cultivars. Hare (1959) reported that ‘Iron’ and four breeding lines are resistant to M. incognita, M. incognita acrita Chitwood & Oteifa, M. jauanica, and M. arenaria. He studied the inheritance of resistance to M. incognita in 80 F3progenies of a resistant by susceptible cross. Eighteen progenies were resistant, 38 were segregating, and 24 were susceptible, and the segregation ratio in the segregating progenies was 2.3 resistant to 1 susceptible. On the basis of these data, he suggested that resistance to M. incognita is governed by a single dominant gene. Amosu and Franckowiak (1974) inoculated several F2 progeny populations of resistant by susceptible crosses with M. incognita and their data support the single dominant gene hypothesis. Fery and Dukes (1979) studied parental, F1, FP,and backcross populations of a resistant X susceptible cross, and demonstrated that resistance to M. incognita is controlled by a single dominant gene. Additionally, they tested 30 Fs progenies of the cross against M. incognita, M. javanica, and M. hapla. The distributions of the 30 F3 families in the 3 tests were similar and this indicates that the gene that conditions resistance to M. incognita also conditions resistance to M. javanica and M. hapla. Fery and Dukes (1979) designated the root-knot resistance gene Rk. L. Resistance to Insects 1. Beetle.-Kolhe (1970) assigned the symbol Rh to a recessive gene conditioning resistance to an unidentified beetle storage pest. Since the gene is recessive, I suggest that it be symbolized rh and not Rh. 2. Cowpea Curcu1io.-The cowpea curculio, Chalcoderrnus aeneus Boheman, is a major cowpea pest in southern and eastern United States. Also, feeding and oviposition punctures of the adult curculio provide entry points for a fungus (Choanephora cucurbitarum (Berkeley et Ravenel) Thaxter) that incites a serious pod rot (Cuthbert and Fery 1975). Youngblood and Chambliss (1973) studied the inheritance of cowpea curculio resistance in F2and backcross generations, but were unable to find any apparent segregation patterns. They concluded that resis-
GENETICS OF VZGNA
347
tance is inherited quantitatively. Cuthbert et al. (1974) showed that resistance is dependent upon various levels of nonpreference, a pod factor inhibiting penetration through the pod wall by the adult, and antibiosis. They demonstrated that each of the three mechanisms is under genetic control and could be transmitted to progeny. Fery and Cuthbert (1978) showed that the nonpreference resistance factor is inherited in a partially dominant manner and found that broad-sense heritability estimates for the trait ranged from 0 to 19%.They suggested that selection in the seedling stage for low amounts of adult curculio feeding can increase the frequency of plants with nonpreference type-resistance. Fery and Cuthbert (1975) calculated the narrow- and broad-sense heritability estimates for pod factor resistance to be 45% and 49%, respectively. They found that gene action is additive and estimated the number of genes conditioning resistance to be one pair. Later, they presented findings indicating that pod wall resistance can be evaluated efficiently by means of pod:seed ratio measurements (Fery and Cuthbert 1979). 3. Pod Borer.-Wolley (1977) studied the inheritance of resistance to the pod borer Maruca testulalis Geyer. Resistance is dominant and probably conditioned by several genes.
M. Gene Linkage Reported instances of gene linkage in cowpea are listed in Table 7.8. Additionally, Spillman and Sando (1930) suggested that Pr, Br, De, T, F, and probably S are linked. Brittingham (1950) reported instances of linkages between qualitative genes and genes conditioning quantitative traits. He demonstrated the following linkages: (1) Vi-1 and early pod maturity, (2) C and pod length, (3) Bu and pod length, and (4) C and seed size. Saunders (1960b), however, suggested that the associations between the general color factor and pod length and seed size should be interpreted as being due to multiple effects of the C gene rather than to linkage. Saunders (1960b) noted an association between seed coat color and date of maturity and suggested that this might be an instance of quantitative-quantitative linkage. Similarly Roy and Richharia (1948) thought that pod length and pod-wall fibrousness might be linked. Harland (1920) stated that B1,P, and E are so closely linked that crossingover seldom occurs. He suggested that these factors might be allelic.
N. Interspecific Hybridization All attempts to hybridize the cowpea with other Vigna species have been unsuccessful. Evans (1976) reported unsuccessful attempts to cross the cowpea with V. uexillata (L.)A. Rich., V. mungo (L.)Hepper (black
348
HORTICULTURAL REVIEWS
TABLE 7.8. LISTING OF PUBLISHED LINKAGE RELATIONSHIPS IN COWPEA, VlGNA UNGUlCULATA
Linkage Relationship’ Bf - V
Bg Bg Bl
B1 B1 B1
-
p Cm
E F 0
P
P‘ P‘
Pf
Pf
Ystp - BP - Ce - E - P -
-
-
Tr
P T
P sh
- Pb - Pbr - Ystp
Pg - W Sk - SP k Wp-a - Dgd-a
I
Cross-over Fre uency ?%)
25.5 20.3 39.5 34.4 -2 -2
20.0 20.0 25.0,” -2
-2
15.4 34.6 19.9 13.5 20.4 23.4 -2
5.8
Reference Saunders 1959 Kolhe 1970 Kolhe 1970 Saunders 1960b Saunders 1960b Harland 1920 Harland 1920 Saunders 1960a,b Saunders 1960b deZeeuw and Crum 1963 Harland 1920 Spillman and Sando 1930 Saunders 1960b Saunders 1960b Sen and Bhowall961 Sen and Bhowall961 Kolhe 1970 Saunders 1960b Saunders 1960a Kolhe 1970
Preferred gene symbols used (see Table 7.1). linked. Estimated value.
* Tightly :3
gram), V radiata (L.) Wilczek (mung bean), V. umbellata (Thunb.) Ohwi & Ohashi (rice bean), V. aconitifolia (Jacq.) Marechal (moth bean), and V. angularis (Willd.) Ohwi & Ohashi (adzuki bean). Singh et al. (1964) found that the cross V. umbellata X V. unguiculata was completely cross-sterile. Ballon and York (1959) attempted intergeneric crosses between the cowpea and the scarlet runner bean (Phaseolus coccineus L.) and the common bean (P. uulgaris L.), but were unable to obtain any hybrid plants.
V. MUNG BEAN The mung bean (V. radiata (L.) Wilczek) is widely grown in southern Asiatic countries. It is also popular in the United States, where 9 million kilos are used annually for sprouting by commercial processors and Oriental restaurants (Anon. 1975). About one-fourth of the mung beans consumed in the United States are grown domestically, primarily in Oklahoma. The mung bean is commonly known in the Asiatic countries as green gram. Other common names include golden gram, mash, moong, Chickasaw pea, Oregon pea, and chop suey bean. The mung bean is a self-pollinated crop and cleistogamy is sometimes prevalent (Narasimham 1929; Purseglove 1968). Natural cross-fertilization of 2.8 to 3.0% (van Rheenen 1964) and 0.5% (Empig et al. 1970) has been reported. De-
GENETICS OF VIGNA
349
tailed hybridization procedures have been published by Sen and Ghosh (1959), Boling et al. (19611, and Singh and Malhotra (1975). A total of 45 genes has been described for the species (Table 7.9). TABLE 7.9. LIST OF MUNG BEAN, WGNA RADIATA, GENES
Preferred Symbol Synonym Character A Green seed coat color.
Reference Bose 1939; van Rheenen 1965
*ab
Almond biscuit pod color.
Sen and Ghosh 1959
a1
Albino seedling.
Sen and Ghosh 1960b
B
Dark green seed coat color.
Bose 1939
bf
Buffseed coat color.
Sen andGhosh 1959
*Bl
B1ue seed coat color.
Sen and Ghosh 1959
*Bla
Black seed coat color.
Murty and Patel 1972
'Bls
Bacterial leafspot resistance.
Thakur et al. 1977c
Colorless plant pubescence (N must be present).
Sen and Ghosh 1959
Brown seed coat color.
Murty and Patel 1972
BSP
Black spot on seed coat.
K.B. Singh and J.K. Singh 1970
C
Dull, rough seed surface. Dominant to glossy, smooth seed surface.
Bose 1939: Sen and Ghosh 1959: van Rheenen 1965; K.B. Singh and J.K. Singh 1970
*c-2
Dull, rough seed surface-2. Dominant to glossy, smooth seed surface.
Sen andGhosh 1959
* c1
Single cluster per node. Dominant over 3 clusters per node.
T.P. Singh and K.B. Singh 1970
Cucumber mosaic virus, mung bean strain, resistance.
Sittiyos et al. 1979
*DP
Dense plant p u bescence. Dominant to medium intensity pubescence.
Murty and Patel 1973
E
Lobed leaf margin. Dominant over entire leaf margin. Heterozygote is intermediate.
Singh and Mehta 1953; Sen and Ghosh 1959
F
Cercospora leafspot resistance.
Thakur et al. 1977c
G
Green seed coat color. Dominant to greenish-yellow .
Sen andGhosh 1959
Br 'Brn
Cmm
350
HORTICULTURAL REVIEWS
TABLE 7.9. (Continued)
*Gn
Green seed coat color.
*Grn
Bottlegreen seed coat color.
Singh 1973
I-1
Simple inflorescence-1 ( I - 2must be present).
Sen and Ghosh 959
I-2
Simple inflorescence-2 (I-1 must be present).
Sen and Ghosh 959
Ic
Incised leaflets. Dominant to ovate shape leaflets.
Pokle 1972
Inhibitor of albino seedling, al.
Sen and Ghosh 1960b
La
Lanceolate leaf. Semidominant and lethal when homozygous.
Singh and Saxena 1959
lP
Light popcorn pod color.
Sen and Ghosh 1959
M
Mosaic seed coat pattern.
Murty and Patel 1972
N
Colorless plant pubescence (Br must be present).
Sen andGhosh 1959
0
Light-yellowish olive flower color and deep red veins on pod sutures. Partially dominant to olive yellow flowers and green pod sutures.
Bose 1939
P
Purple hypocotyl. Dominant to purple spotted hypocotyl.
Sen and Ghosh 1959
* Pe
Purple epicotyl. Dominant to purple spotted and green epicoty 1.
Sen and Ghosh 1959
*pes
Purple spotted epicotyl. Dominant to green epicotyl.
Sen and Ghosh 1959
Palegreen flower color. Dominant topgbandpg".
Murty and Patel 1973
*pgb
Bryta yellow flower color. Dominant to pg".
Murty and Patel 1973
*Pg"
Naphthalene yellow flower color.
Murty and Patel 1973
*Ph
Purple hypocotyl.
Swindell and Poehlman 1978
Ps
Pho toperiod sensitive
Swindell and Poehlman 1978
R
Red color of cotyledons, hypocotyl, and top of leaflet stalk.
van Rheenen 1965
*2' n d
GENETICS OF VIGNA TABLE 7.9. (Continued) Preferred Symbol Synonym Character *SP (S) Spotted seed coat.
Reference van Rheenen 1965
T
Twining habit.
Sen and Ghosh 1959
TP
Swollen pod tip. Dominant to tapering pod tip.
Sen and Ghosh 1959
v
Mung bean yellow mosaic virus resistance.
Thakur et al. 1977c
Y
Yellowishgreen seed coat color. Gene Yg must be present.
Singh 1973
Yellowishgreen seed coat color. Gene Ymust be present.
Singh 1973
* yg
(P)
351
* Proposed new symbol.
A. Cytology
The mung bean is a diploid of 2n = 2r = 22 chromosomes (Karpechenko 1925; Kumar 1945; Frahm-Leliveld 1953; Krishnan and De 1965; Bhatnagar et al. 1974; Joseph and Bouwkamp 1978). Krishnan and De (1965) described the pachytene chromosome in detail and found that the chromosome lengths varied from 28.1 to 73.3 pm. They reported that the somatic metaphase chromosomes varied from 1.4 to 3.3 pm in length. Two bivalents are associated with the nucleolus at pachytene. Krishnan and De (1968a) studied the behavior of the nucleolus chromosomes at pachytene stage in F1 and backcross progenies of a V. radiata autotetraploid X Phaseol us species allotetraploid cross. Shrivastava et al. (1973) reported considerable variation in chromosome morphology among different wild and domestic ecotypes. Bhatnagar et al. (1974) proposed the following karyotypic formula for mung bean: 4L"" + 4 M " + 3M", where L = long (2.7 to 3.5 pm), M = medium (1.9 to 2.6 pm), sm = submedian centromere, and m = median centromere. Joseph and Bouwkamp (1978) published an idiogram of pro-metaphase chromosomes. Swindell et al. (1973) reported the occurrence of a natural 44-chromosome tetraploid mung bean of suspected amphidiploid origin. Induced autotetraploids usually exhibit giganticism in all floral parts, slow germination, late maturity, high sterility, low seed set, and increased seed and stomate size (Kumar and Abraham 1942a,b; Kumar 1945; Mital 1967; Sen and Ghosh 1960a; Bhapkar 1965; Kabi and Bhaduri 1978). Sen and Murty (1960a) found that selection for vegetative growth traits would suffice to bring tetraploids up to diploid level; fruit and seed setting also responded to selection, but diploid level yields could not be achieved. Kabi and Bhaduri (1978) found that the polyploidy status of
352
HORTICULTURAL REVIEWS
the mung bean affected the relative competing abilities of Rhizobium strains for nodule sites. They concluded that polyploidy enhanced root hair infection and early nodulation.
B. Plant Characters 1. Habit.-Sen and Ghosh (1959) assigned the symbol T to a dominant gene that conditions the inheritance of twining growth habit. Pathak and Singh (1963), however, concluded that the twining habit probably is governed by a single recessive gene. Semi-spreading growth habit is dominant to erect growth habit and probably conditioned by a single dominant gene (Pathak and Singh 1963). Published broad-sense heritability estimates for plant height and branch number range from 7.9 to 96.9% and average 68.4% for plant height and 57.3% for branch number (Table 7.10). Swindell and Poehlman (1976) found significant general and specific combining abilities for plant height and branch length. Tiwari and Ramanujam (1974) reported significant general and specific combining abilities for plant habit, number of leaf axils per plant, number of effective leaf axils per plant, and number of branches per plant, but concluded that variances due to general combining ability were preponderant. Yohe and Poehlman (1975) found that the variability in plant height and branch length was accounted for largely by general combining ability. Murty et al. (1976) demonstrated that dominance X dominance gene action was involved to a considerable extent in the expression of plant height and that number of branches was influenced greatly by dominance type gene action. Godhani et al. (1978) showed that additive gene action is involved in the expression of branch number and that additive, dominance, and epistatic gene action are important in the expression of plant height. The association of high heritability and high genetic advance often is interpreted as being indicative of additive gene action. Such relationships have been demonstrated for plant height (Bhargava et al. 1966; Chowdhury et al. 1971; Giriraj 1973; Veeraswamy et al. 1973) and branch number (Veeraswamy et al. 1973). Pokle and Nomulwar (1975) also found that plant height is highly heritable, but their estimate was associated with a low genetic advance estimate and they concluded that the trait is conditioned largely by non-additive gene action effects. 2. Leaves.-Singh and Mehta (1953) showed that lobed leaflet is dominant over entire leaflet and conditioned by a single gene that they symbolized E. Later, Sen and Ghosh (1959) reported that heterozygote E+ plants have intermediately lobed leaflets. They proposed that this gene be redesignated L, but I suggest that Singh and Mehta’s (1953) original E designation be maintained. Incised leaflet is dominant to the
Number of primary branches. Number of secondary branches. Narrow-sense heritability estimate.
Avg of 5 Fz populations.
Pokle and Nomulwar 1975 Swindell and Poehlman 1978 Singh and Malhotra 1970b Tomar et al. 1972 Veeraswamy et al. 1973
Joshi and Kabaria 1973 Murty et al. 1976
Reference Bhargava et a/.1966 Chowdhury et al. 1971 Empig et al. 1970 Giriraj 1973 Gupta and Singh 1969 7.9 75.0 19.0' 96.3 83.0 88.5
-
Plant Height 96.8 87.3 27.0' 96.9 -
Branches perplant (no.) 66.0 34.5 50.g2 54.93 57.0 85.2 31.0 78.9 Stem Diameter 76.0 -
-
(%I
Leaf Length 49.7 -
h2 Days to Flowering 94.9 62.0' 99.0 39.5 88.8 69.0 31.0' 59.0 65.1 90.6 79.0
-
Days to Maturity 71.2l 81.5 61.4
-
-
-
42.W -
-
Maturity Range
TABLE 7.10. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR GROWTH HABIT TRAITS AND EARLINESS PARAMETERS IN MUNG BEAN, VlGNA RADlATA
M
W
cn
W
8
2
M
z
0
354
HORTICULTURAL REVIEWS
normal ovate leaflet and is governed by the gene Ic (Pokle 1972). Veeraswamy and Kunjamma (1958) described a mutant with all leaves having four or five leaflets, instead of the normal three. They concluded that the trait is probably conditioned by a single dominant gene. Santos (1969) induced unifoliata and multifoliata leaf mutants; both behaved as monogenic recessives. Singh and Saxena (1959) described a crinkled, lanceolate leaf mutation. They showed that the trait is conditioned by a single major factor that they designated N. The gene is semidominant and lethal when it is in the homozygous condition. Since the symbol N was first used by Sen and Ghosh (19591, I propose that this gene be redesignated La. Swindell and Poehlman (1976) reported significant general combining ability for leaf size. Tiwari and Ramanujam (1974) found that both general and specific combining abilities for leaf size were significant, but they concluded that most of the variability was due to general combining ability. 3. Pubescence.-Murty and Pate1 (1973) showed that a single dominant gene conditions dense plant pubescence over medium-dense plant pubescence. I propose that this gene be symbolized Dp.
C. Heterosis There is an appreciable amount of heterosis in mung bean for yield and most yield components, days to flowering, and such vegetative traits as plant height, leaf size, and branch number (Bhatnagar and Singh 1964; Misra et al. 1970a; Ramanujam et al. 1974; Singh and Jain 1970; Singh and Singh 1974a,b).Grain yields of F1hybrids have been reported to be as much as 137% (Swindell and Poehlman 1976),158% (Misra et al. 1970a), and 352% (Bhatnagar and Singh 1964) of the higher yielding parent. Sen and Murty (1960b) and Singh and Jain (1970) reported negative heterosis for seed size. Ramanujam et al. (1974) and Singh and Singh (1974b) concluded that there was an association between genetic diversity among parents and the manifestation of heterosis. Singh and Singh (1974a,b) presented evidence that the superiority of F1hybrids for characters like grain yield and number of pods per plant is due to overdominance and non-fixable genic interactions, and showed that there was an appreciable amount of inbreeding depression for yield in the F2 and F3 as compared with the F1hybrid. Heterosis for protein content is small (Singh and Singh 1973b; Tiwari and Ramanujam 1976a). Singh and Singh (1973b) attributed the lack of heterosis manifestation for this trait to the presence of genes with oppositional dominance. Tiwari and Ramanujam (1976a) found substantial heterosis over mid-parent for methionine content.
GENETICS OF VZGNA
355
D. Color 1. Plant Color.-Sen and Ghosh (1959) assigned the symbol P to a gene conditioning purple hypocotyl and the symbols C, ch,and c to a multiple allelic series governing purple, purple spotted, and green epicotyl. Since the symbol C was used earlier by Bose (1939), I suggest that the allelic series governing purple, purple spotted, and green epicotyl be redesignated Pe, pes, and Pe +, respectively. Sen and Ghosh (1959) speculated that the Pe allele is a general color factor. Plants with P and Pe genes have purple hypocotyl, epicotyl, stem, and leaf rachis; plants with P and pe3 have purple hypocotyl, purple spotted epicotyl, green stem, and leaf rachis with many spots; plants with P and pes genes have purple spotted hypocotyl, green epicotyl, green stem, and leaf rachis with few spots; and plants with the Pe +Pe genotype do not develop color pigment in any plant part. The Pe allele conditions a more intense color than pe". Several other studies completed subsequent to the Sen and Ghosh (1959) paper indicate that the inheritance of anthocyanin pigmentation in such plant parts as the hypocotyl, epicotyl, stem, petiole, and peduncle is due to single dominant genes (Misra et al. 1970b; Pathak and Singh 1963; Swindell and Poehlman 1978; Thakur et al. 1977b; van Rheenen 1964, 1965; Verma and Krishi 1969; Virk and Verma 1977). Van Rheenen (1965) proposed the symbol R for a gene that conditions red color of the cotyledons, hypocotyl, and top of the leaflet stalk. He suspected that R is probably synonymous with Sen and Ghosh's (1959) Pe gene. Swindell and Poehlman (1978) proposed the symbol A for a dominant gene that governs purple hypocotyl, but this symbol was used first by Bose (1939) and I suggest that it be changed to Ph. Appa Rao and Jana (1973) reported a mung bean mutant in which anthocyanin pigmentation in the hypocotyl, epicotyl, stem, petiole, and peduncle appears to be a recessive trait. Sen and Ghosh (1960b) studied the inheritance of an albino seedling trait and found that it is conditioned by the recessive gene al. They assigned the symbol i to a gene that was found to inhibit the expression of the a1 gene. Since the symbol I was assigned already, I suggest that the inhibitor of a1 be redesignated in-al. Santos (1969) induced xantha, variegata, and greenish-yellow chlorina chlorophyll mutations; the xantha and variegata traits behave as monogenic recessives and the chlorina trait behaves as a monogenic recessive in some lines, but appears to be governed by two recessive genes in other lines. +
+
2. Seed Coat Color.-One to four genes have been shown to be responsible for differences in seed coat color among various mung bean genotypes. Bose (1939) was the first to study the genetics of this trait and he postulated that two genes are responsible for seed coat color. The gene A
356
HORTICULTURAL REVIEWS
conditions the production of green color and the gene B imparts a darker green color. He assumed that the genotypes of green, pale green, dark green, and greenish-yellow seeds are A A + +, + + + +, A A B B , and + + B B, respectively. Sen and Ghosh (1959) found that seed coat colors are due to sap-soluble pigments and to the color and number of chloroplasts. They assigned the symbols B, b f , and G to genes that conditioned the inheritance of blue sap color, buff sap color, and green chloroplasts, respectively. Since the symbol B was used earlier by Bose (1939), I suggest that Sen and Ghosh’s (1959) B gene be redesignated Bl. The genotypes of Sen and Ghosh’s (1959) blue-green mosaic, green, greenish yellow, and buff seed coat colors were B1 Bl + + G G, + + + G G, +++ +, and + + bf bf G G, respectively. Van Rheenen (1965) assigned the symbols G and S to dominant genes conditioning green and spotted seed coat colors, respectively. He stated that the Ggene probably was Bose’s (1939) A gene. Since the symbol G was used earlier by Sen and Ghosh (1959), I suggest that Bose’s (1939) A designation be used for this gene. The symbol S also was used previously and I suggest that van Rheenen’s (1965) Sgene symbol be redesignated Sp. K.B. Singh and J.K. Singh (1970) assigned the symbol Bsp to a dominant gene conditioning black spot on the seed coat. Murty and Patel (1972) concluded that four genes govern seed coat color and they assigned the following symbols: B, M, Br, and G. Since the symbols B, Br, and G were used previously, I suggest that they be redesignated Bla, Brn, and Gn, respectively. Table 7.11 illustrates the Murty and Patel (1972) model for seven seed coat colors using the proposed new symbolization. Singh (1973) proposed a three-gene model to explain bottle green and yellowish green
+
++
TABLE 7.11. INTERACTION OF MURTY AND PATEL’S (1972) PIGMENT FACTORS FOR THE PRODUCTION OF SEED COAT COLOR IN MUNG BEAN, VlGNA RADIATA Gene Symbol (See Table 7.9)
Color Black
Necessary Bla M Brn Bla Gn Bla
Not Permissible M Brn Gn
Green mosaic
Bla M Gn Brn M Gn
Brn Bla
Yellow mosaic
Bla Mgngn Brn Mgngn
Brn Bla
Brown
Bla Brn Gn
M
Amber
Bla Brn gngn
M
Green
Gn
Bla M Brn
Yellow
gngn
Bla M Brn
GENETICS OF VZGNA
357
seed coat colors. Bottle green was assumed to be due to gene G and yellowish green was due to gene P i n the presence of gene Y. Since the symbols G and P already were assigned, I suggest that Singh's (1973) G and P genes be redesignated Grn and Yg, respectively. Bottle green has the genotype Y Y Grn Grn + + or + + Grn Grn + + and yellowish-green has the genotype Y Y Grn Grn Yg Yg. Singh and Patel (1977b) studied the green and spotted seed color traits and concluded that each is conditioned by a single dominant gene. 3. Flower Color.-Bose (1939) showed that light yellowish olive flower color is partially dominant to olive-yellow flower color and conditioned by the gene 0. Sen and Ghosh (1959) concluded that the hypocotyl-epicotyl color genes P, Pe, pe', and Pe' also govern oil yellow and palmleaf yellow flower colors, but they could not differentiate these colors from the colors described earlier by Bose (1939) and suggested that the latter's 0 color symbol should be retained. Murty and Patel (1973) proposed the symbols Pg, Pb, and Pn for an allelic series conditioning pale green yellow, bryta yellow, and naphthalene yellow flower colors, respectively. Since the Pg, Pb, and Pn genes are allelic, I suggest that they be redesignated Pg, pgb, and pg", respectively. The order of dominance is Pg, pgb, and pg". This allelic series may be synonymous with the Pe, pe', and Pe' allelic series described earlier by Sen and Ghosh (1959). 4. Pod Color.-Bose (1939) speculated that the color of unripe pods is controlled by the same genes responsible for the inheritance of flower color. He showed that the 0 gene for light yellowish olive flowers also conditions dark green pods with deep red veins on the sutures. Later, Pathak and Singh (1963) and Murty and Patel (1973) concluded that the purple color in the ventral suture of unripe pods was conditioned by a single dominant gene. Sen and Ghosh (1959) observed that unripe pods of all plants homozygous for the Pe' allele are green in color. Sen and Ghosh (1959) also studied the inheritance of dry pod colors. They proposed the symbols lp and a for genes conditioning light popcorn and almond biscuit colors, respectively. Since the symbol A was used previously by Bose (19391, I suggest that Sen and Ghosh's (1959) almond biscuit color gene be redesignated ab. The dominant alleles lp' and ab' together condition black pod color. Pathak and Singh (1963) reported that black pods are dominant over light brown pods and probably conditioned by a single gene.
5. Plant Pubescence Color.-Sen and Ghosh (1959) reported that the brown color of unicellular plant hairs is recessive to colorless. Two genes, N and Br, govern the trait, and both dominant alleles are necessary for colorless pubescence.
358
HORTICULTURAL REVIEWS
E. Flowers and Flowering I. Simple Inflorescence.-Simple inflorescence is governed by the two dominant genes I-1 and I-2, and the absence of either of the dominant alleles results in a compound inflorescence (Sen and Ghosh 1959). T.P. Singh and K.B. Singh (1970) assigned the symbol C to a dominant gene that conditions a single cluster a t a node over three clusters a t a node. Since the symbol C was assigned previously, I suggest that the single cluster gene be redesignated C1. 2. Photoperiod.-Sen and Ghosh (1961) demonstrated that it is possible to develop photoperiod-insensitive mung bean cultivars that are adapted to cultivation under a wide range of seasonal conditions. Verma (1971a) and Tiwari and Ramanujam (1976b) found that photoinsensitiveness is dominant over photosensitiveness, and Verma (1971a) concluded that photoinsensitiveness is probably governed by a single gene pair. Swindell and Poehlman (1978) identified a dominant or partially dominant gene, symbolized Ps, for sensitivity to photoperiod in P.I. 180311. They found that the gene was expressed when P.I. 180311 was grown in 14- to 16-hour photoperiods, but was not expressed in a 12-hour photoperiod.
3. Outcrossing Mechanisms.-Ganguli (1972, 1973) and Saini et al. (1974) have successfully induced a number of male- and female-sterile mutants. In all instances, sterility appears to be monogenic recessive in nature. 4. Early Flowering.-The 14 published broad-sense heritability estimates of the earliness parameters, days to flowering or days to maturity, range from 31.0 to 99.0% and average 70.9% (Table 7.10). Bose (1939), Sen and Ghosh (1961), and Tiwari and Ramanujam (1976b) suggested that early maturity is dominant or partially dominant over late maturity while Singh and Singh (1974a) suggested that late maturity is partially dominant over early maturity. Several authors have analyzed such relationships as general combining ability/specific combining ability and heritability/genetic gain and have concluded that the earliness parameters are largely controlled by loci with additive gene action (Chowdhury et al. 1971; Giriraj 1973; Godhani et al. 1978; Singh and Singh 1974a; Swindell and Poehlman 1976; Tiwari and Ramanujam 1974; Yohe and Poehlman 1975). Murty et al. (1976) and Swindell and Poehlman (1978) reported that dominance X dominance gene action is involved in the expression of days to flower. Tiwari and Ramanujam (1976b) noted F2 segregations of 13 moderately early plants to 3 late plants and they suggested that earliness is under digenic control.
GENETICS OF VIGNA
359
F. Pods I. Pod Length.-Pod length is moderately to highly heritable under most environmental conditions; published heritability estimates range from 6.0 to 95.0% and average 63.9% (Table 7.12). There is no general agreement about the nature of gene action for pod length. The association of high heritability and high genetic gain reported by Chowdhury et al. (1971) indicates that additive gene action is important. Pokle and Numulwar (1975), however, speculated that non-additive gene action is important because their high heritability estimate was associated with low genetic gain. Singh and Singh (1974a) concluded that both additive and logarithmic or multiplicative gene action are important. Murty et al. (1976) showed that pod length is influenced by dominance, dominance X dominance, and additive X additive gene action, but Godhani et al. (1978) found only additive and additive X additive or dominance gene effects. TABLE 7.12. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR POD AND SEED TRAITS IN MUNG BEAN. VlGNA RADlATA
Reference Bhargava et al. 1966 Chowdhury et al. 1971 Empig et al. 1970 Giriraj 1973 Gupta and Singh 1969 Joshi and Kabaria 1973 Malhotra and Singh 1976 Murty et al. 1976 Pokle and Nomulwar 1975 Singh and Malhotra 1970b Singh and Singh 1973b Tomar et al. 1972 Veeraswamy et al. 1973
Pod Length 66.0 88.6 89.7 89.9 -
74.0 95.0 33.3 31.0 6.0 79.0 53.4
Seed per Pod (no.) 41.3 39.0 10.0' 49.02 70.2 58.7 12.3 -
78.0 68.3 30.5 26.0 6.0 83.0 60.1
100-seed wt 85.3 98.6 51.2l 85.02 97.0 92.9 -
95.3 88.9 97.0 -
-
Protein (%)
-
50.8
Test wt -
-
-
-
-
-
61.0 -
-
-
-
73.53 -
-
-
Avg of 5 FZpopulations. FSpopulation. '3 Narrow-sense heritability estimate. 1
2
2. Seed Number.-The number of seeds per pod is a t least moderately heritable under most environmental conditions. The 14 published heritability estimates range from 6.0 to 83.0% and average 45.2% (Table 7.12). The data of Singh and Singh (1974a), Swindell and Poehlman (19761, and Yohe and Poehlman (1975) indicate that the trait is controlled predominantly by loci with additive gene effects. Singh and Jain (1971) and Tiwari and Ramanujam (1974),however, found that both ad-
360
HORTICULTURAL REVIEWS
ditive and non-additive gene action are important. Singh and Jain (1971) observed partial to over-dominance and speculated that dominance genes govern the inheritance of the number of seeds per pod. Murty et al. (1976) showed that dominance X dominance gene action was important. 3. Pod Shattering.-The shattering of pods a t maturity is a serious problem in mung beans. Verma and Krishi (1969) showed that the shattering characteristic is completely dominant to the non-shattering characteristic and probably conditioned by a single gene pair. P. Singh et al. (1975) noted that the mature pods of the urd bean (V. rnungo) do not shatter, and they attempted to transfer this trait into the mung bean. The shattering characteristic was dominant in the F1 plants of the interspecific cross, but the non-shattering characteristic could not be recovered in the Fz. P. Singh et al. (1975) concluded that resistance to shattering is quantitatively inherited. 4. Pod Shape.-Swollen pod tip is dominant over tapering pod tip and conditioned by the gene T p (Sen and Ghosh 1959).
G . Seeds 1. Seed Size.-Seed size is highly heritable under most environmental conditions. The 9 published heritability estimates for 100-seed weight, a common index of seed size, range from 51.2 to 97.0% and average 87.9% (Table 7.12). The associations between high heritability estimates and high genetic advance estimates that have been reported by a number of researchers indicate that additive gene action plays an important role in the inheritance of this trait (Bhargava et al. 1966; Chowdhury et al. 1971; Giriraj 1973; Pokle and Nomulwar 1975; Singh and Malhotra 1970b). The diallel analyses of Singh and Singh (1972) and Yohe and Poehlman (1975) provide additional evidence that additive gene action is of appreciable magnitude. Singh and Singh (1974a) observed that logarithmic or multiplicative gene action is functioning also and Tiwari and Ramanujam (1974) showed that seed size also is conditioned by some loci with non-additive gene effects. Sen and Murty (1960b) found that small seed size is dominant to larger seed sizes and they speculated that largeseeded mung bean types evolved from small-seeded types through the accumulation of recessive genes with additive effects. Their data indicate that it might be possible to further increase seed size by crossing among large-seeded cultivars. 2. Seed Coat Structure.-Dull, rough seed surface is monogenically dominant over glossy, smooth seed surface (Bose 1939; Murty and Pate1 1973; Sen and Ghosh 1959; K.B. Singh and J.K. Singh 1970; van Rheen-
GENETICS OF VZGNA
361
en 1965). Bose (1939), Sen and Ghosh (1959), van Rheenen (1965), and K.B. Singh and J.K. Singh (1970) assigned the symbols C, S, 0, and Ns, respectively, to the dominant gene conditioning this trait. The S, 0,and Ns are all probably redesignations of Bose's (1939) C gene and I suggest that the original C symbol be used. K.B. Singh and J.K. Singh (1970) noted that shiny seed surface genotype C' C' is expressed only when the dominant allele for black spot on seed surface (Bsp)is present. The data of Sen and Ghosh (1959) indicate that a second dull, rough seed coat gene is sometimes present and they symbolized this gene S-2. I suggest that this mimic gene be redesignated 12-2. 3. Seed Protein.-Singh and Singh (1973b) and Malhotra and Singh (1976) reported that protein content of mung bean seeds is moderately heritable (Table 7.12). Singh and Singh (1973b) showed that both additive and non-additive gene action are important in the inheritance of protein content, but additive gene action plays the predominant role. Singh (1974) also concluded that both additive and non-additive gene action are important. He found that high protein content appears to be controlled by dominant genes. Malhotra and Singh (1976) concluded that the simultaneous improvement in yield and protein will be difficult. They showed, for example, that the direct effects of seeds per pod and yield per plant on protein content were negative and relatively high. Tiwari and Ramanujam (1976a) found that protein content is conditioned largely by additive gene action. They showed that both additive and non-additive gene action are equally important for methionine content.
H. Yield 1. Heritability Estimates and Gene Action.-Yield is moderately heritable under most environmental conditions. The 29 published heritability estimates for the 2 most frequently measured yield parameters, pod number and grain weight, range from 6.0 to 90.4% and average 54.0% for pod number and 51.0% for grain weight (Table 7.13). Singh and Jain (1971) and Singh and Singh (1972) reported partial dominance for grain yield and partial to over-dominance for pod number. Yohe and Poehlman (1975) concluded that these traits are predominantly controlled by loci with additive gene effects, but the analyses of Singh and Jain (19711, Singh and Singh (1974a,b), and Tiwari and Ramanujam (1974) indicate that both additive and non-additive gene action are important. Bhargava et al. (19661, Giriraj (19731, Joshi and Kabaria (19731, Pokle and Nomulwar (19751, and Veeraswamy et al. (1973) reported high expected genetic gains for various yield parameters, which is indicative of strong additive gene effects. Other studies indicate that the role
362
HORTICULTURAL REVIEWS
TABLE 7.13. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR YIELD PARAMETERS IN MUNG BEAN, VlGNA RADlATA
hZ ("lo) Reference Bhargava et al. 1966 Chowdhury et al. 1971 Empig et al. 1970 Giriraj 1973 GuDta and Sineh 1969 Jos'hi and Kabiria 1973 Murty et al. 1976
Clusters per Plant (no.) 93.2 -
-
-
-
Pokle and Nomulwar 1975 Singh and Malhotra 1970b Tomar et al. 1972
86.6 37.8
Veeraswamy et al. 1973
83.8
-
-
Pods per Plant (no.) 87.9 53.8 50.9' 50.42 24.6' 31.04 77.7 47.8 90.4 78.0
Pods per Plant (wt)
Seeds per Plant (no.)
-
-
-
-
21.7 30.9 43.0 48.0 59.0 61.5
-
-
-
-
-
73.0 10.05
-
58.2
27.6? 26.0' -
87.9 -
-
Seeds per Plant (wt) 69.9 56.9 -
8.6? 47.04 79.1 51.1 84.2 75.0 14.05 59.0 27.5 38.0 28.0 79.0 47.2
Number of pods on main shoot. Number of pods on side branches. ? Avg of 5 Fz populations. ' F, population. Narrow-sense heritability estimate.
of additive gene action is minimal. Singh and Singh (1972) showed that non-additive gene action is important for both grain yield and pod number. Godhani et al. (1978) concluded that dominance gene effects are principally responsible for grain yield, whereas non-additive epistatic gene effects are responsible for pod number. Murty et al. (1976) showed that dominance X dominance gene action is involved to a considerable extent in the expression of both grain yield and pod number. 2. Character Association.-Several studies have indicated that the principal yield components of pod number, seed size, and seed number per pod may have considerable value, either alone or in combination, in indirect selection schemes for grain yield (Chandel et al. 1973; Gupta and Singh 1969; Joshi and Kabaria 1973; Krishnaswami et al. 1973; Malhotra et al. 1973; Malhotra et al. 1974; Pokle and Patil 1975; Singh and Malhotra 1970a; Singh and Singh 1973a; Tomar et al. 1972, 1973; Yohe and Poehlman 1975). Other plant traits that have been suggested as possible indirect selection criteria for yield include days to flower (Chandel et al. 1973; Giriraj and Vijayakumar 19741, cluster number (Krishnaswami et al. 1973; Malhotra et al. 1973; Malhotra et al. 1974; Singh and Singh 1973a), pod length (Giriraj and Vijayakumar 1974; Gupta and Singh 1969; Tomar et al. 19731, number of branches per plant (Pokle and Patil 1975; K.K. Singh et al. 19761, number of pods per peduncle (Chandel et al. 19731, plant height (Giriraj and Vijayakumar
GENETICS OF VZGNA
363
1974), number of seeds per plant (Joshi and Kabaria 19731, weight of grain per plant (K.K. Singh et al. 1976), days to maturity (Singh et al. 19681, seed weight of ten pods (Singh et al.1968), and plant size (Yohe and Poehlman 1975). Yadav et al. (1979) found that grain yield was positively associated with net assimilation rate at the post-flowering stage and with leaf-area ratio at the pre-flowering stage. I. Resistance to Fungal and Bacterial Diseases 1. Bacterial Leaf Spot.-Singh and Patel (1977b) and Thakur et al. ( 1 9 7 7 ~reported ) that resistance to bacterial leaf spot, a disease incited by Xanthomonas phaseoli (Smith) Dowson mung bean strain, is conditioned by a single dominant gene and the latter proposed that the gene be symbolized B. Since the symbol B was used earlier by Bose (19391, I suggest that the bacterial leaf spot resistance gene be symbolized Bls. Thakur et al. (1977a) studied the genetics of resistance of four mung bean differential hosts inoculated with six races of the pathogen. The inheritance pattern in all the differentials was simple and involved a single dominant gene. 2. Cercospora Leaf Spot.-Resistance to Cercospora leaf spot (CLS), a disease incited by Cercospora canescens Ellis & Martin, is conditioned by the dominant gene F (Thakur et al. 1977b,c). Menancio and Ramirez (1977) showed that peroxidase polymorphism may be used as a selection index for CLS resistance.
3. Powdery Mildew.-Yohe and Poehlman (1975) concluded that resistance to powdery mildew, a disease incited by Erysiphe polygoni DC. ex St. Amans, is controlled largely by loci with additive gene action.
J. Resistance to Virus Diseases 1. Mung Bean Yellow Mosaic Virus.-Tolerance to mung bean yellow mosaic virus (MBYMV) is governed by a single recessive gene (Singh and Patel 197713; Thakur et al. 1977~).Thakur et al. (1 9 7 7 ~) proposed that this gene be designated u. Singh and Ahuja (1977) identified MBYMV resistance in Phaseolus sublobatus Roxb. (= V . radiata var. sublobata), a suspected progenitor of the cultivated mung bean, and have successfully transferred the resistance into commercial types. 2. Cucumber Mosaic Virus.-Resistance to cucumber mosaic virus, mung bean strain, is governed by the dominant gene Cmm (Sittiyos et al. 1979).
364
HORTICULTURAL REVIEWS
K. Gene Linkage Sen and Ghosh (1959) reported linkage relationships between the B1,lp, and P genes. The cross-over values between B1 and lp, B1 and P, and lp and P were 15.7, 4.3, and 19.4%, respectively. Van Rheenen (1965) found that the R and C genes were linked and he estimated the crossover frequency a t 15.0%. L. Interspecific Hybridization
V. radiata hybridizes with V. mungo, but only when V. radiata is used as the seed parent (Ahuja and Singh 1977; Boling et al. 1961; Chowdhury and Chowdhury 1978; Chowdhury et al. 1977; Dana 1966a; De and Krishnan 1966b; Khanna et al. 1962; Sen and Ghosh 1960c; Singh et al. 1964; P. Singh et al. 1975; Singh and Malhotra 1975; Singh and Singh 1975; Verma 1977). Other species that have been crossed successfully with V radiata include V. umbellata (Ahn 1975; Baker et al. 1975; Dana 1966d, 1967; Evans 1976; Sawa 19741, V. angularis (Ahn and Hartmann 1978a; Sawa 19731, Phaseolus trilobus (Dana 1966b,c), P. lathyroides (Biswas and Dana 1975b), and an unidentified naturallyoccurring allotetraploid Phaseolus species (Dana 1965b; Krishnan and De 1968a,c). Evans (1976) reported pod formation, but no seed set, in a V. radiata X V vexillata cross. The amphidiploids between V. radiata and the following species are partially or fully fertile: V. mungo (Chowdhury and Chowdhury 1974; Chowdhury e t al. 1977; Singh and Singh 19751, V umbellata (Ahn 1975; Dana 1966d, 1967; Sawa 19741, and P. trilobus (Dana 1966b). VI. URD BEAN The urd bean ( V mungo (L.) Hepper) is grown throughout southeast Asia and is a staple grain legume crop in India. The plant is commonly known in the Asiatic countries as black gram. The urd bean is selfpollinated, and cleistogamy up to 42% is sometimes observed (Bose 1932; Narasimham 1929; Purseglove 1968). Emasculation and hybridization procedures have been described by Sen and Jana (1963). A total of 40 genes has been described for the species (Table 7.14).
A. Cytology The urd bean is a diploid of 2n = 2x = 22 chromosomes (Chaurasia and Sharma 1974; De and Krishnan 1966a; Karpechenko 1925). De and Krishnan (1966a) found that V mungo chromosomes show close resemblance to those of V. radiata. They presented detailed descriptions of the
GENETICS OF VIGNA
365
TABLE 7.14. LIST OF URD BEAN, VlGNA MUNGO, GENES
Preferred Symbol Synonym a1 *a-1
Character Anthocyanin-negative1
Reference Jana and Appa Rao 1974
Anthocyanin-negative I1
Jana and Appa Rao 1974
alb
Albino chlorophyll mutant.
Jana 1963
alves
A lbo-oirescence chlorophyll mutant.
Appa Rao and Jana 1975
as
Asynaptic.
Jana 1962
b
Brown seed coat color. Recessive to green.
Sen and Jana 1963
bb
Basal branch growth habit (spreading branches develop mostly from the lower nodes).
Jana 1962
bd
B u d mutant (small nonflowering bud).
Jana 1962
Black pod color. Dominant to brown color.
Verma 1971b
C
Black seed coat color. Dominant over brown color and epistatic to G.
Verma 1973
ch
Chlorina chlorophyll mutant.
Jana 1963
chi
Chlorotica chlorophyll mutant.
Appa Rao and Jana 1975
cht
Chlorina-terminalis chlorophyll mutant.
Appa Rao and Jana 1975
chves
Chlorina-uirescence chlorophyll mutant.
Appa Rao and Jana 1975
cl
Crinkled leaf.
Appa Rao and Jana 1976
crpt
Crumpled petal.
Appa Rao and Reddy 1976
d
Dull seed coat.
Sen and Jana 1963
dw
Dwarf habit.
Appa Rao et al. 197513
g
Glabrous pod surface.
Sen and Jana 1963
Green seed coat color. Dominant over brown seed coat.
Verma 1973
H
Hairy pod.
Verma 1973
1
Purple cotyledon.
Jana and Appa Rao 1974
k
Keel mutant (extra set of keel petals).
Jana 1962
m
Malformed flower.
Jana 1962
nl
Narrow leaf.
Appa Rao and Jana 1976
*a-2
*BP
*Gn
a2
(B)
(GI
366
HORTICULTURAL REVIEWS
TABLE 7.14. (Continued)
Preferred Symbol Synonym 0 r S
Character Ovate LeafshaDe. Dominant over lanceolati shape.
~
Reference Verma 1971b
Rolled leaf(1eaf margins rolled inward).
Jana 1962
Straw pod color. Recessive to bluish black color.
Sen and Jana 1963
*Sh
(S)
Shining seed coat.
Verma 1973
*Si
(S)
Semi-spreadinggrowth habit. Dominant to erect habit.
Verma 1971b
SP
Spreadinggrowth habit.
Sen and Jana 1963
t
Tall growth habit.
Jana 1962
tw
Twining habit.
Jana 1962
uc
Uniformly colored seed. Recessive to blue mosaic seed coat pattern.
Sen and Jana 1963
uar
Variegated chlorophyll mutant.
Jana 1963
vim
Viridis chlorophyll mutant.
Appa Rao and Jana 1975
uir
Virescent chlorophyll mutant.
Jana 1963
wx
Waxy leaf.
Appa Rao and Jana 1976
xa
Xantha chlorophyll mutant.
Jana 1963
xalb
Xanthoalba chlorophyll mutant.
Jana 1963
* Proposed new symbol.
pachytene chromosomes and constructed idiograms of the pachytene and somatic karyotypes. The pachytene chromosomes varied in length from 35.7 to 78.5 pm and the somatic chromosomes varied from 1.2 to 2.5 pm. Two bivalents are associated with the nucleolus at. pachytene. Jana (1962) assigned the symbol as to an induced asynaptic mutant gene. The as gene prohibits pairing a t diakinesis and metaphase I, which results in a large number of univalents and an irregular anaphase division. Sen and Chheda (1958) induced tetraploidy in five urd bean cultivars and found that there were differences in cultivar response to polyploidy for many traits. Generally, the tetraploid differed from the diploids in the following traits: (1) shorter and less spreading growth habit, (2) smaller, thicker, and darker green leaves, (3) larger flowers, flower parts, pollen grains, and stomata, (4) shorter pods with fewer seeds, and (5)
GENETICS OF VIGNA
367
larger seeds. Pollen fertility in the tetraploids ranged from 75 to 80%, compared to 95% fertility observed for the diploids. Overall, the tetraploids were less vigorous and yielded less than diploids.
B. Plant Characters 1. Habit.-Dahiya et al. (1977) observed that tall and spreadinggrowth habit is dominant over dwarf and compact habit. Verma (1971b) assigned the symbol S to a dominant gene that conditions semi-spreading habit. Since the symbol S was used previously for another gene, I suggest that Verma’s (1971b) S gene be redesignated Si. Sen and Jana (1963) found that spreading growth habit is recessive to erect growth habit and conditioned by a single gene that they symbolized sp. Jana (1962) assigned the symbols t, tw, and bb to X-ray induced recessive genes that condition tall, twining, and basal branch type growth habits, respectively. Appa Rao et al. (1975b) reported that an induced dwarf mutant is governed by a recessive gene that they symbolized dw. The 17 published broad-sense heritability estimates for plant height and branch number range from 17.8 to 97.3% and average 80.0% for plant height and 56.4% for branch number (Table 7.15). Much of the variability in plant height is probably conditioned by loci with additive gene effects. Chowdhury et al. (19691, U.P. Singh et al. (1975), and Soundrapandian et al. (1975) reported that the high heritability estimate for plant height was associated with a high expected genetic advance estimate. Singh and Singh (1971a) observed heterosis over midparent value for branch number.
TABLE 7.15. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR GROWTH HABIT TRAITS AND DAYS TO FLOWERING IN URD BEAN, VlGNA
MUNGO
Reference Chowdhury et al. 1969 Goud et al. 1977 Luthra and Singh 1978 Sagar et al. 1976 Singh et al. 1972
U.P. Sineh et al. 1975 SoundrGandian et al. 1975 Veeraswamy et al. 1973b
Plant Height 50.9 93.6 69.0 97.3 73.2 96.2
Branches per Plant (no.) 49.4 62.6 56.4 59.0 80.0 65.0 25.6 17.8 89.2 30.4 84.6
Fruiting Nodes Der Plan’t (no.)
33.2 36.8
Days to Flowering 82.9 19.6 13.0 49.0 38.8 95.0 -
368
HORTICULTURAL REVIEWS
2. Leaves.-Verma (1971b) found th at ovate leaf shape is dominant over lanceolate leaf and is governed by a single dominant gene th a t he symbolized 0. Singh and Singh (1971b) showed th a t the hastate shape is dominant over ovate shape and probably controlled by duplicate dominant genes. Appa Rao and Jana (1976) showed th a t the crinkled, waxy, and narrow leaf mutations are all conditioned by single recessive genes. They proposed the following symbols: cl, crinkled leaf; wx, waxy leaf; and nl, narrow leaf. Jana (1962) assigned the symbol r to the recessive gene controlling the rolled-leaf mutant trait.
C. Color 1. Seed Coat Color.-Sen and Jana (1963) showed th a t brown seed coat color is recessive to green seed coat color and is conditioned by a single gene t ha t they symbolized b. They also showed th a t uniformly colored seed coat is recessive to blue mosaic seed coat pattern and conditioned by the gene uc. Later, Verma (1973) also studied the inheritance of green seed coat color and arrived a t similar conclusions. He proposed the symbol G for a dominant gene th at conditions green seed coat color, but this gene may be a redesignation of b’. Since the symbol g was used earlier by Sen and Jana (1963), I suggest th a t Verma’s (1973) gene for green seed coat color be symbolized Gn. Verma (1973) proposed the symbol C for a dominant gene th at conditions black seed coat color. T h e gene C is epistatic to Gn. Appa Rao and Jana (1974) induced a brownseeded mutant and a yellowish-green-seeded mutant and showed th a t both are probably conditioned by single recessive genes. Both mutant colors are recessive to dull, mosaic brown seed coat. 2. Pod Color.-Straw pod color is recessive to bluish black color and conditioned by gene s (Sen and Jana 1963). Verma (1971b) proposed the symbol B for a dominant gene th at conditions black pod color over brown pod color, but this symbol was used previously by Sen and Jana (1963). I propose t ha t the symbol B p be used.
3. Plant Color.-Jana (1963) induced several chlorophyll mutants in the urd bean and showed th at each was governed by a single recessive gene. He assigned the following symbols: alb, albino; xalb, xanthoalba; ch, chlorina; uar, variegated; uir, virescent; a n d xa, xantha. Appa Rao and Jana (1975) induced additional chlorophyll mutants th a t were conditioned by recessive genes and they assigned the following symbols: vim, viridis; chi, chlorotica; cht, chlorina-terminalis; chues, chlorinavirescence; and alues, albo-virescence. An aureo-virescence mutant was cytoplasmically inherited. Jana and Appa Rao (1974) induced the anthocyanin-negative I, anthocyanin-negative 11, and purple cotyledon mutants and showed th a t each
GENETICS OF VZGNA
369
was conditioned by a single recessive gene. They proposed the following symbolization: a-1, anthocyanin-negative I; a-2, anthocyanin-negative 11; and i, purple cotyledon. The a-1 and a-2 loci are complementary; plants homozygous recessive a t either locus are devoid of normal anthocycanin pigmentation in the hypocotyl, epicotyl, stem, petiole, and peduncle. Homozygous i alleles condition purple cotyledons in the presence of a normal a-1' or a-2' allele. Th e normal' i allele is an inhibitor of anthocyanin production in the cotyledon.
D. Flowers and Flowering 1. Flower Mutants.-Appa Rao and Reddy (1976) induced a crumpled petal mutant th at might have potential for use in a program to obtain hybrid seeds without artificial emasculation procedures. Self-fertilization is restricted in the mutant because the anthers are enclosed in the petals. A single recessive gene, designated crpt, was found to condition the trait. Jana (1962) induced three flower mutants and found th a t each is conditioned by a single recessive gene. He assigned the following symbols: bd, bud mutant (small non-flowering bud); m, malformed flower; and k, keel mutant (extra set of keel petals). 2. Early Flowering.-The 6 published broad-sense heritability estimates for days to flowering range from 13.0 to 95.0% and average 49.7% (Table 7.15). Singh and Dhaliwal(1971) showed th a t general combining ability was much larger than specific combining ability for days to 50% flowering, and they concluded th at the trait is conditioned largely by loci with additive gene effects. Chowdhury et al. (1969) noted th a t both the heritability and expected genetic advance estimates for days to flowering were high, which they interpreted as being indicative of large additive gene effects. Singh and Dhaliwal (1971) and Dahiya et al. (1977) noted t ha t earliness is recessive to late maturity.
E. Pods 1. Pod Size.-The traits pod length and seed number per pod are a t least moderately heritable under most environmental conditions. T h e 20 published broad-sense heritability estimates for these traits range from 13.5 to 96.0% and average 52.4% for pod length and 46.7% for seed number per pod (Table 7.16). 2. Pod Pubescence.-Pathak and Singh (1961) found th a t non-hairy pods are recessive to hairy pods and they concluded th a t the non-hairy trait is probably conditioned by a single gene. Sen and Jana (1963) assigned the symbol g to a recessive gene controlling glabrous pod surface, but they concluded th at the density of the pod surface hairs is
370
HORTICULTURAL REVIEWS
TABLE 7.16. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR POD AND SEED TRAITS IN URD BEAN. WGNA MUNGO
Reference Chowdhury et al. 1969 Goud et al. 1977 Luthra and Singh 1978 Sagar et al. 1976 Singh et al. 1972 U.P. Singh et al. 1975 Soundrapandian et al. 1975 Veeraswamy et al. 1973b
Pod Length 62.4 96.0 39.6 13.5 35.6 35.8 74.0 43.9 19.0 -
81.0 75.7
Seed per Pod (no.) 35.1 91.1 15.1 58.5 35.6 36.1 54.0 -
100-seed wt 90.2 92.5 9.9 12.2 16.0 24.4 77.0 35.5 63.8
29.0 65.7
-
-
-
Protein (%)
-
76.0 -
-
Test wt -
-
-
72.5 -
controlled by more than one gene pair. Verma (1973) assigned the symbol H to a dominant gene that governs hairy pod. Dahiya et al. (1977) observed that hairy pods are dominant to smooth pods.
F. Seeds 1. Seed Size.-The 9 published broad-sense heritability estimates for 100-seed weight, a commonly used seed size criterion, range from 9.9 to 92.5% and average 46.8% (Table 7.16). Chowdhury et al. (1969) noted high heritability and genetic gain estimates for 100-seed weight and they concluded that additive gene effects are important for the trait. 2. Glossy Seed Coat.-Sen and Jana (1963) showed that dull, rough seed coat is recessive to glossy, smooth seed coat and is conditioned by a single gene that they symbolized d. Verma (1973) assigned the symbol S to a dominant gene that conditions shining seed coat over dull seed coat. The symbol S was used earlier for another gene (Sen and Jana 1963) and I suggest that Verma's (1973) shining seed coat gene be resymbolized Sh. The Sh allele is probably synonymous with the Sen and Jana's (1963) d' allele.
3. Seed Dormancy.-Seed dormancy in the urd bean is due to hard seed coat. Appa Rao et al. (1975a) found that blue-mosaic seed coat pattern and dormancy are always associated and it is possible to identify nondormant types by the absence of the mosaic pattern. They speculated that the uc' allele that conditions the mosaic pattern also produces blue pigments, which in turn impart dormancy.
GENETICS OF VIGNA
371
4. Seed Protein.-The only data on the inheritance of seed protein in urd bean is that of Sagar et al. (1976), who reported a broad-sense heritability estimate of 76.0%.
G. Yield 1. Heritability Estimates and Gene Action.-Yield in urd bean is a t least moderately heritable under most environmental conditions. The 22 published heritability estimates for the 2 most frequently measured yield parameters, pod number and seed weight, range from 21.2 to 86.0% and average 57.6% for pod number and 59.6% for seed weight (Table 7.17). The results of diallel analyses of pod number, cluster number, and seed weight indicate that general combining ability is more important than specific combining ability and that the majority of the variance for these traits can be attributed to additive gene effects (Dhaliwal and Singh 1970; Singh and Dhaliwal 1972). The high heritability and expected genetic advance estimates for pod and seed yields reported by Luthra and Singh (1978), Soundrapandian et al. (1975), and U.P. Singh et al. (1975) provide additional evidence that urd bean yield is largely conditioned by loci with additive gene effects. Dhaliwal and Singh (1970) concluded that high pod and cluster numbers seem to be governed by recessive genes. Singh and Singh (1971a) observed heterosis over midparent value for seed weight, cluster number, and pod number. 2. Character Association.-A number of correlation, path coefficient, discriminant function, selection index, or coheritability studies have
TABLE 7.17. LISTING OF PUBLISHED BROAD-SENSE HERITABILITY ESTIMATES FOR YIELD PARAMETERS IN URD BEAN. VlGNA MUNGO
Reference Chowdhury et al. 1969 Goud et al. 1977 Luthra and Singh 1978 Sagar et al. 1976 Singh et al. 1972
U.P.Singh et al. 1975
Soundrapandian et al. 1975 Veeraswamv etal. 1973b
Pods per Cluster (no.)
Clusters Pods Pods Seeds per Plant per Plant per Plant per Plant (wt) (wt) (no.) (no.) 21.2 52.9 75.4 80.7 82.6 73.7 78.6 76.1 60.2 57.0 70.8 77.8 84.2 86.0 57.0 62.0 22.2 24.9 46.0 30.5 61.8 70.5 59.8 47.9 60.7 58.5
56.1
72.0
68.9
372
HORTICULTURAL REVIEWS
evaluated the potential value of various plant characters for use as indirect selection criteria for yield. Several of these studies indicate that such characteristics as pod number per plant, 100-seed weight, cluster number per plant, pod length, plant height, and branch number per plant may have considerable value, either alone or in combination, in indirect selection schemes (Goud et al. 1977; Luthra and Singh 1978; Singh et al. 1972; Singh, Singh, Singh and Singh 1976; Singh, Singh and Singh 1976; Singh and Singh 1976; U.P. Singh et al. 1975; Soundrapandian et al. 1976; Tripathi and Singh 1975; Verma and Dubey 1970). Other plant characteristics that have been suggested as indirect selection criteria for yield are pod number per cluster (Singh, Singh, Singh and Singh 1976; U.P. Singh et al. 19751, plant spread (Singh and Singh 19761, number of fruiting branches (Singh and Singh 19761, test weight (U.P. Singh e t al. 1975), and pod number on side branches (Tripathi and Singh 1975). H. Resistance to Yellow Mosaic Virus Dahiya et al. (1977) showed that yellow mosaic virus resistance in urd bean is probably controlled by a single dominant gene. A study reported by Jeswani (Fourth Annual Workshop Conference on Pulse Crops, Ludhiana, April 1970) and mentioned by Singh and Pate1 (1977b), however, indicates that the resistance is governed by two recessive genes. I. Gene Linkage Verma (1973) reported linkage relationships among the Bp, C, and Gn loci; the cross-over values between Bp and C, Bp and Gn, and C and Gn are 17.4596, 32.3%, and 14.85%, respectively. Sen and Jana (1963) reported an average cross-over frequency of 17.0% between the s and uc loci and 18.6% between the d and b loci.
J. Interspecific Hybridization
V. mungo hybridizes with V. radiata (see p. 364). Other species that have been crossed successfully with V. mungo include V. umbellata (Biswas and Dana 1975a1, Phaseolus vulgaris (Strand 1943), P. trilobus (Dana 1966e), and unidentified naturally-occurring allotetraploid Phaseolus species (Dana 1968; Krishnan and De 1968b,c). Al-Yasiri and Coyne (1966) found that crosses between V. mungo and the species P. vulgaris, V. umbellata, and V. angularis resulted in pod set, but the pods collapsed in the early stages of development. They concluded that these crosses were partially compatible because fertilization probably occurred. The amphidiploids or alloploids between V. mungo and the
GENETICS OF VZGNA
373
following species are partially or fully fertile: V. umbellata (Biswas and Dana 1975a), P. trilobus (Dana 1966e), and allotetraploid Phaseolus species (Dana 1968; Krishnan and De 1968b).
VII. ADZUKI BEAN The adzuki bean (V. angularis (Willd.) Ohwi & Ohashi) is popular in Japan, China, and Korea, but it is of little economic importance elsewhere. I t is the sixth most widely grown crop in Japan where 120,000 ha are grown annually (Sacks 1977). The adzuki bean is self-pollinated, but out-crossing occurs frequently and to a much greater extent than in the related species (Purseglove 1968). It is a diploid of 2n = 2x = 22 (Karpechenko 1925; Darlington and Wylie 1955; Purseglove 1968; Joseph and Bouwkamp 1978). Joseph and Bouwkamp (1978) published an idiogram of the pro-metaphase chromosomes and reported that the chromosomes varied in length from 1.19 to 2.06 pm. The taxonomic history of the adzuki bean is quite tangled, and the exact identification of the actual plant species studied in many early “adzuki” bean reports is difficult. Matsuura (1933) reviewed the early genetics work on adzuki bean, but he identified the species as Phaseolus chrysanthos. Although not universally considered to be a synonym of V. angularis, Sacks (1977) has pointed out that the species name P. chrysanthos was used sometimes for the adzuki bean during the early 1900’s. A listing of the P. chrysanthos genes discussed by Matsuura (1933) is presented in Table 7.18. Matsuura (1933) noted the following linkage of groups: R and Z; C, M and P; and I and B-1 (or B-2).Additionally, he cited studies indicating the existence of a dominant gene that conditions narrow leaf shape over round leaf shape and a partially dominant gene that conditions plant hair with sharp apex over plant hair with round apex. V. angularis hybridizes with V. radiata (Ahn and Hartmann 1978a; Sawa 1973) and V. umbellata (Ahn and Hartmann 1978b; Evans 1976). Al-Yasiri and Coyne (1966) found that crosses between V. angularis and the species V. mungo, P. acutifolius A. Gray. Ann., P. vulgaris, and V. umbellata resulted in pod set, but the pods collapsed in the early stages of development. They concluded that these crosses were partially compatible because fertilization probably occurred.
VIII. MOTH BEAN The moth bean (V. aconitifolia (Jacq.) Marechal) is native to India, Pakistan, and Burma. It is extensively grown for food in the arid and semi-arid regions of India and has been used in the southwestern regions
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of the United States for pasture, fodder, and green manure. The crop is sometimes known as the mat bean. The moth bean is a self-pollinated diploid of 2n = 2x = 22 chromosomes (Bhatnager et al. 1974; Darlington and Wylie 1955; Purseglove 1968). Bhatnagar et al. (1974) proposed the following karyotypic formula: 1Lsm+ 5M’“’ + M”’ + 4Ss”’,where L = long (2.7 to 3.5 pm), M = medium (1.9 to 2.6 pm), sm = sub-medium centromere, and m = median centromere. Tikka et al. (1973) published the following broad-sense heritability estimates: days to flowering, 85.7; days to maturity 89.9; plant height, 88.9; number of primary branches per plant, 83.1; pod number per plant, 89.7; pod length, 73.3; number grains per pod, 87.5; test weight, 93.2; and grain yield per plant, 93.4. TABLE 7.18. LIST OF PHASEOLUS CHRYSANTHOS (PROBABLE SYNONYM OF VIGNA ANGULARIS) GENES CITED BY MATSUURA (1933)
Symbol
Synonym
c F G H R
Character Seed Coat Color Black seed coat color (R and M necessary). Also conditions purple stem color ( Rnecessary). Buffseed coat color ( Rnecessary). Green seed coat color. Inhibitor of R. Red seed coat color (dominant over white).
M
2
Seed Coat Pattern Black mottling(R necessary). Solid seed coat color (dominant over eye-type pattern).
I P
S t e m Color Intensifier of purple color conditioned by P. Purple stem color.
*B-1 *B-2
BI B2
Pod Color Brown pod color-l (black if B-2present). Brown pod color-2 (black if B-1 present).
* Proposed new symbol.
Plant height, number of primary branches per plant, pod number per plant, test weight, and grain yield per plant all had high estimates of genetic advance. Tikka and Kumar (1976) suggested that selection for pod number per plant, number of grains per pod, and pod length should be given emphasis in any indirect selection scheme for grain yield. Later, Tikka, Yadavendra, Bordia and Kumar (1976) concluded that pod number per plant, test weight, and number of grains per pod were the key traits for indirect selection schemes. Tikka, Asawa and Kumar (1977) showed that selection for pod number per plant has better prospects for increasing grain yield than selection for any other tested plant characteristic.
GENETICS OF VZGNA
375
IX. RICE BEAN The rice bean ( V . umbellata (Thunb.) Ohwi & Ohashi) is native to southeastern Asia and is cultivated to limited extents in India, Burma, Malaysia, China, Fiji, Mauritius, and the Philippines (Purseglove 1968; Rachie and Roberts 1974). The flower is self-fertile (Piper and Morse 1914; Purseglove 1968), but there is evidence of some natural outcrossing (Sastrapradja and Sutarno 1977). The rice bean is a diploid of 2n = 2x = 22 chromosomes (Darlington and Wylie 1955; Joseph and Bouwkamp 1978; Singh and Roy 1970). Joseph and Bouwkamp (1978) published an idiogram of the pro-metaphase chromosomes and reported that the chromosome lengths varied from 1.12 to 2.46 pm. Singh and Roy (1970) published the following karyotype formula: 5M(D) + 4Sm(D) + 2M(E), where M = medium constriction, Sm = submedium constriction, D = chromosome length > 1.0 but 5 2.0 pm, and E = chromosome length < 1.0 pm. Das and Dana (1977) showed that the inheritance of base color mosaic spotting of seed coat can be explained with two independent, non-interacting genes of three alleles each. They proposed the following gene sap green color; tgb,garnet brown color; Md, symbols: T”’,straw color; tSR, dense mosaic spotting; m i ,light mosaic spotting; and m, no mosaic spotting. The orders of dominance are straw color > sap green color > garnet brown color and dense mosaic > light mosaic > nonmosaic. Chatterjee and Dana (1977) cited unpublished work of Das (1977) on the inheritance of a number of rice bean characteristics. Seedling stem color, flower bud pigmentation, petal color, hilum color, earliness, and seed coat color are all monogenically inherited and dry pod color is governed by two interacting genes. The genes conditioning stem color, flower bud pigmentation, seed coat color, and one of the pod color genes are linked. The size of primary leaves, seedling height, plant height, days to flowering, number of pods per plant, number of seeds per plant, and seed size were highly heritable (95.8 to 98.5%) and largely conditioned by additive gene action. Low heritabilities (8.0 to 55.8%) and significant dominance effects were found for green and dry forage yields, succulency of green forage, number of branches per plant, pod size, and seed yield. Considerable heterosis was noted for green forage yield. V. umbellata hybridizes with V. radiata (Ahn 1975; Baker et al. 1975; Dana 1966d, 1967; Evans 1976; Sawa 1974), V. mungo (Biswas and Dana 1975a), V. angularis (Ahn and Hartmann 1978b; Evans 1976), and a naturally-occurring allotetraploid Phaseolus species (Dana 1964, 1965a). Al-Yasiri and Coyne (1966) reported that the crosses between V. umbellata and the species V. mungo, V. angularis, and P. vulgaris resulted in pod set, but the pods collapsed in the early stages of develop-
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ment. They concluded that these crosses were partially compatible because fertilization probably occurred. The amphidiploids between V. umbellata and the following species are fertile: V. r a d i a t a (Ahn 1975; Dana 1966d, 1967; Sawa 1974), V. mungo (Biswas andDana 1975a),and allotetraploid Phaseolus species (Dana 1964). X. LITERATURE CITED AGBLE, F. 1972. Seed size heterosis in cowpeas (Vigna unguiculata (L.) Walp.). Ghana J. Sci. 12:30-33. AHN, C.S. 1975. Interspecific hybridization between Phaseolus aureus Roxb. and P. calcaratus Roxb. Rural Dev. Rev. 9:63-70. AHN, C.S. and R.W. HARTMANN. 1978a. Interspecific hybridization between mung bean (Vigna radiata (L.) Wilczek) and adzuki bean ( V angularis (Willd.) Ohwi & Ohashi). J. Amer. SOC. Hort. Sci. 103:3-6. AHN, C.S. and R.W. HARTMANN. 197813. Interspecific hybridization between rice bean (Vigna umbellata (Thunb.) Ohwi & Ohashi) and adzuki bean (Vigna angularis (Willd.) Ohwi & Ohashi). J. Amer. SOC. Hort. Sci. 103:435438. AHUJA, M.R. and B.V. SINGH. 1977. Cross between P. aureus X P. mungo. G. B. Pant Univ. Agr. Tech. (India), Ann. Rpt. Res. 1975-1976. p. 71. AL-YASIRI, S.A. and D.P. COYNE. 1966. Interspecific hybridization in the genus Phaseolus. Crop Sci. 6:59-60. AMOSU, J.O. and J.D. FRANCKOWIAK. 1974. Inheritance of resistance to root-knot nematode in cowpea. Plant Dis. Rptr. 58:361-363. ANON. 1975. Mung bean culture and varieties. US. Dept. Agr., Agr. Res. Ser., Northeast Reg. CA-NE-11. ANON. 1976. Annual report, 1975. IITA, PMB 5320. International Institute of Tropical Agriculture, Ibadan, Nigeria. APPA RAO, S. and M.K. JANA. 1973. Inheritance of anthocyanin coloration in Phaseolus mutants. Indian Sci. Congr. Assoc. Proc. 60:302. APPA RAO, S. and M.K. JANA. 1974. Alteration of seed characters in blackgram. Indian J. Agr. Sci. 44:657-660. APPA RAO, S. and M.K. JANA. 1975. Characteristics and inheritance of chlorophyll mutations in Phaseolus mungo. Biol. Plant. 17:88-94. APPA RAO, S. and M.K. JANA. 1976. Leaf mutations induced in black gram by X-rays and EMS. Enuir. Expt. Bot. 16:151-154. APPA RAO, S., S. PADMAJA RAO, and M.K. JANA. 1975a. Induction of non-dormant mutants in black gram. J. Hered. 66:388-389. APPA RAO, S., S. PADMAJA RAO, and M.K. JANA. 1975b. New plant type in black gram. Curr. Sci. 44:679-680. APPA RAO, S. and B.M. REDDY. 1976. Crumpled petal mutants in black gram and cowpea. Indian J. Genetics Plant Breeding 35:391-394.
GENETICS OF VIGNA
377
ARYEETEY, A.N. and E. LAING. 1973. Inheritance of yield components and their correlation with yield in cowpea (Vigna unguiculata (L.) Walp.). Euphytica 22:386-392. BAKER, L.R., N.C. CHEN, and H.G. PARK. 1975. Effect of an immunosuppressant on an interspecific cross of the genus Vigna. HortScience 10:313. BALLON, F.B. and T.L. YORK. 1959. Crossing the common and scarlet bean (Phaseolus spp.) with Vigna species. Philip. Agr. 42:454-455. BAPNA, C.S. and S.N. JOSHI. 1973. A study on variability following hybridization in Vigna sinensis (L.) Savi. Madras Agr. J. 60:1369-1372. BAPNA, G.S., S.N. JOSHI, and M.M. KABARIA. 1972. Correlation studies on yield and agronomic characters in cowpeas. Indian J. Agron. 17:321-324. BARTON, D.W., L. BUTLER, J.A. JENKINS, C.M. RICK, and P.A. YOUNG. 1955. Rules for nomenclature in tomato genetics. J. Hered. 46:22-26. BHAPKAR, D.G. 1965. Uptake of P32and growth pattern in autopolyploids, and changes in nucleic acid content of germinating diploid and tetraploid Phaseolus seeds. Diss. Abstr. 26:44. BHARGAVA, P.D., N.N. JOHRI, S.K. SHARMA, and B.N. BHATT. 1966. Morphological and genetic variability in green gram. Indian J. Genetics Plant Breeding 26:3 70-3 7 3. BHATNAGAR, C.P., R.P. CHANDOLA, D.K. SAXENA, and S. SETHI. 1974. Cytotaxonomic studies on the genus Phaseolus. Indian J . Genetics Plant Breeding 34A:800-804. BHATNAGAR, P.S. and B. SINGH. 1964. Heterosis in mungbean. Indian J. Genetics Plant Breeding 2499-91. BHOWAL, J.G. 1976. Inheritance of pod length, pod breadth and seed size in a cross between cowpea and catjang bean. Libyan J. Sci. 6:17-21. BISWAS, M.R. and S. DANA. 1975a. Black gram X rice bean cross. Cytologia 40:787-795. BISWAS, M.R. and S. DANA. 1975b. Phaseolus aureus X P. lathyroides cross. Nucleus (India) 18:81-85. BLISS, F.A., L.N. BARKER, J.D. FRANCKOWIAK, and T.C. HALL. 1973. Genetic and environmental variation of seed yield, yield components, and seed protein quantity and quality of cowpea. Crop Sci. 13:656-660. BLISS, F.A. and D.G. ROBERTSON. 1971. Genetics of host reaction in cowpea to cowpea yellow mosaic virus and cowpea mottle virus. Crop Sci. 11:258262. BOLING, M., D.A. SANDER, and R.S. MATLOCK. 1961. Mung bean hybridization technique. Agron. J . 53:54-55. BORDIA, P.C., J.P. VADAVENDRA, and S. KUMAR. 1973. Genetic variability and correlation studies in cowpea (Vigna sinensis L. Savi ex Hassk.). Rajasthan J. Agr. Sci. 4:39-44. BOSE, R.D. 1932. Studies in Indian pulses: V. Urd or black gram (Phaseolus mungo Linn.) var. Roxburghii Prain. Indian J. Agr. Sci. 2:625-637.
378
HORTICULTIJRAL REVIEWS
BOSE, R.D. 1939. Studies in Indian pulses: IX. Contributions to the genetics of mung (Phaseolus radiatus Linn., Syn. Ph. aureus Roxb.). Indian J. Agr. Sci. 9:575-594. BRANTLEY, B.B. and C.W. KUHN. 1970. Inheritance of resistance to southern bean mosaic virus in southern pea, Vigna sinensis. Proc. Amer. SOC.Hort. Sci. 95:155-158. BRITTINGHAM, W.H. 1950. The inheritance of date of pod maturity, pod length, seed shape, and seed size in the southern pea, Vigna sinensis. Proc. Amer. SOC.Hort. Sci. 56:381-388. CAPINPIN, J.M. 1935. A genetic study of certain characters in varietal hybrids of cowpea. Philip. J. Sci. 57:149-164. CAPINPIN, J.M. and T.A. IRABAGON. 1950. A genetic study of pod and seed characters in Vigna. Philip. Agr. 33:263-277. CHAMBLISS, O.L. 1974. Green seedcoat: A mutant in southernpea of value to the processing industry. HortScience 9:126. CHANDEL, K.P.S., B.S. JOSHI, and K.C. PANT. 1973. Yield in mung bean and its components. Indian J. Genetics Plant Breeding 33:271-276. CHANDRAPPA, H.M., A. MANJUNATH, S.R. VISHWANATHA, and G. SHIVASHANKAR. 1974. Promising introductions in cowpea and their genetic variability. Curr. Res. (Bangalore, India) 3:123-125. CHATTERJEE, B.N. and S. DANA. 1977. Rice bean (Vigna umbellata (Thunb.) Ohwi & Ohashi). Trop. Grain Legume Bul. 10:22-25. CHAURASIA, B.D. and V.K. SHARMA. 1974. Karyological studies in Phaseolus mungo Linn. Broteria Ser Trimest Cienc. Nut. 43:33-34. CHOPRA, S.K. and L.N. SINGH. 1977. Correlation and path coefficient analysis in fodder cowpea. Forage Res. 3:97-101. CHOWDHURY, R.K. and J.B. CHOWDHURY. 1974. Induced amphidiploidy in Phaseolus aureus Roxb. X P. mungo L. hybrids. Crop Improu. 1:46-52. CHOWDHURY, R.K. and J.B. CHOWDHURY. 1978. Studies on crossability between Phaseolus aureus and P. mungo. Acta Bot. Indica 6:185-187. CHOWDHURY, R.K., J.B. CHOWDHURY, P.N. BHAT, and S.N. KAKAR. 1969. Evaluation of some varieties of Phaseolus mungo and assessment of genetic variability of different characters. Punjab Agr. Uniu. J. Res. 62367874. CHOWDHURY, J.B., R.B. CHOWDHURY, and S.N. KAKAR. 1971. Studies on the genetic variability in moong (Phaseolus aureus). J. Res. Punjab Agr. Uniu. 8:169-172. CHOWDHURY, R.K., J.B. CHOWDHURY, and V.P. SINGH. 1977. An amphidiploid between Vigna radiata var. radiata and Vigna mungo. Crop Improu. 4: 113-114. CLAYBERG, C.D., L. BUTLER, E.A. KERR, C.M. RICK, and R.W. ROBINSON. 1966. Third list of known genes in the tomato with revised linkage map and additional rules. J. Hered. 57:189-196. CLAYBERG, C.D., L. BUTLER, E.A. KERR, C.M. RICK, and R.W. ROBINSON. 1970. Rules for nomenclature in tomato genetics. Tomato Genetics
GENETICS OF VIGNA
379
COOP.Rpt. 20:3-5. CLAYBERG, C.D., L. BUTLER, C.M. RICK, and P.A. YOUNG. 1960. Second list of known genes in the tomato including supplementary rules for nomenclature. J. Hered. 51:167-174. CUTHBERT, F.P. and R.L. FERY. 1975. Relationship between cowpea curculio injury and Choanephora pod rot of southern peas. J. Econ. Entomol. 68:105-106. CUTHBERT, F.P., R.L. FERY, and O.L. CHAMBLISS. 1974. Breeding for resistance to the cowpea curculio in southern peas. HortScience 9:69-70. DAHIYA, B.S., K. SINGH, and J.S. BRAR. 1977. Incorporation of resistance to mungbean yellow mosaic virus in black gram (Vigna mungo L.). Trop. Grain Legume Bul. 9:28-32. DANA, S. 1964. Interspecific cross between tetraploid Phaseolus species and P. ricciardianus Ten. Nucleus 7:l-10. DANA, S. 1965a. Hybrid between tetaploid Phaseolus sp. and P. calcaratus Roxb. Biol. Planta 7:7-12. DANA, S. 1965b. Phaseolus aureus Roxb. X tetraploid Phaseolus species cross. Rev. Biol. (Lisbon) 5:109-114. DANA, S. 1966a. Cross between Phaseolus aureus Roxb. and P. mungo L. Genetica 37:259-274. DANA, S. 1966b. Species cross between Phaseolus aureus Roxb. and P. trilobus Ait. Cytologia 31:176-187. DANA, S. 1966c. Spontaneous amphidiploidy in F, Phaseolus aureus Roxb. X P. trilobus Ait. Curr. Sci. 35:629-630. DANA, S. 1966d. Cross between Phaseolus aureus Roxb. and P. ricciardianus Ten. Genetics Iberica 18:141-156. DANA, S. 1966e. Interspecific hybrid between Phaseolus mungo L. and P. trilobus Ait. J. Cytol. Genetics (India) 1:61-66. DANA, S. 1967. Hybrid from the cross Phaseolus aureus Roxb. and P. calcaratus Roxb. J. Cytol. Genetics (India) 2:92-97. DANA, S. 1968. Hybrid between Phaseolus mungo L. and tetraploid Phaseolus species. Japan J. Genetics 43:153-155. DANGI, O.P. and R.S. PARODA. 1974. Correlation and path coefficient analysis in fodder cowpea (Vigna sinensis Endl.). Expt. Agr. 10:23-31. DARLINGTON, C.D. and A.P. WYLIE. 1955. Chromosome atlas of flowering plants. 2nd edition. George Allen & Unwin Ltd., London. DAS, N.D. 1977. Genetics of Phaseolus calcaratus. PhD Thesis, Bidham Chandra Krishi Vidyalaya, West Bengal. DAS, N.D. and S. DANA. 1977. Inheritance of seed coat color in rice bean. Seed Res. (New Delhi) 5:119-128. DE, D.N. and R. KRISHNAN. 1966a. Studies on pachytene and somatic chromosomes of Phaseolus mungo L. Genetica 37:581-587. DE, D.N. and R. KRISHNAN. 1966b. Cytological studies of the hybrid, Phaseolus aureus X P. mungo. Geneticu 37:588-600.
380
HORTICULTURAL REVIEWS
DE ZEEUW, D.J. and J.C. BALLARD. 1959. Inheritance in cowpea of resistance to tobacco ringspot virus. Phytopathology 49:332-334. DE ZEEUW, D.J. and R.A. CRUM. 1963. Inheritance of resistance to tobacco ringspot and cucumber mosaic viruses in black cowpea crosses. Phytopathology 53:337-340. DHALIWAL, H.S. and K.B. SINGH. 1970. Combining ability and inheritance of pod and cluster number in Phaseolus mungo L. Theor. Appl. Genetics 40:117-120. DUNDAS, B. 1939. Inheritance of resistance to powdery mildew in runner beans (Phaseolus coccineus), tepary beans (P. acutifolius),. yard-long beans (Vigna sesquipedalis) and cowpeas (Vigna sinensis). Phytopathology 29:824. (Abstr.) EBONG, U.U. 1972. Optimum time for artificial pollination in cowpeas, Vigna sinensis Endl. Samaru Zaria Inst. Agr. Res. Samaru Agr. Newsl. 14:31-35. EMPIG, L.T., R.M. LANTICAN, and P.B. ESCURO. 1970. Heritability estimates of quantitative characters in mung bean (Phaseolus aureus Roxb.). Crop Sci. 10:240-241. ERSKINE, W. and T.N. KHAN. 1977. Genotype, genotype X environmental and environmental effects on grain yield and related characters of cowpea (Vigna unguiculata (L.) Walp.). Austral. J. Agr. Res. 28:609-617. ERSKINE, W. and T.N. KHAN. 1978. Inheritance of cowpea yields under different soil conditions in Papua, New Guinea. Expt. Agr. 14:23-28. EVANS, A.M. 1976. Species hybridization in the genus Vigna. Proceedings of IITA collaborators meeting on grain legume improvement, plant improvement. IITA, PMB 5320, June 9-13, 1975. International Institute for Tropical Agriculture, Ibadan, Nigeria. p. 31-34. FARIS, D.G. 1964. The chromosome number of Vigna sinensis (L.) Savi. Canadian J. Genetics Cytol. 6~255-258. FENNELL, J.L. 1948. New cowpeas resistant to mildew. J. Hered. 39:275279. FERY, R.L. and F.P. CUTHBERT, JR. 1975. Inheritance of pod resistance to cowpea curculio infestation in southern peas. J . Hered. 66:43-44. FERY, R.L. and F.P. CUTHBERT, JR. 1978. Inheritance and selection of nonpreference resistance to the cowpea curculio in the southernpea ( Vigna unguiculata (L.) Walp.). J. Amer. SOC.Hort. Sci. 103:370-372. FERY, R.L. and F.P. CUTHBERT, JR. 1979. Measurement of pod-wall resistance to the cowpea curculio in southernpea (Vigna unguiculata (L.) Walp.). HortScience 14:29-30. FERY, R.L. and P.D. DUKES. 1977. An assessment of two genes for Cercospora leaf spot resistance in the southernpea (Vigna unguiculata (L.) Walp.). HortScience 12:454-456. FERY, R.L. and P.D. DUKES. 1979. Genetics of root knot resistance in the southernpea (Vigna unguiculata (L.) Walp.). HortScience 14:406. (Abstr.)
GENETICS OF VZGNA
381
FERY, R.L., P.D. DUKES, and F.P. CUTHBERT, JR. 1976. The inheritance of Cercospora leaf spot resistance in southernpea (Vigna unguiculata (L.) Walp.). J. Amer. SOC. Hort. Sci. 101:148-149. FRAHM-LELIVELD, J.A. 1953. Some chromosome numbers in tropical leguminous plants. Euphytica 246-48. FRAHM-LELIVELD, J.A. 1965. Cytological data on some wild tropical Vigna species and cultivars from cowpea and asparagus bean. Euphytica 14:251270. FRANCKOWIAK, J.D. and L.N. BARKER. 1974. Inheritance of testa color in cowpea, Vigna unguiculata (L.) Walp. Agron. Abstr. p. 52-53. GANGULI, P.K. 1972. Cytogenetic study of an induced flower-color mutation in green gram (Phaseolus aureus Roxb.). Indian Sci. Congr. Assoc. Proc. 59:553. GANGULI, P.K. 1973. Radiation induced sterile mutant in green gram (Phaseolus aureus Roxb.). Indian Sci. Congr. Assoc. Proc. 60:640-641. GIRIRAJ, K. 1973. Natural variability in green gram (Phaseolus aureus Roxb.). Mysore J. Agr. Sci. 7:184-187. GIRIRAJ, K. and S. VIJAYAKUMAR. 1974. Path coefficient analysis for yield attributes in mung bean. Indian J. Genetics 34:27-30. GODHANI, P.R., B.G. JAISANI, and G. J. PATEL. 1978. Epistatic and other genetic variances in green gram varieties. Gujarat Res. J. 4:l-6. GOUD, J.V., B.C. VIRAKTAMATH, and P.V. LAXMI. 1977. Variability and correlation studies in blackgram (Phaseolus mungo (L.)). Mysore J. Agr. Sci. 11:322-325. GUNN, C.R. 1973. Recent nomenclatural changes in Phaseolus L. and Vigna Savi. Crop Sci. 13:496. GUPTA, M.P. and R.B. SINGH. 1969. Variability and correlation studies in green gram (Phaseolus aureus Roxb.). Indian J . Agr. Sci. 39:482-493. HARE, W.W. 1956. Some characters identified in cowpeas segregating for resistance to Fusarium wilt. Phytopathology 46:14. (Abstr.) HARE, W.W. 1957. Inheritance of resistance of Fusarium wilt in cowpeas. Phytopathology 47:312-313. (Abstr.) HARE, W.W. 1959. Resistance to root-knot nematodes in cowpea. Phytopathology 49:318. (Abstr.) HARLAND, S.C. 1919a. Inheritance of certain characters in the cowpea (Vigna sinensis). J. Genetics 8:lOl-132. HARLAND, S.C. 1919b. Notes on inheritance in cowpea. Agr. News, Barbados 18:20. HARLAND, S.C. 1920. Inheritance of certain characters in the cowpea (Vigna sinensis). J. Genetics 10:193-205. HARLAND, S.C. 1922. Inheritance of certain characters in the cowpea (Vigna sinensis). 111. The very small-eye pattern of the seed coat. J. Genetics 12: 254.
382
HORTICULTURAL REVIEWS
HAWTHORNE, P.L. 1943. The breeding and improvement of edible cowpeas. Proc. Amer. SOC.Hort. Sci. 42:562-564. HOFMANN, F.W. 1926. Hybrid vigor in cowpeas. J. Hered. 17:209-211. JANA, M.K. 1962. X-ray induced mutations of Phaseolus mungo L. 11. Sterility and vital mutants. Genetics Iber. 14:l-34. JANA, M.K. 1963. X-ray induced mutations of Phaseolus mungo L. I. Chlorophyll mutations. Caryologia 16:685-692. JANA, M.K. and S. APPA RAO. 1974. Inheritance of pigmentation in black gram. Indian J. Genetics 34:36-40. JANORIA, M.P. and M.A. ALI. 1970. Correlation and regression studies in cowpeas. J N K V V Res. J. 4:15-19. JINDLA, L.N. and K.B. SINGH. 1970. Inheritance of flower color, leaf shape, and pod length in cowpea (Vigna sinensis L.). Indian J. Hered. 2:45-49. JONES, S.T. 1965. Radiation-induced mutations in southern peas. J. Hered. 561273-276. JOSEPH, L.S. and J.C. BOUWKAMP. 1978. Karyomorphology of several species of Phaseolus and Vigna. Cytologia 43:595-600. JOSHI, S.N. and M.M. KABARIA. 1973. Interrelationship between yield and yield components in Phaseolus aureus Roxb. Madras Agr. J. 60:1331-1334. KABI, M.C. and P.N. BHADURI. 1978. Nodulating behaviour of colchicine induced polyploids of Phaseolus aureus Roxb. Cytologia 43:467-475. KARPECHENKO, G.D. 1925. On the chromosomes of Phaseolinae. T r u d y po Prikladnoi Botanike, Genetike i Selektses 14:143-148. KHALF-ALLAH, A.M., F.S. FARIS, and S.H. NASSAR. 1973. Inheritance and nature of resistance to cucumber mosaic virus in cowpea, Vigna sinensis. Egypt. J . Genetics Cytol. 2:274-282. KHANNA, A.N., B. SINGH, and S.M. VAIDYA. 1962. Crossability studies in search of new characters. Allahabad Fmr. 36:20-21. KHERADNAM, M., A. BASSIRI, and M. NIKNEJAD. 1975. Heterosis, inbreeding depression, and reciprocal effects for yield and some yield components in a cowpea cross. Crop Sci. 15:689-691. KHERADNAM, M. and M. NIKNEJAD. 1971a. Crossing technique in cowpeas. Iran J. Agr. Res. 1:57-58. KHERADNAM, M. and M. NIKNEJAD. 1971b. Combining ability in cowpeas (Vigna sinensis L.). 2.Pflanzenzucht. 66:312-316. KHERADNAM, M. and M. NIKNEJAD. 1974. Heritability estimates and correlations of agronomic characters in cowpea (Vigna sinensis L.). J. Agr. Sci. 82:207-208. KOHLI, K.S., C.B. SINGH, A. SINGH, K.L. MEHRA, and M.L. MAGOON. 1971. Variability of quantitative characters in a world collection of cowpea; interregional comparisons. Genetics Agrar. 25:231-242. KOLHE, A.K. 1970. Genetic studies in Vigna sp. Poona Agr. Coll. Mag. 59: 126-137.
GENETICS OF VZGNA
383
KRISHNAN, R. and D.N. DE. 1965. Studies on pachytene and somatic chromosomes of Phaseolus aureus. Nucleus 8:7-16. KRISHNAN, R. and D.N. DE. 1968a. Suppression of nucleolus-organiser in Phaseolus. Nucleus 11:155-159. KRISHNAN, R. and D.N. DE. 196813. Cytogenetical studies in Phaseolus. 11. Phaseolus mungo X tetraploid Phaseolus species and the amphidiploid. Indian J. Genetics Plant Breeding 28:23-30. KRISHNAN, R. and D.N. DE. 1968c. Cytogenetical studies in Phaseolus. I. Autotetraploid Phaseolus aureus X a tetraploid species of Phaseolus and the backcrosses. Indian J. Genetics Plant Breeding 28:12-22. KRISHNASWAMI, S., A.K. FAZLULLAH KHAN, and S.R. SREE RANGASAMY. 1973. Association of metric traits in mutants of Phaseolus aureus Roxb. Madras Agr. J. 60:1323-1326. KRISHNASWAMY, N., K.K. NAMBIAR, and A. MARIAKULANDAI. 1945. Studies in cowpea (Vigna unguiculata (L.) Walp.). Madras Agr. J. 33:145160, 193-200. KRUTMAN, S., S.C. ARAUJO, and M.S. DESOUZA. 1975. Melhoramento do feijoeiro de Macassar Vigna unguicula ta Walp, hibirdacao e selecao. Ciencia e Cultura 27(7, suppl.):256. KUMAR, L.S.S. 1945. A comparative study of autotetraploid and diploid types in mung (Phaseolus radiatus Linn.). Proc. Indian Acad. Sci. 21B:266-268. KUMAR, L.S.S. and A. ABRAHAM. 1942a. Induction of polyploidy in crop plants. Curr. Sci. 11:112-113. KUMAR, L.S.S. and A. ABRAHAM. 1942b. A study of colchicine induced polyploidy in Phaseolus radiatus L. J. Uniu. Bombay 11:30-37. KUMAR, P., R. PRAKASH, and M.F. HAQUE. 1976a. Floral biology of cowpea (Vigna sinensis L.). Trop. Grain Legume Bul. 6:9-11. KUMAR, P., R. PRAKASH, and M.F. HAQUE. 1976b. Interrelationsip between yield components in cowpea (Vigna sinensis L.1. Proc. Bihar Acad. Agr. Sci. 24:13-18. LAKSHMI, P.V. and J.V. GOUD. 1977. Variability in cowpea (Vigna sinensis L.). Mysore J. Agr. Sci. 11:144-147. LAL, S., M. SINGH, and M.M. PATHAK. 1976. Combining ability in cowpea. Indian J. Genetics Plant Breeding 35:375-378. LEFEBVRE, C.L. and H.S. SHERWIN. 1950. Inheritance of resistance to bacterial canker (Xanthomonas uignicola) in cowpea, Vigna sinensis. Phytopathology 40:17-18. (Abstr.) LELEJI, 0.1. 1975. Inheritance of three agronomic characters in cowpea (Vignu unguiculata L.). Euphytica 24:371-378. LIAN, T.S. 1975. Studies on varietal performance and agronomic characters of long bean (long bean varietal and correlation study). Mardi Res. Bul. 3:l-13. LOUIS, I.H. and M. KADAMBAVANA SUNDARAM. 1975. Induction of white eye mutant in cowpea (Vigna sinensis L. (Savi)). Madras Agr. J. 62:9597.
384
HORTICULTURAL REVIEWS
LUTHRA, J.P. and K.B. SINGH. 1978. Genetic variability and correlations in the F3 populations of blackgram. Indian J. Agr. Sci. 48:729-735. MACKIE, W.W. 1934. Breeding for resistance in blackeye cowpeas to Fusarium wilt, charcoal rot, and nematode root knot. Phytopathology 24:1135. (Abstr.) MACKIE, W.W. 1939. Breeding for resistance in blackeye cowpeas to cowpea wilt, charcoal rot, and root-knot nematode. Phytopathology 299326. (Abstr.) MACKIE, W.W. 1946. Blackeye beans in California. Unio. Calif. Agr. Expt. Sta. Bul. 696. MACKIE, W.W. and F.L. SMITH. 1935. Evidence of field hybridization in beans. J. Amer. Soc. Agron. 27:903-909. MAK, C. and T.C. YAP. 1977. Heterosis and combining ability of seed protein, yield, and yield components in long bean. Crop Sci. 17:339-341. MALHOTRA, R.S., K.B. SINGH, and J.S. SODHI. 1973. Discriminant function in Phaseolus aureus Roxb. Madras Agr. J. 60:1327-1330. MALHOTRA, V.V. and K.B. SINGH. 1976. Genetic variability and path coefficient analysis for protein in green gram (Phaseolus aureus Roxb.). Egypt. J. Genetics Cytol. 5:170-173. MALHOTRA, V.V., S. SINGH, and K.B. SINGH. 1974. Yield components in green-gram (Phaseolus aureus Roxb.). Indian J . Agr. Sci. 44:136-141. MANN, A. 1914. Coloration of the seed coat of cowpeas. J. Agr. Res. 2:33-57. MATSUURA, H. 1933. A bibliographical monograph on plant genetics (genic analysis), 2nd edition. Hokkaido Imperial University, Tokyo, Japan. pp. 296299. MENANCIO, D.I. and D.A. RAMIREZ. 1977. Genetic polymorphism and ontogenetic isozyme patterns of Cercospora leaf spot resistant and susceptible varieties of mung bean. Philip. J. Crop Sci. 2:197-202. MISRA, R.C., R.C. SAHU, and D. TRIPATHY. 1970a. A note on heterosis in green gram (Phaseolus aureus Roxb.). Curr. Sci. 39:190-191. MISRA, R.C., R.C. SAHU, and D. TRIPATHY. 1970b. Inheritance of hypocotyl color in green gram (Phaseolus aureus Roxb.). Indian Sci. Congr. Assoc. Proc. 57:290. MITAL, R.K. 1967. Effect of colchicine on ‘mung’ (Phaseolus aureus Roxb.). Kanpur Agr. Coll. J. 27:13-21. MOORE, W.F. 1974. Studies on techniques of hybridization and the inheritance of resistance to Verticillium wilt in protepea (cowpea). PhD Thesis, Mississippi State University, State College, Miss. MORTENSEN, J.A. and W.H. BRITTINGHAM. 1952. The inheritance of pod color in the southern pea, Vigna sinensis. Proc. Amer. SOC. Hort. Sci. 59:451-456. MUKHERJEE, P. 1968. Pachytene analysis in Vigna. Chromosome morphology in Vigna sinensis (cultivated). Sci. Cult. 34:252-253. MURTY, B.K. and G.J. PATEL. 1972. Inheritance of seed coat color in green gram. Indian J. Genetics Plant Breeding 32:373-378.
GENETICS OF VZGNA
385
MURTY, B.K. and G.J. PATEL. 1973. Inheritance of some morphological characters in mung bean. Bansilal Amrital Coll. Agri. Mag. 25:l-9. MURTY, B.K., G.J. PATEL, and B.G. JAISANI. 1976. Gene action and heritability estimates of some quantitative traits in mung. Gujarat Res. J. 2:l-4. NARASIMHAM, M. 1929. A note on the pollination of black and green gram in the Godavari district. Agr. J. India 24:397-401. NORTON, J.D. 1961. Inheritance of growth habit and flowering response of the southern pea, Vigna sinensis Endl. PhD Thesis, Louisiana State University, Baton Rouge. OJOMO, O.A. 1971. Inheritance of flowering date in cowpeas (Vigna unguiculata (L.) Walp.). Trop. Agr. (Trinidad) 48:279-282. OJOMO, O.A. 1972. Inheritance of seed coat thickness in cowpeas. J. Hered. 63:147-149. OJOMO, O.A. 1974. Yield potential of cowpeas, Vigna unguiculata (L.) Walp.: Results of mass and bulk pedigree selection methods in western Nigeria. Nigerian Agr. J. 11:150-156. OJOMO, O.A. 1977. Morphology and genetics of two gene markers, 'swollen stem base' and 'hastate leaf' in cowpea, Vigna unguiculata (L.) Walp. J. Agr. Sci. 88227-231. OLIVER, G.W. 1910. New methods of plant breeding. US. Dept Agr. Bur. Plant Industry Bul. 167. ORTON, W.A. 1913. The development of disease resistant varieties of plants. Compt. Rendn. & Rapp. Iv" Conf. Intern. Genetique, Sept. 18-23, 1911, Paris. Nasson et Cie., Paris. p. 247-261. OTOUL, E., R. MARECHAL, G. DARDENNE, and F. DESMEDT. 1975. Des dipeptides soufres differencient mettement Vigna radiata de Vigna mungo. Phytochemistry 14:173-179. PARTRIDGE, J.E. and N.T. KEEN. 1976. Association of the phytoalexin kievitone with single-gene resistance of cowpeas to Phytophthora uignae. Phytopa tho logy 66:426-429. PATHAK, G.N. and B. SINGH. 1963. Inheritance studies in green gram. Indian J. Genetics Plant Breeding 23:215-218. PATHAK, G.N. and K.P. SINGH. 1961. Inheritance of hairy character on pods in black gram (Phaseolus mungo L.). Curr. Sci. 30:434-435. PIPER, C.V. and W.J. MORSE. 1914. Five oriental species of beans. US. Dept. Agr. Bul. 119. POKLE, Y.S. 1972. Spontaneous mutation in mung (Phaseolusaureus Roxb.). Sci. Cult. 38:142. POKLE, Y.S. and N.N. DESHMUKH. 1972. Keel cap-a new method of pollination in Papilionaceous flowers. Punjabrao Krishi Vidyapeeth Res. J. l : 137-139. POKLE, Y.S. and M.T. NOMULWAR. 1975. Variability studies in some quantitative characters of mung (Phaseolus aureus Roxb.). Punjabrao Krishi Vidyapeeth Res. J. 3:129-132.
386
HORTICULTURAL REVIEWS
POKLE, Y.S. and V.N. PATIL. 1975. Path coefficient analysis in green-gram (Phaseolus aureus Roxb.). Sci. Cult. 41:265-266. PREMSEKAR, S. and V.S. RAMAN. 1972. A genetic analysis of the progenies of the hybrid Vigna sinensis (L.) Savi. and Vigna sesquipedalis (L.) Fruw. Madras Agr. J. 159:449-456. PURSEGLOVE, J.W. 1968. Tropical crops: dicotyledons. John Wiley & Sons, New York. PURSS, G.S. 1958. Studies on varietal resistance to stem rot (Phytophthora vignae Purss) in the cowpea. Queensland J. Agr. Sci. 15:l-14. RACHIE, K.O., K. RAWAL, and J.D. FRANCKOWIAK. 1975. A rapid method of hand crossing cowpeas. Intern. Inst. Trop. Agr. Tech. Bul. 2. RACHIE, K.O., K. RAWAL, J.D. FRANCKOWIAK, and M.A. AKINPELU. 1975. Two outcrossing mechanisms in cowpeas. Vigna unguiculata (L.) Walp. Euphytica 24:159-163. RACHIE, K.O. and L.M. ROBERTS. 1974. Grain legumes of the lowland tropics. Adv. Agron. 26:l-132. RACHIE, K.O. and P. SILVESTRE. 1977. Grain legumes. In Food crops of the lowland tropics. C.L.A. Leakey and J.B. Wills (Editors). Oxford Univ. Press, London. p. 41-74. RAMANUJAM, S., A.S. TIWARI, and R.B. MEHRA. 1974. Genetic divergence and hybrid performance in mung bean. Theor. Appl. Genetics 45:211214. RAWAL, K.M., P. BRYANT, K.O. RACHIE, and W.M. PORTER. 1978. Cross pollination studies of male-sterile genotypes in cowpeas. Crop Sci. 18: 283-285. RAWAL, K.M., W.M. PORTER, J.D. FRANCKOWIAK, I. FAWOLE, and K.O. RACHIE. 1976. Unifoliate leaf: a mutant in cowpeas. J. Hered. 67: 193-194. REEDER, B.D., J.D. NORTON, and O.L. CHAMBLISS. 1972. Inheritance of bean yellow mosaic virus resistance in southern pea, Vigna sinensis (Torner). J . Amer. SOC. Hort. Sci. 97:235-237. ROBINSON, R.W., H.M. MUNGER, T.W. WHITAKER, and G.W. BOHN. 1976. Genes of the Cucurbitaceae. HortScience 11:554-568. ROGERS, K.M., J.D. NORTON, and O.L. CHAMBLISS. 1973. Inheritance of resistance to cowpea chlorotic mottle virus in southern pea, Vigna sinensis. J. Amer. SOC. Hort. Sci. 98:62-63. ROY, R.S. and R.H. RICHHARIA. 1948. Breeding and inheritance studies on cowpea, Vigna sinensis. J. Amer. SOC. Agron. 40:479-489. SACKS, F.M. 1977. A literature review of Phaseolus angularis-the adzuki bean. Econ. Bot. 31:9-15. SAGAR, P., S. CHANDRA, and N.D. ARORA. 1976. Analysis of diversity in some urd bean (Phaseolus mungo) cultivars. Indian J. Agr. Res. 10:73-78. SAINI, R.G., J.L. MINOCHA, and A. SINGH. 1974. Sterile mutants in Phaseolus aureus. Sci. Cult. 40:37-38. SANTOS, I.S. 1969. Induction of mutations in mungbean (Phaseolus aureus
GENETICS OF VZGNA
387
Roxb.) and genetic studies of some of the mutants. p. 169-179.In E. Doyle (ed.) Induced mutations in plants. International Atomic Energy Agency, Vienna. (Distributed in USA by Unipub, Inc., New York.) SASAKI, T. 1922. Inheritance of eye and flower-color in the cowpea (in Japanese). J. Sci. Agr. SOC.232:19-38. SASTRAPRADJA, S. and H. SUTARNO. 1977. Vigna umbellata in Indonesia. Ann. Bogor. 6:155-167. SAUNDERS, A.R. 1952. Complementary lethal genes in the cowpea. S. Afr. J. Sci. 48:195-197. SAUNDERS, A.R. 1959. Inheritance in the cowpea (Vigna sinensis Endb.). I. Color of the seed coat. S. Afr. J. Agr. Sci. 2:285-307. SAUNDERS, A.R. 1960a. Inheritance in the cowpea (Vigna sinensis Endb.) 11. Seed coat colour pattern; flower, plant and pod colour. S. Afr. J. Agr. Sci. 3:141-162. SAUNDERS, A.R. 1960b. Inheritance in the cowpea (Vigna sinensis Endb.) 111. Mutations and linkages. S. Afr. J. Agr. Sci. 3:327-348. SAUNDERS, A.R. 1960c. Inheritance in cowpea (Vigna sinensis Endb.) IV. Lethal combinations. S. Afr. J. Agr. Sci. 3:497-515. SAWA, M. 1973. On the interspecific hybridization between the adzuki bean, Phaseolus angularis (Willd.) W.F. Wight and the green gram, Phaseolus radiatus L. I. Crossing between a cultivar of the green gram and a semi-wild relative of the adzuki bean. Jap. J. Breeding 23:61-66. SAWA, M. 1974. On the interspecific hybridization between the adzuki bean, Phaseolus angularis (Willd.) W.F. Wight and the green gram, Phaseolus radiatus L. I. On the characteristics of amphidiploid in C1generation from the cross green gram X rice bean, Phaseolus calcaratus Roxb. Jap. J Breeding 24:282-286. SEN, N.K. and J.G. BHOWAL. 1960. Colchicine-induced tetraploids of six varieties of Vigna sinensis. Indian J. Agr. Sci. 30:149-161. SEN, N.K. and J.G. BHOWAL. 1961. Genetics of Vigna sinensis (L.) Savi. Genetica 32:247-266. SEN, N.K. and J.G. BHOWAL. 1962. A male-sterile mutant cowpea. J Hered. 53:44-46. SEN, N.K. and H.R. CHHEDA. 1958. Colchicine induced tetraploids of five varieties of black gram. Indian J. Genetics Plant Breeding 19:238-248. SEN, N.K. and A.K. GHOSH. 1959. Genetic studies in green gram. Indian J. Genetics Plant Breeding 19:210-227. SEN, N.K. and A.K. GHOSH. 1960a. Studies on the tetraploids of six varieties of green gram. Proc. Nut. Inst. Sci. 26B:291-299. SEN, N.K. and A.K. GHOSH. 1960b. Inheritance of a chlorophyll deficient mutant in green gram (Phaseolus aureus Roxb.). Bal. Bot. SOC. Bengal 14: 80-81. SEN, N.K. and A.K. GHOSH. 1960c. Interspecific hybridization between Phaseolus aureus Roxb. (green gram) and P. mungo L. (black gram). Bul. Bot. SOC. Bengal 14:l-4.
388
HORTICULTURAL REVIEWS
SEN, N.K. and A.K. GHOSH. 1961. Breeding of a day-neutral type of green gram var. Sonamung from the short photoperiod one. Proc. Nut. Inst. Sci. India 27B:172-178. SEN, N.K. and M.N. HARI. 1956. Comparative study of diploid and tetraploid cowpea. Proc. 43rd Indian Sci. Congr. (III):258. (Abstr.) SEN, N.K. and M.K. JANA. 1963. Genetics of black gram (Phaseolus m u n g o L.). Genetica 34:46-57. SEN, N.K. and A. MURTY. 1960a. Effects of selection in tetraploid green gram varieties. Euphytica 9:235-242. SEN, N.K. and A.S.N. MURTY. 1960b. Inheritance of seed weight in green gram (Phaseolus aureus Roxb.). Genetics 45:1559-1562. SENE, D. 1967. Determinisme genetique de la precocite chez Vigna unguiculata (L.) Walp. Agron. Trop. (Paris) 22:309-318. SENE, D. 1968. Heredite du poids decent graines chez Vigna unguiculata (L.) Walp. (Niebe). Agron. Trop. (Paris) 23:1345-1351. SHARMA, B. 1969a. Chemically induced mutations in cowpea (Vigna sinensis L. Savi.). Curr. Sci. 38:520-521. SHARMA, B. 1969b. Induction of a wide-range mutator in Vigna sinensis. Proc. symp. on radiations and radiomimetric substances in mutation breeding, Sept. 26-29, 1969, Bombay. Bhabka Atomic Research Centre, Bombay. p. 13-22. SHRIVASTAVA, M.P., L. SINGH, and D. SHARMA. 1973. Karyomorphology of different ecotypes of green gram (Phaseolus aureus Roxb.). Jawaharla1 Nehru Krishi Vishwa Vidyalaya Res. J. 7236-90. SINCLAIR, J.B. and J.C. WALKER. 1955. Inheritance of resistance to cucumber mosaic virus in cowpea. Phytopathology 45:563-564. SINGH, A. and R.P. ROY. 1970. Karyological studies in Trigonella, Indigofera and Phaseolus. Nucleus 13:41-54. SINGH, B., A.N. KHANNA, and S.M. VAIDYA. 1964. Crossability studies in the genus Phaseolus. J. Post-grad Sch. (Indian Agr. Res. Inst.) 2:47-50. SINGH, B.C. 1975. Inbreeding depression in cowpea. p. 8. I n V. S . Motial (ed.) Seminar on recent advances in plant sciences. Association for Advancement of Plant Sciences, Kalyani, India. SINGH, B.V. and M.R. AHUJA. 1977. Phaseolus sublobatus Roxb.: A source of resistance to yellow mosaic virus for cultivated mung. Indian J. Genetics Plant Breeding 37:130-132. SINGH, C.B., K.L. MEHRA, K.S. KOHLI, A. SINGH, and M.L. MAGOON. 1977. Correlations and factor analysis of fodder yield components in cowpea. Acta Agronomica Academiae Scientiarum Hungaricae 26:378-388. SINGH, D. and T.R. MEHTA. 1953. Inheritance of lobed leaf margin in mung (Phaseolus aureus L.). Curr. Sci. 22:348. SINGH, D. and P.N. PATEL. 1977a. Studies on resistance in crops to bacterial diseases in India. Part VII. Inheritance of resistance to bacterial blight in
GENETICS OF VIGNA
389
cowpea. Indian Phytopathol. 30:99-102. SINGH, D. and P.N. PATEL. 1977b. Studies on resistance in crops to bacterial diseases in India, Part VIII. Investigations on inheritance of reactions to bacterial leaf spot and yellow mosaic diseases and linkage, if any, with other characters in mung bean. Indian Phytopathol. 30:202-206. SINGH, D. and J.K. SAXENA. 1959. A semi-dominant lethal leaf mutation in Phaseolus aureus. Indian J. Genetics Plant Breeding 1933-89. SINGH, H.B., S.P. MITAL, B.S. DABAS, and T.A. THOMAS. 1974. Breeding for photoinsensitivity and earliness in grain cowpea. Indian J . Genetics Plant Breeding 34A:77 1- 77 6. SINGH, K.B., G.S. BHULLAR, R.S. MALHOTRA, and J.K. SINGH. 1972. Estimates of genetic variability, correlation and path coefficients in urd and their importance in selection. Punjab Agr. Uniu. Res. J. 9:410-416. SINGH, K.B. and H.S. DHALIWAL. 1971. Combining ability and genetics of days to 50 percent flowering in black gram (Phaseolus mungo Roxb.). Indian J. Agr. Sci. 41:719-723. SINGH, K.B. and H.S. DHALIWAL. 1972. Combining ability for seed yield in black gram. Indian J. Genetics 32:99-102. SINGH, K.B. and R.P. JAIN. 1970. Heterosis in mungbean. Indian J. Genetics Plant Breeding 30:251-260. SINGH, K.B. and R.P. JAIN. 1971. Analysis of diallele cross in Phaseolus aureus Roxb. Theor. Appl. Genetics 41:279-281. SINGH, K.B. and R.P. JAIN. 1972. Heterosis and combining ability in cowpea. Indian J. Genetics 32:62-66. SINGH, K.B. and L.N. JINDLA. 1971. Inheritance of bud and pod color, pod attachment, and growth habit in cowpeas. Crop Sci. 11:928-929. SINGH, K.B. and R.S. MALHOTRA. 1970a. Estimates of genetic and environmental variability in mung (Phaseolus aureus Roxb.). Madras Agr. J. 57: 155-159. SINGH, K.B. and R.S. MALHOTRA. 1970b. Interrelationships between yield and yield components in mungbean. Indian J. Genetics Plant Breeding 30: 244-250. SINGH, K.B. and P.D. MEHNDIRATTA. 1969. Genetic variability and correlation studies in cowpea. Indian J. Genetics Plant Breeding 29:104-109. SINGH, K.B. and P.D. MEHNDIRATTA. 1970. Path analysis and selection indices for cowpea. Indian J. Genetics Plant Breeding 30:471-475. SINGH, K.B. and J.K. SINGH. 1970. Inheritance of black spot on seed coat and shiny seed surface in mung bean (Phaseolus aureus Roxb.). Indian J. Hered. 2:61-62. SINGH, K.B. and J.K. SINGH. 1971a. Heterosis and combining ability in black gram. Indian J. Genetics Plant Breeding 31:491-498. SINGH, K.B. and J.K. SINGH. 1971b. Inheritance of leaf shape in black gram (Phaseolus mungo L.). Sci. Cult. 37:583.
390
HORTICIJLTURAL REVIEWS
SINGH, K.K., W. HASAN, S.P. SINGH, and R. PRASAD. 1976. Correlation and regression in green gram (Phaseolus aureus Roxb.). Proc. Bihar Acad. Agr. Sci. 24:40-43. SINGH, M.K. 1973. Inheritance of seed coat color in Phaseolus radiatus L. (Syn. P. aureus Roxb.). Part 111, p. 321-322. Indian Sci. Congr. Assoc. Proc. 60th. Jan. 3-9, 1973, Panjab Univ., Chandigarh, India. Indian Sci. Congress Assoc., Calcutta. SINGH, P., I.B. SINGH, U. SINGH, and H.G. SINGH. 1975. Interspecific hybridization between mung (Phaseolus aureus Roxb.) and urd (Phaseolus mungo L.). Sci. Cult. 41:233-234. SINGH, S.P., H.B. SINGH, S.N. MISHRA, and A.B. SINGH. 1968. Genotypic and phenotypic correlations among some quantitative characters in mung bean. Madras Agr. J. 55:233-237. SINGH, T.P. 1974. Epistatic bias and gene action for protein content in green gram (Phaseolus aureus Roxb.). Euphytica 23:459-465. SINGH, T.P. and R.S. MALHOTRA. 1975. Crossing technique in mung bean (Phaseolus aureus Roxb.). Curr. Sci. 44:64-65. SINGH, T.P. and K.B. SINGH. 1970. Inheritance of clusters per node in mungbean (Phaseolus aureus Roxb.). Curr. Sci. 39:265. SINGH, T.P. and K.B. SINGH. 1972. Mode of inheritance and gene action for yield and its components in Phaseolus aureus. Canadian J. Genetics Cytol. 14:517-525. SINGH, T.P. and K.B. SINGH. 1973a. Association of grain yield and its components in segregating population of green gram. Indian J. Genetics 33:112117. SINGH, T.P. and K.B. SINGH. 1973b. Combining ability for protein content in mungbean. Indian J. Genetics Plant Breeding 33:430-435. SINGH, T.P. and K.B. SINGH. 1974a. Components of genetic variance and dominance pattern for some quantitative traits in mungbean (Phaseolus a u r e us Roxb.). 2. Pflanzenzucht. 71:233-242. SINGH, T.P. and K.B. SINGH. 197413. Heterosis and combining ability in Phaseolus aureus Roxb. Theor. Appl. Genetics 44:12-16. SINGH, U. and P. SINGH. 1975. Colchicine induced amphidiploid between mung (Phaseolus aureus Roxb.) and urd (Phaseolus mungo L.). Curr. Sci. 44:394-395. SINGH, U. and P. SINGH. 1976. Selection index as an effective aid for the improvement of grain yield in black gram (Phaseolus mungo L.). Indian J. Farm Sci. 4:26-28. SINGH, U., P. SINGH, and I.B. SINGH. 1976. Path coefficient analysis for yield attributes in black gram (Phaseolus mungo L.). Indian J. Farm Sci. 4:23-25. SINGH, U., P. SINGH, U.P. SINGH, and I.B. SINGH. 1976. Discriminant function technique for the improvement of grain yield in black gram (Vigna mungo (L.) Wilczek). Trop. Grain Legume Bul. 6:15-16.
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SINGH, U.P., U. SINGH, and P. SINGH. 1975. Estimates of variability, heritability and correlations for yield and its components in urd (Phaseolus mungo L.). Madras Agr. J. 62:71-72. SITTIYOS, P., J.M. POEHLMAN, and O.P. SEHGAL. 1979. Inheritance of resistance to cucumber mosaic virus infection in mungbean. Crop Sci. 19:5153. SOHOO, M.S., N.D. ARORA, G.P. LODHI, and S. CHANDRA. 1971. Genotypic and phenotypic variability in cowpeas (Vigna sinensis).under different environmental conditions. Punjab Agr. Uniu. J . Res. 8:159-164. SOUNDRAPANDIAN, G., R. NAGARAJAN, K. MAHUDESWARAN, and P.V. MARAPPAN. 1975. Genetic variation and scope of selection for yield attributes in black gram (Phaseolus mungo L.). Madras Agr. J. 62:318-320. SOUNDRAPANDIAN, G., R. NAGARAJAN, K. MAHUDESWARAN, and P.V. MARAPPAN. 1976. Genotypic and phenotypic correlations and path analysis in blackgram, Vigna mungo (L.). Madras Agr. J. 63:141-147. SPILLMAN, W.J. 1911. Inheritance of the “eye” in Vigna. Amer. Nut. 45: 513-523. SPILLMAN, W.J. 1912. The present status of the genetics problem. Science 35:751-767. SPILLMAN, W.J. 1913. Color correlation in cowpea. Science 38:302. SPILLMAN, W.J. and W.J. SANDO. 1930. Mendelian factors in the cowpea (Vigna species). Michigan Acad. Sci., Arts & Letters Papers 11:249-283. STRAND, A.B. 1943. Species crossing in the genus Phaseolus. Proc. Amer. SOC. Hort. Sci. 42:569-573. SWINDELL, R.E. and J.M. POEHLMAN. 1976. Heterosis in the mung bean (Vigna radiata (L.) Wilczek). Trop. Agr. 53:25-30. SWINDELL, R.E. and J.M. POEHLMAN. 1978. Inheritance of photoperiod response in mungbean (Vigna radiata (L.) Wilczek.). Euphytica 27:325-333. SWINDELL, R.E., E.E. WATT, and G.M. EVANS. 1973. A natural tetraploid mungbean of suspected amphidiploid origin. J. Hered. 64:107. TANAKA, Y., B. EPHRUSSI, E. HADARN, A. HAGBERG, T. KEMP, A. LOVE, H. NACHTSHEIM, G. PONTECORVO, and M.M. RHOADES. 1957. Report of the International Committee on Genetic Symbols and Nomenclature. Intern. Union Biol. Sci. Colloques. B30:l-6. THAKUR, R.P., P.N. PATEL, and J.P. VERMA. 1977a. Studies on resistance in crops to bacterial diseases in India. Part XI. Genetic make-up of mung bean differentials of the races of bacterial leaf spot pathogen, Xanthomonas phaseoli. Indian Phytopathol. 30:217-221. THAKUR, R.P., P.N. PATEL, and J.P. VERMA. 1977b. Independent assortment of pigmentation and resistance to Cercospora leaf spot in mung bean. Indian Phytopathol. 30:264-265. THAKUR, R.P., P.N. PATEL, and J.P. VERMA. 1977c. Genetical relationships between reactions to bacterial leaf spot, yellow mosaic and Cercospora leaf spot diseases in mungbean (Vigna radiata). Euphytica 26:765-774.
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TIKKA, S.B.S. and B.M. ASAWA. 1978. Note on selection indices in cowpea. Indian J. Agr. Sci. 48:767-769. TIKKA, S.B.S., B.M. ASAWA, and S. KUMAR. 1977. Correlated response to selection in moth bean (Vigna aconitifolia Jacq. Marechal.). Gujarat Agr. Uniu. Res. J. 3:l-4. TIKKA, S.B.S., B.M. ASAWA, R.K. SHARMA, and S. KUMAR. 1978. Path coefficient analysis of association among some biometric characters in cowpea under four environments. Genetica Polonica 19:33-38. TIKKA, S.B.S., S.N. JAIMINI, B.M. ASAWA, and J.R. MATHUR. 1977. Genetic variability interrelationships and discriminant function analysis in cowpea (Vigna unguiculata (L.) Walp.). Indian J. Hered. 9:l-9. TIKKA, S.B.S. and S. KUMAR. 1976. Association analysis Vigna aconitifolia (Jacq.) Marechal. Sci. Cult. 42:182-183. TIKKA, S.B.S., R.K. SHARMA, and J.R. MATHUR. 1976. Genetic analysis of flower initiation in cowpea (Vigna unguiculata (L.) Walp.). 2.Pflanzenzucht. 77:23-29. TIKKA, S.B.S., J.P. YADAVENDRA, P.C. BORDIA, and S. KUMAR. 1973. Variation in moth bean (Phaseolus aconitifolius Jacq.). Rajasthan J. Agr. Sci. 4:50-55. TIKKA, S.B.S., J.P. YADAVENDRA, P.C. BORDIA, and S. KUMAR. 1976. A correlation and path coefficient analysis of components of grain yield in Phaseolus aconitifolius Jacq. Genetics Agr. 30:241-248. TIWARI, AS. and S.RAMANUJAM. 1974. Partial diallel analysis of combining ability in mung bean. 2.Pflanzenzucht. 73:103-111. TIWARI, AS. and S. RAMANUJAM. 1976a. Combining ability and heterosis for protein and methionine contents in mung bean. Indian J. Genetics Plant Breeding 36:353-357. TIWARI, AS. and S. RAMANUJAM. 1976b. Genetics of flowering response in mung bean. Indian J. Genetics Plant Breeding 36:418-419. TOMAR, G.S., S. LAXMAN, and P.K. MISHRA. 1973. Correlation and path coefficient analysis of yield characters in mung bean. SABRAO Newsl. 5: 125-127. TOMAR, G.S., L. SINGH, and D. SHARMA. 1972. Effects of environment on character correlation and heritability in green gram. SABRAO Newsl. 4:49-52. TREHAN, K.B., L.R. BAGRECHA, and V.K. SRIVASTAVA. 1970. Genetic variability and correlations in cowpea, Vigna sinensis, under rainfed conditions. Indian J. Hered. 2:39-43. TRIPATHI, I.D. and M. SINGH. 1975. Association of yield components and their functions in black gram (Phaseolus mungo). Haryana Agr. Uniu. J. Res. 5:260-266. TYAGI, I.D., B.P.S. PARIHAR, R.K. DIXIT, and H.G. SINGH. 1978. Component analysis for green fodder yield in cowpea. Indian J.Agr. Sci. 48:646649. VAN RHEENEN, H.A. 1964. Preliminary study of natural cross-fertilization
GENETICS OF VIGNA
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in mung bean, Phaseolus aureus Roxb. Netherlands J. Agr. Sci. 12:260-262. VAN RHEENEN, H.A. 1965. The inheritance of some characters in the mungbean, Phaseolus aureus Roxb. Genetica 36:412-419. VEERASWAMY, R. and V.K. KUNJAMMA. 1958. A note on foliar variation in greengram or mung (Phaseolus aureus L.). Madras Agr. J. 45:151-152. VEERASWAMY, R., G.A. PALANISAMY, and R. RATHNASWAMY. 1973a. Genetic variability in some quantitative characters of Vigna sinensis (L.) Savi. Madras Agr. J. 60:1359-1360. VEERASWAMY, R., G.A. PALANISAMY, and R. RATHNASWAMY. 1973b. Yield attributes and heritability in some varieties of Phaseolus mungo L. Madras Agr. J. 60:1834-1835. VEERASWAMY, R., R. RATHNASWAMY, and G.A. PALANISAMY. 1973. Genetic variability in some quantitative characters of Phaseolus aureus Roxb. Madras Agr. J. 60:1320-1322. VENUGOPAL, R. and J.V. GOUD. 1977. Inheritance of pigmentation of cowpea. Curr. Sci. 46:277. VERDCOURT, B. 1970. Studies in the Leguminosae-Papilionoideae for the ‘flora of Tropical East Africa’: IV. Kew Bul. 24:507-569. VERMA, S.N.P. 1971a. Inheritance of photo sensitivity in mung bean (Phaseolus aureus Roxb.). Mysore J. Agr. Sci. 5:477-480. VERMA, S.N.P. 1971b. Genetic studies in black gram (Phaseolus mungo L.). Madras Agr. J. 58:304-305. VERMA, S.N.P. 1973. Linkage studies in Phaseolus mungo L. Madras Agr. J. 60:1335-1338. VERMA, S.N.P. 1977. Recombined progenies in interspecific cross between green gram (Phaseolus aureus Roxb. syn. Vigna radiatus) and black gram (Phaseolus mungo L. syn. Vigna mungo). Mysore J . Agr. Sci. 11:431-434. VERMA, S.N.P. and C.S. DUBEY. 1970. Correlation studies in black gram (Phaseolus mungo L.). Allahabad Farm. 44:419-422. VERMA, S.N.P. and J.N. KRISHI. 1969. Inheritance of some qualitative characters in green gram (Phaseolus aureus Roxb.). Indian J. Hered. 1:105-106. VIRK, D.S. and M.M. VERMA. 1977. A dominant mutation in Vigna radiata var. radiata. Crop Impr. 4:115-116. WATT, E.E. and R. MARECHAL. 1977. The difference between mung and urd beans. Trop. Grain Legume Bul. 7:31-33. WEBBER, H.J. and W.A. ORTON. 1902. Some diseases of the cowpea. 11. A cowpea resistant to root knot (Heterodera radicicola). US. Dept. Agr., Bur. Plant Ind. Bul. 17. p. 23-36. WOLLEY, J.N. 1977. Breeding cowpea, Vigna unguiculata (L.) Walp., for resistance to Maruca testulalis Geyer. PhD Thesis, University of Cambridge, King’s College. YADAV, A.K., T.P. YADAVA, and B.D. CHOUDHARY. 1979. Path-coefficient analysis of the association of physiological traits with grain yield and harvest index in greengram. Indian J. Agr. Sci. 49:86-90.
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YARNELL, S.H. 1965. Cytogenetics of the vegetable crops. IV. Legumes. Bot. Rev. 31:241-330. YOHE, J.M. and J.M. POEHLMAN. 1975. Regressions, correlations, and combining ability in mung beans (Vigna radiata (L.) Wilczek). Trop. Agr. 52: 343-352. YOUNGBLOOD, J.P. and O.L. CHAMBLISS. 1973. Inheritance of cowpea curculio resistance in southern peas. HortScience 8:283. (Abstr.)
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
8 Ammonium and Nitrate Nutrition of Horticultural Crops Allen V. Barker
University of Massachusetts, Amherst, Massachusetts 01003
Harry A. Mills
University of Georgia, Athens, Georgia 30602
I. Introduction 396 11. Nitrogen Balances 397 A. Soil and Fertilizer Nitrogen 397 1. Forms of Nitrogen in Soils 397 2. Nitrogen Inputs 398 a. Nitrogen Mineralization 398 b. Fertilizer Nitrogen 399 401 3. Soil and Fertilizer Nitrogen Loss 401 a. Leaching Loss b. Loss of Nitrogen Through the Denitrification Process 402 c. Ammonia Volatilization 403 111. Soil/Plant Relations with Nitrogen Nutrition 404 A. Acquisition of Nitrogen by Plants 404 404 1. Environmental Factors Affecting Acquisition of Nitrates 404 a. Presence and Concentration of Nitrate b. Effects of Other Ions 405 406 c. Light d. Effectsof Carbon Dioxide 407 B. Factors Affecting Acquisition of Ammonium Nitrogen by Plants 407 1. Environmental Factors Affecting Acquisition 407 a. Ammonium Concentration 407 b.pH 408 c. Other Ions 409 409 d. Light and Carbohydrate Status 2. Genetic Factors Affecting Acquisition of Nitrate and Ammonium 410 Nitrogen 41 1 C. Crop Responses to Form of Nitrogen 1.Nitrate Versus Ammonium Form 411 41 1 a. Ammonium Toxicity 395
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b. Nitrate Toxicity 412 2. Physiology of Ammonium Toxicity IV. Literature Cited 414
413
I. INTRODUCTION In most cropping systems, available nitrogen is often a more limiting factor influencing plant growth than is any other nutrient. Complicating this problem for agriculture is the fact th a t often less than 50% of nitrogen fertilizer applied to crops ultimately may be utilized by the crop (Allison 1966). Nitrate ions are highly mobile and are not adsorbed by soil colloids. Loss of NzO, N P ,and other oxides of nitrogen are recognized as major contributors to ineffective nitrogen utilization. T o offset these nitrogen losses, agriculturists often add nitrogen in large quantities to maintain adequate levels in the rhizosphere. This excessive use of nitrogen fertilizers can result in undesirable conditions such as the accumulation of nitrate in plant tissues and contamination of ground water supplies via nitrate leaching. More recently gaseous loss of nitrogen as N 2 0 has been recognized as a potential factor leading to deterioration of the ozone layer of the atmosphere (Bremner and Blackmer 1978). Application of ammoniacal fertilizer would seem to offer a potential means of increasing the utilization of applied nitrogen fertilizer because the ammonium ion is not as readily subject to leaching loss or volatilization losses as is the nitrate ion. Th e major disadvantage of ammonium nutrition is th at many plants are sensitive to continuous ammonium nutrition. However, nitrification, the soil process by which ammonium is converted to nitrate, occurs rapidly in most cropped soils, limiting the effectiveness of applying ammoniacal fertilizer as a means to increase the utilization of fertilizer N, but also alleviating the potential toxicity associated with continuous ammonium nutrition. Many sources of nitrogen contribute to the nitrogen balance under the diversified cropping conditions with horticultural crops, but the major inputs of nitrogen can be identified as mineralization of organic matter, nitrogen fixation, and fertilizers (Stanford et al. 1969). T h e contribution of nitrogen mineralization to the nutrition of most crops is limited, and supplemental nitrogen is required under most cropping conditions with mineral soils to achieve maximum yields. Though approximately 35,000 tons of elemental nitrogen cover each acre of the earth’s surface, this gaseous form of nitrogen can be utilized directly only by plants forming a symbiotic relationship with certain bacteria, or indirectly through plant decomposition and the decomposition or release from microorganisms capable of fixing nitrogen (Mulder et al. 1969). Thus, the inability of most horticultural crops to fix nitrogen limits the adaptation of sym-
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biotic fixation to the leguminous crops or to where a leguminous crop is incorporated into a crop rotation system. With horticultural crops it is generally recognized that nitrogen fertilizer is necessary to produce yields or growth rates considered to be economical under most soil and cropping conditions. Though several avenues of nitrogen loss from media have been identified (Parr 1973), the major avenues of nitrogen loss are leaching of the nitrate ion, denitrification, and ammonia volatilization (Keeney and Walsh 1972; Gardner 1965; Parr 1973; Allison 1973; Batholomew and Clark 1965). T h e rate and form of nitrogen utilized by plants are highly influenced by both internal and external factors. External factors such as the form of nitrogen (Maynard and Barker 1969), the concentration and ratio of nitrate and ammonium (McElhannon and Mills 1978), availability of molecular nitrogen (Pilot and Patrick 1972), pH, light, temperature and moisture (Bremner and Shaw 1958; Mahendrappa and Smith 1966), and the presence of a particular anion or cation (Kirby and Mengel 1967) influence the absorption and utilization of nitrogen by plants. Internal factors such as the dual or multiphasic patterns of ion uptake for a particular plant species (Nissen 1974), rate of absorption of other anions and cations (Barker et al. 1965), protein synthesis (Barker 1968), nitrate reductase capacity, and physiological age of the plant (McKee 1962) influence the rate of absorption and assimilation of nitrogen in horticultural crops. I t is our intention in this paper to review selected factors instrumental in the nitrogen nutrition of horticultural crops. 11. NITROGEN BALANCES A. Soil and Fertilizer Nitrogen 1. Forms of Nitrogen in Soils.-Analysis of the soil nitrogen composition shows that nitrogen assumes several valence states and exists in many ionic and molecular combinations. Elemental nitrogen (N2)is one of the more abundant forms of soil nitrogen and exists in the soil atmosphere, dissolved in the soil water, or adsorbed to the soil complex. In comparison to N2, some of the more highly oxidized forms of soil nitrogen are nitrous oxide (N20), nitrogen dioxide (NO,), nitric oxide (NO), and the nitrite (NOz -) and nitrate (NOa -1 ions. T h e primary reduced forms of nitrogen in comparison to Nz are the amino radical (-NH2) contained in amino acids, proteins, and other nitrogenous compounds, ammonia (NH,), and the ammonium ion (NH,'). Bartholomew and Clark (19651, Black (1968), Allison (19731, and Nielsen and MacDonald (1978a,b) have presented excellent reviews on nitrogen and may be consulted for addi-
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tional specific information on inorganic and organic forms of nitrogen in soils, their sources and fate. 2. Nitrogen Inputs.-a. Nitrogen Mineralization.-More than 90% of the total nitrogen in soils exists in organic combinations. Heterotrophic soil microorganisms are involved in the mineralization process termed ammonification in which the ammonium ion is released from organic combinations. Ammonium ions released from organic combinations are subjected to various fates: (1) leached with percolating water, (2) adsorbed to the negatively charged particles of clay minerals and soil organic matter, (3) immobilized by various soil microorganisms, (4) volatilized a s ammonia gas primarily under alkaline condition, (5) utilized by plants to satisfy their nitrogen requirements, or (6) nitrified to the highly mobile nitrate ion. Nitrification occurs rapidly in most soils; this is the primary fate of soil ammonium. Th e nitrification process is mediated by a number of genera of facultative aerobic bacteria, though with most cropped soils the autotrophs, Nitrosomonas and Nitrobacter, are the primary bacterial species concerned. T he contribution of the nitrogen mineralization process to the annual nitrogen balance on cropland was estimated by Stanford et al. (1969) to be in excess of 3 million tons annually. Though many factors such as environmental conditions and cultural practices influence the rate of nitrogen mineralization, the soil type and organic composition are primary factors influencing the quantity of nitrogen released for crop utilization. With mineral soils of the temperate region, nitrogen mineralization is generally 3% or less annually of the total organic N (Bremner 1965; Allison 1973), and as such is less than adequate to supply the nitrogen requirements of most crop plants. With organic soils or histosols, the normal rate of nitrogen mineralization is usually adequate in terms of supplying the quantity of nitrogen needed by most crops (Allison 1973). However, due to various factors such as leaching of the highly mobile nitrate ion and the gaseous loss of nitrogen through the denitrification process, adequate nitrogen may not be available during peak demand periods (Guthrie and Duxbury 1978). High-nitrogen-requiringcrops such as celery have responded to nitrogen fertilization in the peat soil of Everglades (Beckenbach 19391, and vegetable crops grown on the muck soils of New York (Guthrie and Duxbury 1978) and peat soils of Michigan (Allison 1973) have responded to nitrogen fertilization. In contrast, in well drained peats of the USSR (Skoropanou 1968) and in Israeli peats (Aunimelech 1971), higher nitrate levels are generally found, and crops in these soils show little response to nitrogen fertilizers. Th e differences between these organic soils probably can be attributed to the quantity of nitrogen lost through leaching and denitrification.
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The mineralization rate of nitrogen from nursery media composed of organic components, such as peat and bark, is generally considered to contribute little to maintaining the nitrogen balance (Goh and Haynes 1977). Though a high proportion of the nitrogen added as fertilizer may be immobilized in these types of media, the fate and subsequent availability of this nitrogen is presently not known.
b. Fertilizer Nitrogen.-Anhydrous ammonia, nitrogen solutions, and various formulations with urea are leading sources of nitrogen applied to various horticultural crops (Nelson 1968). The horticultural industry’s ever increasing dependence on ammoniacal fertilizers arises from the low efficiency of nitrogen fertilizers due primarily to nitrate leaching and denitrification losses (Allison 1966; Parr 1973). Ammoniacal fertilizers offer a means of increasing the efficiency of fertilizer nitrogen as the positively charged cation is not as readily subject to leaching loss or gaseous loss as is the nitrate ion (Parr 1973). However, rapid conversion of the ammonium ion to nitrate limits the effectiveness of applying ammoniacal nitrogen to cropped soils as a means of increasing the utilization of fertilizer nitrogen (Alexander 1965; Parr 1973). Goring (1962) reported that 66 to 92% of all added ammonium is converted to nitrate in most soils within 4 weeks after application. Lorenz et al. (1972) found that 90% of the nitrogen from (NH4I2SO4and urea had nitrified and leached from the fertilizer band within 40 days after application to a Hesperia fine sandy loam soil in California. For acidic soils of Florida, Polizotto et al. (1975) reported that (NH4)&304was toxic to potato plants. The adverse plant response to (NH4I2SO4was attributed to the low rates of nitrification in these acidic soils. The use of urea and ammoniacal fertilizers in the acidic soils of Florida has resulted in adverse effects on plant growth in the leather leaf fern and citrus industries (Mills, personal observations). Apparently during heavy rains or during periods of high temperatures when frequent irrigations are applied, the nitrate ion is leached from the rhizosphere, exposing these crops to a higher level of the ammonium ion. When these conditions exist, two adverse effects on plant growth occur. Competition between the ammonium ion and potassium reduces the potassium level in the plant tissue and in turn can cause plant wilting. A second effect is a reduction in plant growth. Several factors cause the reduction in plant growth, two of which are the acidifying effects of ammonium in the rhizosphere (see section on pH) and a reduction in the mobility of nitrogen compounds in plants cultured in 50% or more ammonium. Sparks (Sparks and Baker 1975) found that pecan seedlings grown in sand culture on NH4N03 developed symptoms of ammonium toxicity and that the mobility of nitrogen compounds from older to younger leaflets was very low. This reduced mobility of nitrogen compounds has been observed in
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southernpeas (Sasseville an d Mills 1979a,b) a n d lima beans (McElhannon and Mills 1978) when ammonium supplied a t least 50% of the nitrogen in solution culture studies. To increase the efficiency of fertilizer nitrogen, controlled or slowrelease nitrogen fertilizers are employed in all areas of the horticultural industry. Byrne and Lunt (1962) reported th a t 25% of the nitrogen in urea-formaldehyde is soluble in cold water and, in a greenhouse evaluation, found that the nitrogen mineralization rate was 6 to 7% per month. Lorenz et al. (1972) in a field study in California found th a t half of the nitrogen from urea-formaldehyde remained in the fertilizer band 120 days after application to a potato crop. Slightly higher release rates were reported with sulfur-coated urea. Results with these slow-release fertilizers indicate that excellent plant responses can be obtained with slowly maturing crops; however, for rapidly maturing crops, such as vegetables, the release rate of nitrogen may be too slow to be an effective nitrogen source (Lorenz et al. 1972). Even in media where the ammonium ions are rapidly adsorbed by the soil and organic fractions, loss of the nitrogen fertilizer may occur (Cribbs and Mills 1979). Mills and Pokorny (1978) found th a t the growth of tomato plants was reduced significantly as ammonium supplied more of the nitrogen form in a pine bark and sand media. However, incorporating the nitrification-denitrification inhibitor nitrapyrin into the media increased nitrate retention, total nitrogen in the plant tissue, and plant growth. Without the use of nitrapyrin these results would indicate th a t the restriction in growth was due to ammonium toxicity. However, the increase in growth, total nitrogen, and soil nitrates with nitrapyrin incorporated into the media suggests th at the ammonium was unavailable (possible tied up by the bark) and after being converted to nitrate was lost before its utilization by plants could occur. These same trends have been observed in field studies with corn in which soil nitrate levels, plant total nitrogen, and yield were increased when denitrification was inhibited with nitrapyrin (Mills, unpublished data). T he determination of whether to use a slow-release nitrogen fertilizer or single or split applications of nitrogen fertilizer must take into consideration t hat the nitrogen requirements of many crops may be greater a t certain times during the growth cycle. Sayer (1948), Terman and Noggle (19731, and Bar-Yosef and Kafkafi (1972) reported th a t the greatest accumulation of nitrogen in corn occurred between 30 days and 45 days after planting. With sweet corn a rapid increase in the nitrogen requirements was observed a t the whorl stage (25 days after planting), and the nitrogen requirements increased in an exponential fashion until tasseling (Mills, unpublished data). McColm and Miller (1971) reported t ha t maximum yields of cucumber fruits occurred 55 days after planting
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with over 40% of the nitrogen being taken up during the period of rapid fruit development. Mills et al. (1976a) found that radishes ceased to absorb appreciable quantities of nitrogen when root was three-fourths of its marketable size. Roy and Wright (1974) found that nitrogen uptake in soybeans was greatest a t periods corresponding with peak vegetative growth and pod filling. Sasseville and Mills (1979a,b) observed a similar trend with southernpeas. With lima beans peak nitrogen uptake periods were identified with specific physiological stages, flower initiation, pod initiation, and pod filling (McElhannon and Mills 1978). In addition to the time of nitrogen application, the selective absorption of a particular nitrogen form during the growth cycle must be considered. McKee (1962) stated that seedlings of several species absorbed more ammonium than nitrate early in their growth cycle while later this trend was reversed. Ingestad (1972) found that nitrate was accumulated more rapidly by cucumber seedlings than was ammonium. With southernpeas, no preference for ammonium or nitrate was observed early in the growth cycle through flower initiation when these plants were cultured in a 50% nitrate-50% ammonium solution (Sasseville and Mills 1979a,b). However, a preference for nitrate was observed during reproductive development and was intensified under nitrogen-deficient conditions. Similar trends were observed with lima beans (McElhannon and Mills 1978). Kafkafi et al. (1971) reported an ammonium preference with tomatoes though physiological disorders occurred under continuous ammonium nutrition. Additional factors influencing the selectivity of plants for a particular nitrogen form are discussed in subsequent sections. Other problems associated with the extensive use of nitrogen fertilizers have been identified. The nitrification of ammonium to nitrate can result in a nitrate-rich growing medium, promoting conditions favoring excessive accumulation of nitrate in certain plant tissue and ground water resources (Wright and Davidson 1964). In addition, fertilizer applications and the evolution of nitrous oxides through denitrification have been implicated as having a detrimental effect on the ozone layer in our atmosphere (Bremner and Blackmer 1978). 3. Soil and Fertilizer Nitrogen Loss.-a. Leaching Loss.-Leaching of the negatively charged nitrate ion is a significant avenue of nitrogen loss from cropped soils and media. Allison (1966) identified several factors contributing to the leaching loss of nitrogen: (1)the quantity and form of soluble nitrogen, (2) the quantity and time of rainfall, (3) infiltration and percolation rates, (4)water-holding capacity and soil moisture content a t the time of rainfall, (5) evapotranspiration, (6) vegetative cover, (7) upward movement of nitrogen during droughts, and (8) nitrogen availability and uptake by the crop. In addition to these factors the
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cations associated with the nitrate ion and temperature were found to significantly influence leaching loss (Burns and Dean 1964). Stanford et al. (1969) estimated th at over 2 million tons of N are lost annually from cropland through leaching, but Allison (1973) suggested th a t few d a ta show accurately the amount of nitrogen lost through leaching under field conditions. A summary of lysimeter experiments measuring the leaching loss of nitrogen was presented by Allison (1965, 1966). T he intensive use of irrigation in the horticultural industry increases the potential for nitrogen leaching loss. Studies by Bingham et al. (1971), Stewart et al. (1968), and Ward (1970) have shown a direct correlation between leaching of fertilizer nitrogen and irrigation practices. T he extensive use of irrigation with greenhouse and containerized crops and the subsequent effects on nitrogen loss have not been delineated. Preliminary studies with nursery media by Mills and Pokorny (unpublished da t a ) suggest th at up to 33% of the applied nitrogen can be lost by leaching.
b. Loss of Nitrogen Through the Denitrification Process-Denitrification is a dissimilatory reduction process in which molecular nitrogen or an oxide of nitrogen is formed from the reduction of nitrite and nitrate ions. In soils where atmospheric oxygen is available, Nz and NzO are the primary nitrogen gases evolved in appreciable quantities (Hauck and Melsted 1956; Nommik 1956). Several environmental factors have been identified as influencing biodenitrification. In general, biodenitrification in soils increases with increasing water content (Mahendrappa and Smith 1966),increasing temperature, pH and carbon substrate (Bremner and Shaw 1958), decreasing oxygen availability (Pilot and Patrick 1972), and the presence of a living plant (Cribbs and Mills 1979). A generalized pathway for biodenitrification is given by the following equation:
acid
However, biodenitrification losses from field soils are difficult to determine due to variations among bacterial species, the presence of molecular nitrogen, and changes in the soil environment resulting from the equipment necessary to measure the denitrification process (Bollag 1970).
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Most of the early investigators of the denitrification process indicated that this process was not a significant avenue of nitrogen loss in most soils, though more recent investigations have identified a significant loss of nitrogen through the biodenitrification process occurring as short bursts of NzO evolution (Bremner and Blackmer 1978; McGarity and Rajaratnum 1973). Woldendorp (1962) reported that biodenitrification losses are greater in the rhizosphere where there is a high demand for oxygen by both the roots and the rhizosphere microorganisms feeding on root exudates and cell debris. Mills and Pokorny (1978) and Cribbs and Mills (1979) were able to show that this nitrogen loss through the denitrification process from media containing a plant was great enough to reduce plant growth and total nitrogen content. This is significant in that most of the earlier studies determining denitrification losses were made without the presence of a plant and may indeed explain the earlier concepts regarding low losses of nitrogen through the denitrification process. In addition, the findings of Mills and Pokorny (1978) show that the quantity of nitrogen lost through the denitrification process increases with increments of organic matter, suggesting that denitrification from an organic nursery medium would be extensive. Though the total quantity of nitrogen lost is greater in organic media, loss of nitrogen from soils low in organic matter through the denitrification process is significant and reduces overall plant growth and yield (Mills and Pokorny 1978; Mills, unpublished data). Losses of gaseous nitrogen by chemical means from well drained acidic soils have been suggested (Nelson and Bremner 1969). The quantity of nitrogen lost by this means for cropped soils is generally not known. The complexity of the denitrification process is apparent in that gaseous nitrogen losses can occur partly by biological means and partly by chemical means (Steen and Stojanovic 1971).
c. Ammonia Volatilization.-Rapid losses of gaseous nitrogen have been reported after application of urea and ammonium fertilizers. Several environmental factors that enhance ammonia volatilization from soils have been identified. Ernst and Massey (1960) found that temperature, rate of soil drying, initial soil moisture content, depth of urea incorporation, method of nitrogen application, and soil reactions influenced nitrogen loss as ammonia. DuPlessis and Kroontje (1964) found that ammonia volatilization was directly related to soil pH. Mills et al. (1974) reported that loss of nitrogen as ammonia gas with the soil pH below 7.2 would not result in substantial volatilization loss. Also, the quantity of ammonium nitrogen applied to soils influences the quantity of ammonium volatilization (Parr and Papendick 1966; DuPlessis and Kroontje 1964). Ammonia volatilized from an organic medium is probably very low (Mills
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and Pokorny 1978) and would not be a primary avenue of nitrogen loss under these cultural conditions. 111. SOIL/PLANT RELATIONS WITH NITROGEN NUTRITION A. Acquisition of Nitrogen by Plants 1. Environmental Factors Affecting Acquisition of Nitrates.-The uptake mechanism for nitrate appears to be very complex and to be altered by a number of environmental factors which affect the external supply of nitrate and the physiological and biochemical processes operating within plants.
a. Presence and Concentration of Nitrate.-The nitrate uptake system of roots is apparently inducible, requiring the presence of nitrate for activation (see Jackson 1978). Plant tissues or cells cultured in the absence of nitrate exhibit a lag in uptake upon exposure to nitrate. The rate of uptake increases steadily to a relatively constant value (Minotti et al. 1968; Jackson et al. 1972,1973;Ezeta and Jackson 1975; Neyra and Hageman 1975; Rao and Rains 1976a,b). Nitrate has been shown to induce nitrate reductase (Heimer 1975), and a relationship between nitrate reductase and uptake is possible (Huffaker and Rains 1978; Jackson 1978; Schrader 1978). However, treatments with tungstate or vanadium which inhibits nitrate reductase have not been shown to prevent the development of the nitrate transport system (Heimer et al. 1969; Heimer and Filner 1971; Huffaker and Rains 1978). Transfer of bacteria to a nitrate-free medium resulted in the decline of activity for nitrate uptake (Goldsmith et al. 1973). This decline was more rapid than that of nitrate reductase activity. On the other hand, high concentrations of molybdenum, a constituent of nitrate reductase, appear to increase the activity of the nitrate transport system (Lycklama 1963). More than one nitrate transport system may operate in plants (Huffaker and Rains 1978). Nitrate uptake increases sharply with increases in the external supply of nitrate, and when the supply is high, nitrates will be absorbed in excess of the needs of plants and will accumulate internally. The external supply of nitrate is probably the most important environmental factor controlling the accumulation of nitrates in plants (see Wright and Davidson 1964; Maynard et al. 1976). Generous nitrogen fertilization of crops may elevate concentrations in edible plant parts sufficiently to be of concern in the health of humans or livestock consuming the vegetation (Wright and Davidson 1964; Maynard et al. 1976; Maynard 1978). Kinetic studies on the uptake of nitrate in relation to external concentrations are confounded by the metabolism of nitrate after its absorption. However, sufficient studies have shown that the mechanism is com-
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plex. At low NOs - concentrations, less than 0.001 M , uptake fits a simple Michaelis-Menten equation (Huffaker and Rains 1978). At higher concentrations, a dual mechanism of absorption becomes apparent so that Michaelis-Menten kinetics are not followed. The second mechanism is probably the functional one which leads to nitrate accumulation in plants growing in a highly fertilized medium. Plants which have efficient mechanisms for nitrate absorption appear to have relatively low Michaelis-Menten (Km) values and, consequently, have a high affinity for nitrate in soils of low fertility. The ecological significance is that the ability of plants to survive and to compete in soils of varying fertility may be shown by differences in their kinetics of nitrate absorption (Huffaker and Rains 1978).
b. Effects of Other Ions.-Nitrate absorption may be affected by the presence of other ions in the environment of the root. Normally, one considers that ions with similar charge and chemical properties might compete in absorption by plants; but, on the other hand, ion absorption is very selective, and little interference is encountered by similar ions a t low concentrations (Elzam and Epstein 1965; Elzam and Hodges 1967; Epstein 1972). However, in the system of complex kinetics a t higher concentrations of ions, ion absorption is generally competitive. This phenomenon may occur in nutrient solutions or in highly fertilized fields. Nitrate absorption, nevertheless, appears to be influenced little by similar ions such as chloride, bromide, or sulfate (Rao and Rains 1976a), but cations, such as calcium, potassium, and ammonium, affect nitrate uptake significantly (Minotti et al. 1968, 1969a,b; Rao and Rains 1976a; Jackson 1978). Increasing the supply of calcium or potassium generally accelerates the rate of nitrate uptake, whereas ammonium ions have an inhibitory effect. The effect of cations, like calcium, on nitrate uptake may be to counter the negative charges on the roots’ cell walls so that nitrate ions may migrate more closely to the plasmalemma and its uptake sites than they could in the absence of these ions (Elzam and Epstein 1965). The mode of the inhibitory action of ammonium ions is also unclear. Jackson (1978) proposed and discussed a number of alternative mechanisms by which ammonium nutrition may alter nitrate accumulation in plants. In microorganisms and cell cultures, amino acids have been implicated as being the inhibitory factor (Goldsmith et al. 1973; Heimer and Filner 1971). However, in order for ammonium ions to exhibit their inhibitory effect on nitrate uptake by plants, they must be present continuously, for pretreatment of roots with ammonium ions does not inhibit subsequent nitrate uptake (Minotti et al. 1969a; Jackson et al. 1972). The inhibition of nitrate uptake in the presence of ammonium ions is apparently incomplete and may be nutritionally unimportant, for the toxicity of am-
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monium ions is diminished in the presence of nitrate, and the growth of plants in a medium with half of the nitrogen supplied as nitrate and half as ammonium is usually as good as that occurring when all of the nitrogen is supplied as nitrate (Mills et al. 1976a,b; McElhannon and Mills 1977). Uptake of nitrate is apparently sensitive to the external hydrogen ion concentration. Above pH 6, nitrate uptake decreases (Rao and Rains 1976a). High acidity does not affect nitrate uptake until the pH falls below 4.5 (Minotti et al. 1969a). Rao and Rains (1976a) observed no decline in nitrate uptake a t pH values as low as 4.0. The driving force for the influx of nitrate has been suggested as being a pH gradient across the plasmalemma (Hodges 1973) with an ATPase extruding hydrogen ion vectorially across the membrane. The reduction of nitrate in the cell could operate in maintaining a hydrogen or hydroxyl ion balance within the cell and a high pH relative to the ambient solution, thus again associating nitrate reductase activity with nitrate transport into the cell.
c. Light.-An effect of light on nitrate acquisition may be related to the supplying of materials to provide energy for nitrate uptake. The rate of nitrate uptake by decapitated wheat seedlings is considerably less than that attained by illuminated intact seedlings (Minotti et al. 1968). Excision of shoots usually causes a greatly diminished rate of nitrate uptake, and nitrate leakage from previous absorption may occur (Minotti and Jackson 1970). Supplying an energy source such as glucose in the nutrient solution aids in the maintenance of uptake activity by excised roots (Minotti and Jackson 1970). Absorption of nitrate appears to be more sensitive to decapitation of shoots and to the removal of an energy source than that of other ions, such as chloride or phosphate (Jackson et al. 1973; Koster 1963). A continual supply of energy appears to be essential for maintenance of nitrate uptake. Light and photosynthesis appear to be the sources of energy in intact plants. Nitrate reduction and its assimilation into organic compounds are closely related to photosynthesis in green plants (Huffaker and Rains 1978; Schrader 1978). Light reportedly has a role in mobilizing nitrate from storage tissue or cell components (Beevers et al. 1965; Huffaker and Rains 1978; Jackson 1978). Light also provides for the synthesis of carbon compounds which generate the reductant for nitrate assimilation and may provide reductant directly for nitrate assimilation (Neyra and Hagemen 1974; Magalhaes et al. 1974; Schrader 1978). Nitrate reductase is activated by light (Beevers and Hageman 1969, 1972; Jordan and Huffaker 1972). Short periods of illumination are sufficient for activation (Jones and Sheard 1972, 19751, and the same kinds of effects on nitrate uptake have been observed (Jones and Sheard 1975). Since activation of nitrate reductase and stimulation of nitrate
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uptake are red/far-red reversible, phytochrome may be involved in mobilizing an inducer or in mobilizing nitrate from a storage pool to a metabolic pool (Jones and Sheard 1975; Briggs and Rice 1972). Nitrate reductase is postulated as having both retention and transport functions (Butz and Jackson 1977). Therefore, activation of nitrate reductase through the mobilization of inducers or by a general stimulation of protein synthesis would enhance nitrate uptake if the absorption and reduction systems coincided (Travis and Key 1971). d. Effects of Carbon Dioxide.-Reduction of nitrate requires the presence of carbon dioxide, as well as light and nitrate, for nitrate reductase activity is diminished in carbon dioxide-free air (Kannangara and Woolhouse 1967; Klepper et al. 1971). On the other hand, nitrate uptake has been shown to be greater in the absence of carbon dioxide than in its presence (Neyra and Hageman 1976; Huffaker and Rains 1978). The effects of carbon dioxide on nitrate uptake are greater a t high light intensities than a t low intensities (Huffaker and Rains 1978). The inhibitory effect of carbon dioxide may be due to the competition of carbon dioxide reduction with nitrate uptake for energy or reducing power generated by light or due to stomata1 closure in the presence of carbon dioxide. The latter effect results in a lessening of transpiration and water flux through the roots to the shoots.
B. Factors Affecting Acquisition of Ammonium Nitrogen by Plants Plants have evolved in soils in which nitrates are the primary form of inorganic nitrogen available for their nutrition; consequently, they have little tolerance for high levels of ammonium nitrogen in their root environment. Ammonium ions are readily absorbed by plant roots, but they must not be absorbed more rapidly than they can be utilized in the cell; otherwise, toxic reactions occur (Barker et al. 1967; Ajayi et al. 1970; Maynard and Barker 1969; Maynard et al. 1966). Theoretically, ammonium-nitrogen should be the preferred form (Reisenauer 1978). It should be used more efficiently in the plant, for it need not be reduced before incorporation into organic matter. In the soil, ammonium is less subject to leaching and to denitrification losses than is nitrate. The ammonium intake by a plant must be carefully regulated, for the tolerance range of plants to ammonium nitrogen is quite narrow and is dependent upon the presence of nitrate in the medium (Mills et al. 1976 a,b; McElhannon and Mills 1977). 1. Environmental Factors Affecting Acquisition.-a. Ammonium Concentration.-As with nitrate, the most important factor affecting the uptake of ammonium ions by plants is the ions’ concentration in the en-
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vironment of the roots (Munn and Jackson 1978); increasing the total supply of ammonium-nitrogen in a medium may increase its uptake to the point of toxicity in the plant. Toxicity of ammonium ultimately decreases root and total plant growth sufficiently so that total nitrogen intake by a plant nourished with ammonium-nitrogen may be far less than that of plants cultured of nitrate-nitrogen or when the toxic reactions are averted (Barker et al. 1966a; Barker 1967; Maynard and Barker 1969). The proportion of ammonium-nitrogen relative to nitrate in the medium is an important factor governing its acquisition and plant growth response (Mills et al. 1976a,b). Concentrations of ammonium in excess of that required to induce toxicity symptoms in plants can be maintained without adverse effects when nitrate supplies part of the nitrogen form (McElhannon and Mills 1977). If most or all of the nitrogen nutrition of a plant is supplied as ammonium, simply reducing the concentration of ammonium does not eliminate the toxicity. Plants apparently deficient in nitrogen will exhibit symptoms of ammonium toxicity when grown in dilute solutions in which all of the nitrogen is ammoniacal (Barker, unpublished data). Ammonium toxicity symptoms, lesions, and severe wilting developed with snap bean and southernpea plants within 14 days when they were cultured with all-ammonium nutrition a t deficient and sufficient N levels (McElhannon and Mills 1977).
b. pH.-With ammonium nutrition, plants absorb cations in excess of anions and the pH of the growth medium drifts downwardly (Raven and Smith 1976), while nitrate absorption causes an alkaline drift (Smiley 1974). The predominant form of nitrogen supplied to field- and container-grown plants resulted in differences in the rhizosphere pH between nitrate- and ammonium-fed plants of up to 2.2 units (Smiley 1974). Also, the pH of the rhizosphere was lower with ammonium and higher with nitrate in comparison to the bulk soil pH. In nutrient solutions or in sand culture, pH values may fall as low as 2.8 with ammonium nutrition (Maynard and Barker 1969). The decline in pH increases the toxicity of ammonium-nitrogen, for the most favorable pH for its utilization is near neutrality. Even when all of the nitrogen is ammoniacal, nearly normal growth can be obtained if the pH of the medium is buffered near neutrality (Barker et al. 1966a,b; Barker 1967; Sander and Barker 1978). It is interesting that solution pH did not appear to influence the trends of nitrate and ammonium absorption with lima beans as 100% nitrate absorption occurred with solution pH’s ranging from 3.5 to 7.5, while with ammonium, different trends in ammonium absorption occurred a t similar pH’s (McElhannon and Mills 1978). These results suggest that ammonium’s adverse effects on plant growth occur after absorption.
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c. Other Ions.-Nitrate in the presence of ammonium enhances plant growth and increases the total acquisition of nitrogen by plants (Mills et al. 1976a,b). Attempts to overcome the toxicity of ammonium-nitrogen by altering the cationic or anionic composition, with the exception of nitrate, have been unsuccessful and are in part based on the influences which ammonium nutrition has on plant composition. Calcium and magnesium contents are lowered sharply by ammonium nutrition, with these reductions being proportionately greater than those observed for potassium (Barker and Maynard 1972; Barker et al. 1966a; Harada et al. 19681, whereas phosphorus and sulfur concentrations are increased relative to those in plants grown with nitrate nutrition (Barker et al. 1966a; Blair et al. 1970). The decreases in cation uptake have been explained in various ways, ranging from cation competition for absorption sites (Blair et al. 1970) to cation-anion balances including organic and inorganic anions (Kirkby and Hughes 1970; Hiatt 1978). The mechanisms involved by increasing phosphorus and sulfur uptake are also poorly understood but have been postulated as being associated with enhanced cation (NH,') intake (Blair et al. 1970) or, to an effect, on anion uptake mechanisms (Miller 1965). In soils, fixation of K' by NH,' may occur so that potassium uptake by plants is reduced by ammonium nutrition due to the restricted availability of potassium (Barker et al. 1967; Maynard et al. 1968; Ajayi et al. 1970). d. Light and Carbohydrate Status.-Ammonium uptake by plants shows a wide diurnal variation (Van Egmond 1978). The diurnal pattern can be disturbed by providing continuous light or by supplying glucose to the nutrient medium during darkness. Ammonium and nitrate uptake are greater in light than in darkness and increase with increases in light intensity (Van Egmond 1978). The decline in ammonium uptake in darkness is apparently due to the depletion of carbohydrate reserves in roots, for the assimilation of ammonium has high energy requirements (Reisenauer 1978). Absorption and utilization of ammonium-nitrogen are affected by carbohydrate supply and plant age (Street and Sheat 1958). Plants well supplied with carbohydrates are better able to utilize ammonium-nitrogen than are energy-starved plants. Young plants with active photosynthetic mechanisms may be more tolerant than older plants which are declining in photosynthetic capacity; however, older plants with adequate carbohydrate reserves may be quite tolerant of ammonium nutrition, particularly if they have large leaf areas. Seedlings and germinating seeds are very sensitive to ammonium toxicity because of their low carbohydrate contents and inabilities to assimilate ammonium-nitrogen sufficiently rapidly to prevent its internal accumulation.
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Ketoacids, such as a-ketoglutarate, are essential for the initial complexation of ammonium absorbed by roots (McKee 1962; Hewitt 1970). Plants rich in carbohydrates are able to supply the necessary ketoacids for the assimilation of ammonium-nitrogen into amides and other amino acids. Plants which are grown on ammonium nutrition accumulate larger amounts of amides than those grown on nitrate nutrition, and the predominant amide is asparagine rather than glutamine (Barker and Bradfield 1963). Also, plants receiving ammonium-nitrogen have been shown to have higher ratios of aspartate:glutamate than those receiving nitrate-nitrogen (Barker and Bradfield 1963; Richter et al. 1975). These phenomena may be related to the metabolism of the plant being directed toward the conservation of carbon compounds by complexation of ammonium-nitrogen into 4-carbon compounds rather than into 5-carbon compounds. The tolerance of plants for external supplies or for internal accumulation of ammonium-nitrogen is low, whereas the tolerance for nitrate is high. Toxic reactions occur when ammonium nutrition is excessive, but plants will accumulate nitrate and transport it throughout the plant with few toxic effects. On the other hand, ammonium accumulation in plants cannot be tolerated, and its translocation to shoots is especially deleterious (Barker et al. 1966b; Puritch and Barker 1967). Ammonium assimilation into amides within the roots appears to be a detoxification mechanism for plants to survive on high levels of ammonium nutrition (Barker et al. 1966a,b; Maynard and Barker 1969). Proper pH control is essential for assimilation for ammonium-nitrogen into amides in the roots (Barker et al. 1966a,b; Maynard and Barker 1969). Reisenauer (1978) proposed that the ammonium status of a plant can be characterized by the ratio of carboxylates to amides. A rapid drop in carbohydrate level in roots occurs with the initiation of ammonium nutrition (Michael et al. 1970; Reisenauer 1978). Nitrate nutrition does not deplete carbohydrate levels to the same extent, for nitrates can be translocated to the shoots or into vacuoles and stored, processes which cannot occur with ammonium-nutrition without toxic effects. The assimilation of ammonium-nitrogen into amides must be rapid to avoid the toxicity. Therefore, according to Reisenauer (1978) and others (Cox and Reisenauer 1973; Kirkby and Hughes 1970), carboxylates in roots decrease, and amides increase with increases in the level of ammonium supply, producing low carboxy1ate:amide ratios. 2. Genetic Factors Affecting Acquisition of Nitrate and Ammonium Nitrogen.-Plants differ in their abilities to acquire nitrate and ammonium from a medium and in their tolerance of ammonium-nitrogen. Interspecific differences are to be expected. For example, annual range grasses, Auena, Bromus, and Lolium species, were shown to differ in
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abilities to absorb nitrate from a nutrient solution (Huffaker and Rains 1978). Corn (Zea mays L.), soybean (Glycine max Merr.), sorghum (Sorghum bicolor L.), and bromegrass (Bromus inermis L.) also have been shown to differ in capacity to absorb nitrate (Warncke and Barber 1974). Differences in root development and morphology undoubtedly affect the abilities of plants to acquire nitrogen from the soil as well as to affect the efficiency of the uptake mechanism (Huffaker and Rains 1978). Differences for nitrate acquisition within species have been observed for corn (Hoener and Deturk 1938), wheat (Triticurn dururn L.) (Brunetti et al. 1971), and barley (Hordeurn uulgare L.) (Smith 1973). Generally, cultivars with high protein contents absorbed more nitrate than those with low protein contents. Differences among species and cultivars with respect to nitrate accumulation have been documented (Barker et al. 1971, 1974; Maynard and Barker 1974; Maynard et al. 1976). These variations appear to be due to differing abilities of plants to assimilate nitrates (Olday et al. 1976a,b). Plants appear to differ widely in their abilities to reduce nitrate in their roots (Olday et al. 1976b; Pate 1973; Wallace and Pate 1965). Most cultivated plants exhibit some intolerance to ammonium nutrition (Pardo 1935). The tolerance of a plant to ammonium nutrition always should be evaluated by any investigator under prescribed conditions, for tolerance can vary with experimental conditions such as pH of the medium, presence of nitrate, activity of nitrifying organisms, and age of plants. Plants such as the Ericaceae which have evolved or are grown in acidic peaty soils are reported to have a preference for ammonium nitrogen (Cain 1952, 1954; Colgrove and Roberts 1956; Greidanus et al. 1972; Oertli 1963; Townsend 1969). These plants, however, possess the ability to assimilate nitrate (Dirr et al. 1972a) and exhibit toxic reactions to ammonium-nitrogen when grown with nutrient solutions in soil-less culture (Dirr et al. 1972b, 1973). Due to their ability to assimilate ammonium-nitrogen into amides in the roots and bulb, onions have a remarkable tolerance to ammonium nutrition (Maynard and Barker 1969). The assimilation of ammonium nitrogen into amides in onion roots and bulbs parallels that found in the roots of plants grown in a medium buffered a t a neutral pH (Barker et al. 1966a,b). Many of the favorable growth responses of plants to ammonium nutrition have been observed under conditions where the pH of the soil was alkaline (Lorenz et al. 1972, 1974).
C. Crop Responses to Form of Nitrogen 1. Nitrate Versus Ammonium Form.-a. Ammonium Toxicity.-Nitrate has been the primary source of nitrogen in the successful culture of most
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cultivated crops. However, since the work of Muntz (1893) and Maze (1900), it has been known that either nitrate or ammonium salts will serve as nitrogen sources for plant growth. Many studies on the relative merits of nitrate and ammonium nitrogen have been made, and Street and Sheat (1958) reviewed the early work in this field. Reports frequently show that severe injury to plants results from ammonium nutrition in excess of the needs of the plants, for the conditions for optimum utilization differ widely. Often the conditions for optimum utilization of ammonium were not provided (Street and Sheat 1958). On the other hand, Prianishnikov (1951) noted that if the optimum conditions for utilization of each source could be provided, nitrate and ammonium forms of nutrition would be equivalent. Toxicity from ammonium fertilizers occurs when the ammonium ion remains in the root zone in large quantities and when ammonium rather than nitrate is the dominant form of inorganic nitrogen present in acidic media (Barker et al. 1966a, 1967; Maynard and Barker 1969; Maynard et al. 1966, 1968). Conditions which lead to a predominance of ammonium-nitrogen are cool, spring soil conditions which inhibit nitrification (Alexander 1965) or when chemical nitrification inhibitors are added with heavy applications of ammoniacal fertilizers. Some workers have identified ammonia toxicity as that occurring when gaseous NH3 is released from fertilizer bands of urea or diammonium phosphates (Adams 1966; Bennett and Adams 1970; Court et al. 1964a,b).The p H of these bands exceeds 9, resulting in the release of the free ammonia (Allred and Ohlrogge 1964). The phytotoxicity of ammonia is identified as brown and necrotic roots or root tips and death of germinating seedlings near the fertilizer bands. T h e toxicity from ammonium ions, which is exhibited a t low pH, is characterized by greatly restricted root growth which is also discolored (Maynard and Barker 1969). Aerial manifestations of ammonium toxicity are chlorosis and necrosis of leaves, epinasty, and stem lesions (Maynard and Barker 1969; Maynard et al. 1966, 1968). Secondary problems such as potassium deficiency (Barker et al. 1967) and calcium deficiency (Adams 1966) often occur with ammonium nutrition of plants. Germinating seeds are also severely damaged and impaired in further growth by ammonium ions (Barker et al. 1970; Patnaik et al. 1972).
b. Nitrate Toxicity.-Plants can tolerate very high tissue levels of nitrates. Nitrate nitrogen concentrations may rise by several percentage points before phytotoxicity is apparent (Maynard and Barker 1971), whereas a few milligrams of ammonium per gram of tissue (dry weight basis) are sufficient to kill the tissue (Barker et al. 1966a,b; Maynard and Barker 1969). Excess nitrate nutrition is toxic, but the mechanism of toxicity is unknown. Whiptail of czuliflower, a manifestation of molyb-
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denum deficiency, is apparently due to the accumulations of large quantities of nitrate in the leaf margins (Candella et al. 1957). 2. Physiology of Ammonium Toxicity.-Several manifestations of ammonium toxicity have been described. Nonparasitic rots, corkiness, and other damage to roots have been associated with the accumulation of ammonium-nitrogen in fumigated or steam-sterilized soils (Uljee 1964). Similar lesions on the stems of tomato and eggplant (Hohlt et al. 1970) are symptoms of ammonium injury which occurs when potassium is insufficient in the medium (Barker et al. 1967; Barker 1978; Maynard et al. 1968). The development of these lesions occurs only when both factors, excessive ammonium and deficient potassium, are present a t once. Neither factor alone causes the lesions to form, although ammonium ions can induce potassium deficiency through potassium fixation in the clay (Barker et al. 1967). Leaf lesions also form during ammonium toxicity. These lesions appear a s darkened, water-soaked areas or as areas of collapsed tissue which becomes necrotic (Maynard and Barker 1969; Maynard et al. 1966). Marginal burning of leaves as in potassium deficiency is often evident, but supplying potassium does not alleviate the foliar symptoms entirely. T h e necrosis and loss of leaf tissue appear to be one of the most ruinous effects of ammonium toxicity. The appearance of stem lesions is more rapid than that on the leaves, and the development of stem lesions does not imply that lesions will form later on the leaves. Therefore, if plants are fertilized to the point of stem lesion initiation, a signal is given that no further nitrogen fertilization is necessary. In soils where nitrification proceeds normally, yields will not be reduced by stem lesion development a t this stage. T h e root plays a key role in the assimilation of ammonium nitrogen. Plants which complex inorganic ammonium-nitrogen into organic nitrogen in the roots have a much greater range of tolerance to ammonium nutrition than those which translocate ammonium freely to the shoots (Barker et al. 196613; Maynard and Barker 1969). The maintenance of a neutral pH in the root environment favors the detoxification of ammonium in the roots and limits its transport to the shoots. Roots, although injured by ammonium toxicity, are apparently able to tolerate ammonium nutrition as long as an abundant supply of carbohydrate is available (Reisenauer 1978). Once ammonium ions reach the shoots, the biochemistry and physiology of the plant are greatly disrupted. Ammonium ions may inhibit photosynthesis through their uncoupling of photophosphorylation (Krogmann et al. 1959). With the incidence of symptoms of ammonium toxicity in leaves, Barker et al. (1966b) correlated the breakdown of organic nitrogen compounds and the accumulation of uncombined ammonium in the leaves. They showed t h a t the majority of the ammonium-nitrogen accumulating in leaves was from
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an internal source. McElhannon and Mills (1978) found t h a t total nitrogen of the vegetative plant components of lima beans was not a n adequate indicator of the nitrogen available for pod development when ammonium supplied a significant portion of the nitrogen form. Puritch and Barker (1967) showed t h a t the chloroplasts of ammonium-toxic leaves were severely disrupted and t h a t the tissue had impaired photosynthetic capabilities. Similar studies with plants under the stresses of excessive nitrate nutrition have not been made. Ideally, ammonium-nitrogen should be the preferred source, for i t should be used more efficiently in the plant than would nitrate. However, when sufficient nitrogen is supplied to meet the goals of maximum crop production and nitrogen is supplied only in the ammonium form, the toxic reactions of the accumulation of uncomplexed ammonium override the potential increased efficiency of assimilation. Even when the optimum conditions for assimilation of ammonium-nitrogen are provided, yields may not be equivalent to those obtained with nitrate nutrition. With ammonium nutrition, much of the energy production of the plant must go into carbon skeletons for the incorporation of ammonium-nitrogen and its detoxification. This process diverts energy and carbohydrates away from growth. Thus, even when conditions are ideal for ammonium assimilation, growth may be limited relative to t h a t produced with nitrate nutrition. A balance between nitrate and ammonium nutrition normally gives the best of both regimes.
IV. LITERATURE CITED ADAMS, F. 1966. Calcium deficiency as a causal agent of ammonium phosphate injury to cotton seedlings. Soil Sci. SOC. Amer. Proc. 30~485-488. AJAYI, O., D.N. MAYNARD, and A.V. BARKER. 1970. The effect of potassium on ammonium nutrition of tomato (Lycopersicon esculentum Mill). Agron. J. 62:818-821. ALEXANDER, M. 1965. Nitrification. p. 307-343.In W.V. Bartholomew and F.E.Clark (eds.) Soil nitrogen. Agronomy Monograph 10. American Society of Agronomy, Madison. ALLISON, F.E. 1965. Evaluation of incoming and outgoing processes that affect soil nitrogen. p. 573-606. In W.V. Bartholomew and F.E. Clark (eds.) Soil nitrogen. Agronomy Monograph 10. American Society of Agronomy, Madison. ALLISON, F.E. 1966. The fate of nitrogen applied to soils. Adu. Agron. 18: 219-258. ALLISON, F.E. 1973. Soil organic matter and its role in crop production. Elsevier Scientific Publishing Co., New York. ALLRED, S.E. and A.J. OHLROGGE. 1964. Principles of nutrient uptake from fertilizer bands. VI. Germination and emergence of corn as affected by
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ammonia and ammonium phosphate. Agron. J . 56:309-313. AUNIMELECH, Y. 1971. Nitrate transformations in peat. SoilSci. 111:113119. BARKER, A.V. 1967. Growth and nitrogen distribution patterns in bean (Phaseolus vulgaris L.) plants subjected to ammonium nutrition. 11. Effects of potassium in a calcium carbonate buffered system. Adv. Front. Plant Sci. 18:7-22. BARKER, A.V. 1968. Ammonium interactions with proteins. Biochim. Biophys. Acta 168:447-455. BARKER, A.V. 1978. Using tomato plants to assess the release of potassium from fertilizers. J. Agron. Educ. 5:63-65. BARKER, A.V. and R. BRADFIELD. 1963. Effect of potassium and nitrogen on the free amino acid content of corn plants. Agron. J. 55:465-470. BARKER, A.V. and D.N. MAYNARD. 1972. Cation and nitrate accumulation in pea and cucumber as influenced by nitrogen nutrition. J. Amer. SOC. Hort. Sci. 97:27-30. BARKER, A.V., D.N. MAYNARD, and H.A. MILLS. 1974. Variations in nitrate accumulation among spinach cultivars. J. Amer. SOC. Hort. Sci. 99: 132-134. BARKER, A.V., D.N. MAYNARD, B. MIODUCHOWSKA, and A. BUCH. 1970. Ammonium and salt inhibitions of some physiological processes associated with seed germination. Physiol. Plant. 23:898-907. BARKER, A.V., N.H. PECK, and G.E. MACDONALD. 1971. Nitrate accumulation in vegetables. I. Spinach grown in upland soils. Agron. J. 63:126-129. BARKER, A.V., R.J. VOLK, and W.A. JACKSON. 1965. Effects of ammonium and nitrate nutrition on dark respiration of excised bean leaves. Crop Sci. 5:439-444. BARKER, A.V., R.J. VOLK, and W.A. JACKSON. 1966a. Growth and nitrogen distribution patterns in bean plants (Phaseolus vulgaris L.) subjected to ammonium nitrition. I. Effects of carbonates and acidity control. Soil Sci. SOC. Amer. Proc. 30:228-232. BARKER, A.V., R.J. VOLK, and W.A. JACKSON. 1966b. Root environment acidity as a regulatory factor in ammonium assimilation by the bean plant. Plant Physiol. 41:1193-1199. BARTHOLOMEW, W.V. and F.E. CLARK (eds.). 1965. Soil nitrogen. Agronomy Monograph 10. American Society of Agronomy, Madison. BAR-YOSEF, F. and U. KAFKAFI. 1972. Rates of growth and nutrient uptake in irrigated corn as affected by N and P fertilization. Soil Sci. SOC. Amer. Proc. 36:931-935. BECKENBACH, J.R. 1939. A fertility program for celery production of Everglade organic soils. Florida Agr. Expt. Sta. Bul. 333. BEEVERS, L. and R.H. HAGEMAN. 1969. Nitrate reduction in higher plants. Annu. Rev. Plant Physiol. 20:495-522. BEEVERS, L. and R.H. HAGEMAN. 1972. The role of light in nitrate me-
416
HORTICULTURAL REVIEWS
tabolism in higher plants. Photophysiology 7:85-113. BEEVERS, L., L.E. SCHRADER, D. FLESHER, and R.H. HAGEMAN. 1965. The role of light and nitrate in the induction of nitrate reductase in radish cotyledons and maize seedlings. Plant Physiol. 40:691-698. BENNETT, A.C. and F. ADAMS. 1970. Concentrations of NH3 (aq.) required for incipient toxicity to seedlings. Soil Sci. SOC. Amer. Proc. 34259-263. BINGHAM, F.T., S. DAVIS, and E. SHADE. 1971. Water relations, salt balance, and nitrate leaching losses of a 960-acre citrus watershed. Soil Sci. 112:410-418. BLACK, C.A. 1968. Soil-plant relationships. John Wiley & Sons, New York. BLAIR, G.J., M.H. MILLER, and W.A. MITCHELL. 1970. Nitrate and ammonium as sources of nitrogen for corn and their influence on the uptake of other ions. Agron. J. 62:530-532. BOLLAG, J.M. 1970. Denitrification by isolated soil bacteria under various environmental conditions. Soil Sci. Soc. Amer. Proc. 342375-879. BREMNER, J.M. 1965. Organic nitrogen in soils. p. 93-104.1~1W.V. Bartholomew and F.E. Clark (eds.) Soil nitrogen. Agronomy Monograph 10. American Society of Agronomy, Madison. BREMNER, J.M. and A.M. BLACKMER. 1978. Nitrous oxide: Emission from soils during nitrification of fertilizer nitrogen. Science 99:295-296. BREMNER, J.M. and K. SHAW. 1958. Denitrification in soil. 11. Factors affecting denitrification. J. Agr. Sci. 51:40-51. BRIGGS, W.R. and H.V. RICE. 1972. Phytochrome: Chemical and physical properties and mechanism of action. Annu. Rev. Plant. Physiol. 27:293-334. BRUNETTI, N., G. PICCIURRO, and R. BONIFORTI. 1971. Absorption of nitrate (Nitrogen-15) and nitrate reductase activity in three varieties of Triticum durum. Atti Simp. Int. Agrochim. 8238-246. (Chem. Abstr. 77:45578a) BURNS, G.R. and L.A. DEAN. 1964. Movement of water and nitrate around bands of NaN03 in soils and glass beads. Soil Sci. SOC. Amer. Proc. 28:470474. BUTZ, R.G. and W.A. JACKSON. 1977. A mechanism for nitrate transport and reduction. Phytochemistry 16:409-417. BYRNE, T.G. and O.R. LUNT. 1962. Urea formaldehyde controlled availability fertilizers. Calif. Agr. 16(3):10-11. CAIN, J.C. 1952. A comparison of ammonium and nitrate nitrogen for blueberries. Proc. Amer. SOC. Hort. Sci. 62:161-166. CAIN, J.C. 1954. Blueberry leaf chlorosis in relation to leaf pH and mineral composition. Proc. Amer. SOC. Hort. Sci. 64:61-70. CANDELLA, M.E., E.G. FISHER, and E.J. HEWITT. 1957. Molybdenum as a plant nutrient. X. Some factors affecting the activity of nitrate reductase in cauliflower leaves grown with different nitrogen sources and molybdenum levels in sand cultures. Plant Physiol. 32:280-288. COLGROVE, M.S., JR. and A.N. ROBERTS. 1956. Growth of the azalea as influenced by ammonium and nitrate nitrogen. Proc. Amer. SOC. Hort. Sci. 66:522-536.
AMMONIUM AND N I T R A T E NUTRITION
417
COURT, M.N., R.C. STEPHEN, and J.S. WAID. 1964a. Toxicity as a cause of the inefficiency of urea as a fertilizer. I. Review. J. Soil Sci. 15:42-48. COURT, M.N., R.C. STEPHEN, and J.S. WAID. 1964b. Toxicity as a cause of the inefficiency of urea as a fertilizer. 11.Experimental. J. Soil Sci. 15:49-65. COX, W.J. and H.M. REISENAUER. 1973. Growth and ion uptake by wheat supplied with nitrogen as nitrate, or ammonium, or both. Plant & Soil 38: 363-380. CRIBBS, W.H. and H.A. MILLS. 1979. Influence of nitrapyrin on the evolution of N20 from an organic medium with and without plants. Commun. Soil Sci. Plant Anal. 10:785-794. DIRR, M.A., A.V. BARKER, and D.N. MAYNARD. 1972a. Extraction of nitrate reductase from leaves of Ericaceae. Phytochemistry 12:1261-1264. DIRR, M.A., A.V. BARKER, and D.N. MAYNARD. 1972b. Nitrate reduction activity in the leaves of the highbush blueberry and other plants. J.Amer. Soc. Hort. Sci. 97:329-331. DIRR, M.A., A.V. BARKER, and D.N. MAYNARD. 1973. Growth and development of leucothoe and rhododendron under different nitrogen and pH regimes. HortScience 8:131- 132. DUPLESSIS, M.C.F. and W. KROONTJE. 1964. The relationship between pH and ammonia equilibria in soils. Soil Sci. SOC. Amer. Proc. 28:751-754. ELZAM, O.E. and E. EPSTEIN. 1965. Absorption of chloride by barley roots: Kinetics and selectivity. Plant Physiol. 40:620-624. ELZAM, O.E. and T.K. HODGES. 1967. Calcium inhibition of potassium absorption in corn roots. Plant Physiol. 42:1483-1488. EPSTEIN, E. 1972. Mineral nutrition of plants: Principles and perspectives. Academic Press, New York. ERNST, J.W. and H.F. MASSEY. 1960. The effects of several factors on volatilization of ammonia formed from urea in the soil. Soil Sci. SOC. Amer. Proc. 2497-90. EZETA, F.W. and W.A. JACKSON. 1975. Nitrate translocation by detopped corn seedlings. Plant Physiol. 56:148-156. GARDNER, W.R. 1965. Movement of nitrogen in the soil. p. 550-572. I n W.V. Bartholomew and F.E. Clark (eds.) Soil nitrogen. Agronomy Monograph 10. American Society of Agronomy, Madison. GOH, K.M. and R.J. HAYNES. 1977. Evaluation of potting media for commercial nursery production of container grown plants. New Zealand J. Agr. Res. 20:383-393. GOLDSMITH, J., J.P. LIVONI, C.L. NORBERG, and I.H. SEGEL. 1973. Regulation of nitrate uptake in Penicillium chrysogenum by ammonium ion. Plant Physiol. 52:362-367. GORING, C.A.I. 1962. Control of nitrification of ammonium fertilizers and urea by 2-chloro-6-(trichloromethyl) pyridine. Soil Sci. 93:431-443. GREIDANUS, T., L.A. PETERSON, L.E. SCHRADER, and M.N. DANA. 1972. Essentiality of ammonium for cranberry nutrition. J . Amer. Soc. Hort. Sci. 97:272-277.
418
HORTICULTURAL REVIEWS
GUTHRIE, T.F. and J.M. DUXBURY. 1978. Nitrogen mineralization and denitrification on organic soils. Soil Sci. SOC. Amer. Proc. 42:908. HARADA, T., H. TAKAKI, and Y. YAMUDA. 1968. Effect of nitrogen sources on the chemical components in young plants. Soil Sci. Plant Nutr. 14:47-55. HAUCK, R.D. and S.W. MELSTED. 1956. Some aspects of the problem of evaluating denitrification in soils. Soil Sci. SOC. Amer. Proc. 20:361-364. HEIMER, Y.M. 1975. Nitrite induced development of the nitrate uptake system in plant cells. Plant Sci. Lett. 4:137-139. HEIMER, Y.M. and P. FILNER. 1971. Regulations of nitrate assimilation pathway in cultured tobacco cells. 111. The nitrate uptake system. Biochim. Biophys. Acta 230:362-372. HEIMER, Y.M., J.L. WRAY, and P. FILNER. 1969. The effect of tungstate on nitrate assimilation in higher plants. Plant Physiol. 44:1197-1199. HEWITT, E.J. 1970. Physiological and biochemical factors controlling the assimilation of inorganic nitrogen supplies by plants. p. 78-103. In E.A. Kirkby (ed.) Nitrogen nutrition of the plant. Univ. of Leeds, Leeds, England, U.K. HIATT, A.J. 1978. Critique of “Absorption and utilization of ammonium nitrogen by plants.” p. 191-199. I n D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York. HODGES, T.K. 1973. Ion absorption by plant roots. Aduan. Agron. 25:163207. HOENER, I.R. and E.E. DETURK. 1938. The absorption and utilization of nitrate nitrogen during vegetative growth by Illinois high protein and Illinois low protein corn. J. Amer. SOC. Agron. 30:232-243. HOHLT, H.E., D.N. MAYNARD, and A.V. BARKER. 1970. Studies on the ammonium tolerance of some cultivated Solanaceae. J. Amer. SOC. Hort. Sci. 95:345-348. HUFFAKER, R.C. and D.W. RAINS. 1978. Factors influencing nitrate acquisition by plant; assimilation and fate of reduced nitrogen. p. 1-43. I n D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York. INGESTAD, T. 1972. Mineral nutrient requirements of cucumber seedlings. Plant Physiol. 5 2 :33 2-338. JACKSON, W.A. 1978. Nitrate acquisition and assimilation by higher plants: Processes in the root system. p. 45-88. In D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York. JACKSON, W.A., D. FLESHER, and R.H. HAGEMAN. 1973. Nitrate uptake by dark-grown corn seedlings. Plant Physiol. 51:120-127. JACKSON, W.A., R.J. VOLK, and T.C. TUCKER. 1972. Apparent induction of nitrate uptake in nitrate-depleted plants. Agron. J. 64:518-521. JONES, R.W. and R.W. SHEARD. 1972. Nitrate reductase activity: Phytochrome mediation of induction in etiolated peas. Nature New Biol. 238:221222. JONES, R.W. and R.W. SHEARD. 1975. Phytochrome nitrate movement, and induction of nitrate reductase in etiolated pea terminal buds. Plant Physiol.
AMMONIUM AND N I T R A T E NUTRITION
419
55:954-959. JORDAN, W.R. and R.C. HUFFAKER. 1972. Influence of age and light on the distribution and development of nitrate reductase in greening barley leaves. Physiol. Plant. 26:296-301. KAFKAFI, A.I., I. WALERSTEIN, and S. FEIGHNBAUM. 1971. Effect of potassium nitrate and ammonium nitrate on the growth and cation uptake and water requirements of tomato grown in sand culture. Israel J. Agr. Res. 21:13-20. KANNANGARA, C.G. and H.W. WOOLHOUSE. 1967. The role of carbon dioxide, light, and nitrate in the synthesis and degradation of nitrate reductase in leaves by Perilla frutescens. New Phytol. 66:553-561. KEENEY, D.R. and L.M. WALSH. 1972. Available nitrogen in rural ecosystems. Sources and fate. HortScience 7:219-223. KIRKBY, D.W. and E. MENGEL. 1967. Ionic balance in different tissues of the tomato plant in relation to nitrate, urea, or ammonium nutrition. Plant Physiol. 42:6- 14. KIRKBY, E.A. (ed.) 1970. Nitrogen nutrition of the plant. Univ. of Leeds, Leeds, England, U.K. KIRKBY, E.A. and D.A. HUGHES. 1970. Some aspects of ammonium and nitrate nutrition in plant metabolism. p. 69-77. I n E.A. Kirkby (ed.) Nitrogen nutrition of the plant. Univ. of Leeds, Leeds, England, U.K. KLEPPER, L., D. FLESHER, and R.H. HAGEMAN. 1971. Generation of reduced nicotinamide adenine dinucleotide for nitrate reduction in green leaves. Plant Physiol. 48:580-590. KOSTER, A.L. 1963. Changes in metabolism of isolated root systems of soybean (Glycine m a d . Nature 198:709-710. KROGMANN, D.W., A.T. JAGENDORF, and M. AVRON. 1959. Uncouplers of spinach chloroplast photosynthetic phosphorylation. Plant Physiol. 34: 272-277. LORENZ, O.A., B.L. WEIR, and J.C. BISHOP. 1972. Effect of controlledrelease nitrogen fertilizers on yield and nitrogen absorption by potatoes, cantaloupes, and tomatoes. J.Amer. SOC.Hort. Sci. 97:334-337. LORENZ, O.A., B.L. WEIR, and J.C. BISHOP. 1974. Effects of sources of nitrogen on yield and nitrogen absorption of potatoes. Amer. Potato J. 51: 56-65. LYCKLAMA, J.C. 1963. The absorption of ammonium and nitrate by perennial rye-grass. Acta Bot. Neerl. 12:316-423. MAGALHAES, A.C., C.A. NEYRA, and R.H. HAGEMAN. 1974. Nitrate assimilation and amino nitrogen synthesis in isolated spinach chloroplasts. Plant Physiol. 53:411-415. MAHENDRAPPA, M.K. and R.L. SMITH. 1966. Some effects of moisture on denitrification in acidic and alkaline soils. Soil Sci. Soc. Amer. Proc. 31:212215. MAYNARD, D.N. 1978. Critique of “Potential nitrate levels in edible plant parts.” p. 221-233. I n D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York.
420
HORTICULTURAL REVIEWS
MAYNARD, D.N. and A.V. BARKER. 1969. Studies on the tolerance of plants to ammonium nutrition. J. Amer. Soc. Hort. Sci. 94:235-239. MAYNARD, D.N. and A.V. BARKER. 1971. Critical nitrate levels for leaf lettuce, radish, and spinach plants. Commun. Soil Sci. Plant Anal. 2:461470. MAYNARD, D.N. and A.V. BARKER. 1974. Nitrate accumulation in spinach as influenced by leaf type. J. Amer. Soc. Hort. Sci. 99:135-138. MAYNARD, D.N., A.V. BARKER, and W.H. LACHMAN. 1966. Ammoniuminduced stem and leaf lesions of tomato plants. Proc. Amer. SOC. Hort. Sci. 88:516-520. MAYNARD, D.N., A.V. BARKER, and W.H. LACHMAN. 1968. Influence of potassium on the utilization of ammonium by tomato plants. Proc. Amer. SOC. Hort. Sci. 92:537-542. MAYNARD, D.N., A.V. BARKER, P.L. MINOTTI, and N.H. PECK. 1976. Nitrate accumulation in vegetables. Adu. Agron. 28:71-118. MAZE, P. 1900. Recherches sur l’influence de l’azote ammonical sur development du mais. Ann. l’lnstitute Pasteur 14:26-41. MCCOLM, R.E. and C.H. MILLER. 1971. Yield, nutrient uptake and nutrient removal by pickling cucumbers. J. Amer. SOC. Hort. Sci. 96:42-45. MCELHANNON, W.S. and H.A. MILLS. 1977. The influence of N concentration and N03/NH4 ratio on the growth of lima and snap beans and southern pea seedlings. Commun. Soil Sci. Plant Anal. 8:677-687. MCELHANNON, W.S. and H.A. MILLS. 1978. Influence of percent NOa/ NH,’ on growth, N absorption, and assimilation by lima beans in solution culture. Agron. J. 70:1027-1032. MCGARITY, J.W. and J.A. RAJARATNAM. 1973. Apparatus for the measurement of losses of nitrogen as gas from the field in simulated field environments. Soil Biol. Biochem. 5:121-131. MCKEE, H.S. 1962. Nitrogen metabolism in plants. Clarendon Press, Oxford. MICHAEL, G., P. MARTIN, and I. OWISSIA. 1970. Uptake of ammonium and nitrate-N from labelled ammonium nitrate in relation to carbohydrate supply of the roots. p. 22-29. In E.A. Kirkby (ed.) Nitrogen nutrition of plant. Univ. of Leeds, Leeds, England, U.K. MILLER, M.H. 1965. Influence of (NH,),SO, on root growth and P absorption by corn from a fertilizer band. Agron. J . 57:393-396. MILLS, H.A., A.V. BARKER, and D.N. MAYNARD. 1974. Ammonia volatilization from soils. Agron. J. 66:355-358. MILLS, H.A., A.V. BARKER, and D.N. MAYNARD. 1976a. Nitrate accumulation in radish as affected by nitrapyrin. Agron. J. 68:13-17. MILLS, H.A., A.V. BARKER, and D.N. MAYNARD. 1976b. Effects of nitraHort. Sci. 101:202pyrin on nitrate accumulation in spinach. J. Amer. SOC. 204. MILLS, H.A. and F.A. POKORNY. 1978. The influence of nitrapyrin on N retention and tomato growth in sand-bark media. J . Amer. SOC. Hort. Sci. 103:662-664.
AMMONIUM AND NITRATE NUTRITION
421
MINOTTI, P.L. and W.A. JACKSON. 1970. Nitrate reduction in the roots and shoot of wheat seedlings. Planta 95:36-44. MINOTTI, P.L., D.C. WILLIAMS, and W.A. JACKSON. 1968. Nitrate uptake and reduction as affected by calcium and potassium. Soil Sci. SOC. Amer. Proc. 32:692-698. MINOTTI, P.L., D.C. WILLIAMS, and W.A. JACKSON. 1969a. Nitrate uptake in wheat as influenced by ammonium and other cations. Crop Sci.9:9-14. MINOTTI, P.L., D.C. WILLIAMS, and W.A. JACKSON. 1969b. The influence of ammonium on nitrate reduction in wheat seedlings. Planta 86:267271. MULDER, E.G., T.A. LIE, and J.W. WOLDENDORP. 1969. Biology and soil fertility. p. 163-201. In Soil biology. UNESCO Pub. 741. MUNN, D.A. and W.A. JACKSON. 1978. Nitrate and ammonium uptake by rooted cuttings of sweet potato. Agron. J. 70:312-316. MUNTZ, A. 1893. Recherches experimentales sur la culture et l’explortation des vignes. Ann. Agron. 2:l-167. NEGRA, C.A. and R.H. HAGEMAN. 1975. Nitrate uptake and induction of nitrate reductase in excised corn roots. Plant Physiol. 56:692-695. NEGRA, C.A. and R.H. HAGEMAN. 1976. Relationships between carbon dioxide, malate, and nitrate accumulation and reduction in corn (Zea mays L.) seedlings. Plant Physiol. 58:726-730. NELSON, D.W. and S.M. BREMNER. 1969. Gaseous products of nitrite decomposition in soils. Soil Biol. Biochem. 2:203-215. NELSON, L.B. 1968. Changing patterns in fertilizer use. Soil Sci. SOC.Amer., Madison, Wisc. NEYRA, C.A. and R.H. HAGEMAN. 1974. Dependence of nitrite reduction on electron transport in chloroplasts. Plant Physiol. 54:480-483. NIELSEN, D.R. and J.G. MACDONALD (eds.). 1978a. Nitrogen in the environment: nitrogen behavior in field soils. Academic Press, New York. NIELSEN, D.R. and J.G. MACDONALD (eds.). 1978b. Nitrogen in the environment: soil-plant-nitrogen relationships. Academic Press, New York. NISSEN, P. 1974. Uptake mechanisms: inorganic and organic. Annu. Reu. Plant Physiol. 25:53-79. NOMMIK, H. 1956. Investigations on denitrification in soil. Acta Agr. Scand. 6:195-228. OERTLI, J.J. 1963. Effect of form of nitrogen on pH on growth of blueberry plants. Agron. J . 55:305-306. OLDAY, F.C., A.V. BARKER, and D.N. MAYNARD. 1976a. A physiological basis for different patterns of nitrate accumulation in two spinach cultivars. J. Amer. SOC. Hort. Sci. 101:217-219. OLDAY, F.C., A.V. BARKER, and D.N. MAYNARD. 1976b. A physiological basis for different patterns of nitrate accumulation in cucumber and pea. J. Amer. SOC. Hort. Sci. 101:219-221. PARDO, J.H. 1935. Ammonium in the nutrition of higher green plants. Q. Reu. Biol. 101:l-31.
422
HORTICULTURAL REVIEWS
PARR, J.F. 1973. Chemical and biochemical considerations for maximizing the efficiency of fertilizer nitrogen. J. Enuiron. Quality 2:75-84. PARR, J.F. and R.I. PAPENDICK. 1966. Greenhouse evaluation of the agronomic efficiency of anhydrous ammonia. Agron. J. 58:215-219. PATE, J.S. 1973. Uptake, assimilation, and transport of nitrogen compounds by plants. Soil Biol. Biochem. 5:109-119. PATNAIK, R., A.V. BARKER, and D.N. MAYNARD. 1972. Effects of ammonium and potassium ions on some physiological and biochemical processes of excised cucumber cotyledons. Physiol. Plant. 27:32-36. PILOT, L. and W.H. PATRICK. 1972. Nitrate reduction in soils: Effect of moisture tension. Soil Sci. 114:312-316. POLIZOTTO, K.R., G.E. WILCOX, and C.H. JONES. 1975. Response of growth and mineral composition of potato to nitrate and ammonium nitrogen. J. Amer. SOC. Hort. Sci. 100:165-168. PRIANISHNIKOV, D.N. 1951. Nitrogen in the life of plants (Transl. by S.A. Wilde). Kramer Business Service, Madison, Wisc. PURITCH, G.S. and A.V. BARKER. 1967. Structure and function of tomato leaf chloroplasts during ammonium toxicity. Plant Physiol. 42:1229-1238. RAO, K.P. and D.W. RAINS. 1976a. Nitrate absorption by barley. I. Kinetics and energetics. Plant Physiol. 5755-58. RAO, K.P. and D.W. RAINS. 1976b. Nitrate absorption by barley. 11. Influence of nitrate reductase activity. Plant Physiol. 5759-62. RAVEN, J.A. and F.A. SMITH. 1976. Nitrogen assimilation and transport in vascular land plants in relation to intracellular p H regulation. New Phytol. 76:415-431. REISENAUER, H.M. 1978. Absorption and utilization of ammonium nitrogen by plants. p. 157-189. In D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York. RITCHTER, R., W. DIJKSHOORN, and C.R. VONK. 1975. Amino acids of barley plants in relation to nitrate, urea, or ammonium nutrition. Plant Soil 42:601-618. ROY, R.N. and R.C. WRIGHT. 1974. Soybean growth and nutrient uptake in relation to soil fertility. Agron. J. 66:5-8. SANDER, D.J. and A.V. BARKER. 1978. Comparative toxicity of nitrapyrin and 6-chloropicolinic acid to radish and cucumber under different N nutrition regimes. Agron. J. 70:295-298. SASSEVILLE, D.N. and H.A. MILLS. 1979a. N form and concentration: Effects on N absorption, growth, and total N accumulation with southern peas. J Amer. SOC. Hort. Sci. 104:586-591. SASSEVILLE, D.N. and H.A. MILLS. 1979b. N form and concentration: Effects on reproductive development, growth and N content of southern peas. J . Plant Nutr. 1:241-254. SAYER, J.D. 1948. Mineral accumulation in corn. Plant Physiol. 23:267-281. SCHRADER, L.E. 1978. Uptake, accumulation, assimilation, and transport of nitrogen in higher plants. p. 101-141. In D.R. Nielsen and J.G. MacDonald (eds.). Nitrogen in the environment, Vol. 2. Academic Press, New York.
AMMONIUM AND NITRATE NUTRITION
423
SKOROPANOU, S.G. 1968. Reclamation and cultivation of peat-bog soils. U S . Dept. Commerce, Springfield, Va. SMILEY, R.W. 1974. Rhizosphere pH as influenced by plant, soil, and nitrogen fertilizers. Soil Sci. SOC. Amer. Proc. 38:795-799. SMITH, F.A. 1973. The internal control of nitrate uptake into excised barley roots with differing salt contents. New Phytol. 72:769-782. SPARKS, D. and D.H. BAKER. 1975. Growth and nutrient response of pecan seedlings, Carya illinoensis Koch, to nitrate levels in sand culture. J. Amer. SOC. Hort. Sci. 100:392-399. STANFORD, G., C.B. ENGLAND, and A.W. TAYLOR. 1969. Fertilizer use and water quality. USDA/ARS 41-168. STEEN, W.C. and B.J. STOJANOVIC. 1971. Nitric oxide volatilization from a calcareous soil and model aqueous solutions. Soil Sci. SOC. Amer. Proc. 35: 277-282. STEWART, B.A., F.G. VIETS, and G.L. HUTCHINSON. 1968. Agriculture’s effect on nitrate pollution of ground water. J. Soil Water Conserv. 23:13-15. STREET, H.E. and D.E.G. SHEAT. 1958. The absorption and availability of nitrate and ammonia. p. 150-166. In W. Ruhland (ed.) Encyclopedia of plant physiology, Vol. VIII. Springer-Verlag, Berlin. TERMAN, G.L. and J.C. NOGGLE. 1973. Nutrient concentration changes in corn as affected by dry matter accumulation with age and response to applied nutrients. Agron. J. 65:941-945. TOWNSEND, L.R. 1969. Influence of form of nitrogen and pH on growth and nutrient levels in leaves and roots of the lowbush blueberry. Can. J . Plant Sci. 49:333-338. TRAVIS, R.L. and J.L. KEY. 1971. Correlation between polyribosome level and the ability to induce nitrate reductase in dark-grown corn seedlings. Plant Physiol. 48:617-620. ULJEE, A.H. 1964. Ammonium nitrogen accumulation and root injury to tomato plants. New Zealand J. Agr. Res. 7:343-356. VAN EGMOND, F. 1978. Nitrogen nutritional aspects of the ionic balance of plants. p. 171-189. In D.R. Nielsen and J.G. MacDonald (eds.) Nitrogen in the environment, Vol. 2. Academic Press, New York. WALLACE, W. and J.S. PATE. 1965. Nitrate reductase in the field pea (Pisum aruense L.). Ann. Bot. 29:655-671. WARD, P.C. 1970. Existing levels of nitrate in waters-The California situation. p. 14-26. I n V. Snoeyink and V. Griffin (eds.) Nitrate and water supply: source and control. 12th Sanitary Eng. Conf. Proc., College of Eng., Univ. of Illinois, Urbana-Champaign. Engineering Publishing Office, University of Illinois, Urbana. WARNCKE, D.D. and S.A. BARBER. 1974. Nitrate uptake effectiveness of four plant species. J. Environ. Qual. 3:28-30. WOLDENDORP, J.W. 1962. The quantitative influence of the rhizosphere on denitrification. Plant Soil 17:267-270. WRIGHT, M.J. and K.L. DAVIDSON. 1964. Nitrate accumulation in crops and nitrate poisoning in animals. Adv. Agron. 16:197-247.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
9 The Distribution and Effectiveness of the Roots of Tree Crops David Atkinson Department of Pomology, East Malling Research Station, Maidstone, Kent, U.K.
I. Introduction 425 11. Methods Used to Investigate Tree Root Systems 426 A. Excavation 426 B. Sampling 427 C. Observation 429 D. RootActivity 430 E. Indirect 433 111. The Development of Individual Roots 434 434 A. Growth and Changes with Age B. Root Soil Contact 435 C. Secondary Thickening 437 D. The Functions of Different Root Types 437 E. The Longevity of Roots in the Soil 439 IV. The Seasonal Periodicity of Root Growth 445 A. Variations Among Species 446 448 B. Effects of Pruning and the Vigor of Shoot Growth C. Effects of Cropping 449 D. OtherFactors 449 V. The Distribution of the Roots of Tree Crops 453 A. Apple 453 B. Pear 456 C. PrunusSpecies 456 D. Other Tree Crops 457 E. Conclusions 457 VI. Root Density in Tree Crops 457 458 VII. Root Activity and Effectiveness in Relation to Distribution VIII. The Effect of Environmental and Management Factors on the Distribu462 tion and Efficiency of Tree Roots 424
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
IX.
X. XI. XII.
A. SoilType 462 B. Fertilizers 463 C. Irrigation 464 D. Soil Management 465 E. Planting Density and Orchard Systems 469 The Influence of Rootstock and Scion Genotype on the Root System A. Rootstock Effects 471 B. Scion Cultivar Effects 472 Root-Shoot Interactions 472 Conclusions 474 Literaturecited 475
425
471
1. INTRODUCTION
The aerial parts of crops are easily visible and are surrounded by a medium which allows for both simple and complex measurements of growth and activity to be made. In contrast, the root system of a plant is encased in a medium which precludes easy examination of even the simplest growth parameters, and so the available information on the functioning of root systems does not parallel that on shoots. Much of the information available on root function derives from solution culture studies in the laboratory and requires considerable qualification before it can be applied to whole systems growing in the variable environment found under field conditions. Despite these difficulties, the realization of the impact of root performance on shoot growth and crop production has led to a recent surge of interest and the publication of a number of texts which discuss or review the plant root system, e.g., Carson (19741, Clarkson (1974), Torrey and Clarkson (1975), Russell (1977), Nye and Tinker (1978), and Harley and Russell (1979). The emphasis in most of these texts, however, is on the roots of cereals and other annual plants; little attention is given to the unique features of perennial root systems or to the physiology of other than primary roots. Studies on the roots of tree crops have been reviewed only infrequently, although Rogers (1939a) listed 118 and Kolesnikov (1971) about 300 relevant publications in their reviews of this subject. In addition, parts of the subject have been treated by Rogers (1952), Rogers and Booth (1959), Rogers and Head (1966), and Head (1973), and reviews dealing with the root system of trees as a whole, with emphasis on forest trees, have been published by Lyr and Hoffmann (1967) and Bilan (1971). T h e root systems of conifers have also been reviewed (Sutton 1969). In view of the material already available, this review concentrates on papers published in the last 15 years, with reference to some earlier papers where necessary for balance and completeness of treatment.
426
HORTICULTURAL REVIEWS
11. METHODS USED TO INVESTIGATE TREE ROOT SYSTEMS
Information obtained is a function of the techniques available, and its applicability is influenced by the means of data collection. A wide range of methods for the investigation of plant root systems has been reviewed by Bohm (19791, but with major emphasis on field crops. The techniques used in studies of tree crops can be divided as follows: 1. 2. 3. 4. 5.
Whole tree excavation techniques. Sampling methods. Observation techniques. Measurements of root activity. Indirect methods.
A. Excavation
Despite the size of many tree root systems and the weight of soil which needs to be removed to expose the roots (commonly 60 Mg (megagrams or tonnes), and for a tree planted a t 10 m X 10 m with roots to 2 m depth 300 Mg), a large number of these excavations have been performed. In one paper alone Rogers (1935) described the excavation of 177 tree root systems. One of the best descriptions, of perhaps the most frequently used excavation method, is given by Rogers and Vyvyan (1934). In summary, a trench is dug beyond the root area and soil is removed in sections of 50 cm across the ground occupied by the root system until the excavation is complete. T h e soil is gently removed in small pieces from the side of the vertical soil face and the position of each root marked upon a plan which enables the root system to be reconstructed. Following excavation, roots either can be left intact (skeleton method) or cut off within 125 liter units to allow for the recording of root weight, length, etc., within specific soil areas, before, in some cases, reassembly of the root system. The advantages and disadvantages of this method have been discussed by Bohm (1979). Excavation is the only method which gives a clear picture of the entire root system of a plant as it grows in the field. T h e length, weight, volume, surface area, shape, color, 3-dimensional distribution, and other characteristics of both the individual roots and the root system as a whole can be recorded. Because of the small number of really large roots in a root system, this is the only accurate way of estimating the weight of a root system or the distribution of major (> 5 mm diameter) roots. This method also allows for studies of the interrelationships of competing root systems (i.e., Coker 1959; Atkinson et al. 1976) and for studies of the relationships between soil condition, soil cracks, worm holes, etc., and root growth (i.e., Rogers and Vyvyan 1934;
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
427
Atkinson 1973a). However, it requires a large amount of labor, which often can be prohibitively expensive, and can irreparably disturb the soil and so increase variability in a field to be used for other experiments. In addition, there is usually a limitation to the number of specimens which can be removed so the population is seldom sampled adequately. Another serious limitation is the relatively high potential losses of fine roots during the field extraction. Dudney (1972) estimated that 22 to 37% of root weight remained in the soil after a partial excavation. The weight remaining normally would be much less than this with a full excavation.
B. Sampling These include monolith, auger and core sampling, profile wall, partial excavation, and other methods where only a portion of the soil volume is examined to estimate the performance of the root system as a whole. Little use has been made of monolith methods (including needle boards, box samples, etc.) in studies of trees, perhaps because the detailed visual presentation of only part of the root system is of limited value. The use of auger and core sampling methods has been discussed by Weller (1971) who counted the numbers of root tips in 10 replicate 4.0 cm diameter samples. He showed large variations among replicate samples. For example, under a 35-year-old tree of ‘Boskoop’ apple on seedling stock growing in a soil with intermittent waterlogging, the mean number of tips a t 30 to 40 cm depth (the horizon with the highest density of tips) was 203 and the range was 4 to 463. This range paralleled those for the mean numbers of root tips present a t 10 cm intervals from 0 to 150 cm depth, 2 to 203. However, despite this variability, the average patterns of root distribution appeared to be related closely to both soil condition and applied treatments. In a study involving core sampling around 26-yearold apple trees of ‘Fortune’/M 9 (Atkinson 1974a), 100 core samples taken from close to the trunk of a small number of trees gave a standard error of 10% of the mean for roots -= 1 mm in diameter. When a similar number of samples was taken (1) from a larger number of apparently similar trees, (2) a t a greater distance from the trunk, or (3) of roots of a greater diameter, the variation rose sharply so that differences reaching statistical significance were rare. Similarly, in a study of Douglas fir (Pseudotsuga taxifolia (Poir) Britt), Reynolds (1970) found that the “percent standard error” for root weight, estimated from 10 replicate core samples, averaged 30% and ranged up to 95%. Thus, he was unable to detect significant differences among different horizontal zones or depths. However, Roberts (1976) for Pinus sylvestris L. and Ford and Deans (1977) for Picea sitchensis (Bong.) Carr. found lower variability and were able to confirm significant differences in root density with
428
HORTICULTURAL REVIEWS
depth and horizontal position. In these latter studies, the estimated mean root densities, LA (cm/cm’ soil surface), were 126 and 68, respectively, and, therefore, much higher than that of 7 found by Atkinson and Wilson (1980) for mature trees of ‘Fortune’ apple/M 9. This lower value of LA may have influenced the higher apparent variability. Statistical analysis of core sampling results has been discussed by Persson (1978). Despite these problems, core sampling has been used frequently in studies of fruit and other trees and can allow relatively rapid comparisons of positions and treatments without the disturbance caused by total excavation. Profile wall methods also have been used by a number of investigators, e.g., Oskamp and Batjer (1932) and Atkinson and White (1980). With this method a soil profile is exposed either mechanically or by hand, and then a further layer of soil is carefully removed to expose any roots present a t the surface of the profile. Roots present are recorded with the aid of a grid and a diagram of distribution produced, with each root identified by a dot. This method has been discussed in detail by Bohm (1979). In applying the method to fruit and other trees, the siting of the trench is critical. Root distribution differs between row and interrow areas (Atkinson and White 1980) and with distance from the trunk (Gurung 1979).T h e siting of the trench will thus influence the density of roots recorded, and, if the treatments to be compared have affected horizontal distribution, will interact with assessed treatment effects. To counteract some of these problems, Huguet (1973) suggested using a logarithmic spiral trench, rather than a simple straight trench. T h e modification is based on the hypothesis that under homogeneous conditions the tree root system is a “radient” system with the plantation line as a symmetrical axis. In view of this, a logarithmic spiral will provide the most information, as it samples all parts of the tree area and different areas in proportion to the volume of soil present a t distances from the trunk. Data obtained from both this type of trench and from a straight trench have been compared by Gurung (1979). H e found no significant difference in the mean density of roots detected by the 2 methods, although the overall variability among replicate trees was such that only very large differences (> 60%) would have been detected. Variability among replicates was, however, higher for data obtained from straight trenches. Partly as a result of this, the spiral trench method was better a t detecting significant differences among applied treatments. Partial excavations have been used as means of sampling by some workers. Coker (1958) excavated quarter sections of the root volume, rather than all of it. Rogers and Vyvyan (1934) and Atkinson (1973a) showed that the major roots of some trees are unevenly distributed. In
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
429
extreme cases most of the root system can be found in half of the soil volume; thus, the excavation of only one segment can give misleading results unless replication is good. Dudney (1972) used a partial excavation technique which involved removing the soil from an area a t the base of a tree within a circle of approximately 1.5 m diameter and a depth of about 30 cm. Following this the root system was strained with a tractormounted jack to expose major roots, and those attached to them unearthed by hand to a depth of about 50 cm. Atkinson et al. (1976) showed that this type of method couId recover about half of the weight of roots obtained by a conventional excavation and could give good relative data. The proportion recovered clearly will be influenced by the root distribution with depth, the soil type (which will influence the ease with which roots free themselves from the soil), and root strength (which will influence the length of root pulled from the soil). Thus, method may interact with treatments. With all of these methods variability within the volume of the root system provides a major problem with respect to easy sampling. With sparse root systems like apple (Atkinson and Wilson 1980) the number of cores found without roots and the non-normal distribution usually obtained also complicate the statistical treatment of results.
C. Observation Total excavation does not allow the growth and development of the root system to be followed easily, although this has been done by frequent core sampling (Weller 1971; Roberts 1976; Ford and Deans 1977). T h e development of the root system and the periodicity of its growth are probably most easily followed using observation windows in the soil. T h e disadvantages of this type of method were listed by Rogers (1934) as: (1) only a small sample of the roots of the plant is seen, although this can be compensated for by replication; (2) the installation of a window against an established tree causes the cutting of some large roots which may induce abnormal patterns of growth; (3) the observed roots are growing against a sheet of glass which may modify water, mineral, and air movement; and (4) the roots are exposed to light during recording. However, the method does allow a series of direct and detailed measurements to be made on the same roots or the same part of the root system over a period of time. In addition, photographic methods such as time-lapse cinematography may be used. T h e measurements obtained can be used for correlation studies with environmental variables in the same way as is done for shoot growth. While early investigations with this type of method were in chambers
430
HORTICULTURAL REVIEWS
dug in the field, usually against established trees, some later studies involved trees planted adjacent to a permanent installation (Rogers 1969). This negates the abnormal effects of a severe root pruning of one face of the root system and allows environmental variables to be related to growth and development more conveniently. Measurements obtained with this technique on fruit trees compare favorably with those obtained by other methods, e.g., tracer uptake (Atkinson 1974b), excavation (Atkinson 1978), or water depletion (Atkinson 1978). Roberts (1976) compared the use of core sampling methods and observation trenches in recording the seasonal periodicity of root growth in Pinus syluestris and found that the peak number of root tips seen against the windows of his observation pit occurred two to three months later than peak numbers in the core samples. In addition, the yearly trends were not the same with the two methods. These differences are difficult to explain, but could be due to a number of causes. They emphasize the need for care in interpreting any information on root activity. Two of the principal disadvantages of using permanent root observation laboratories are that trees have to be brought to the root facility (i.e., they cannot be used to investigate problems in the orchard) and that only limited replication is possible. Both of these disadvantages can be overcome by the use of observation tubes as suggested by Waddington (1971) and developed for use in the orchard by Gurung (1979). This method, called the mini-rhizotron method by Bohm (1974), involves the installation of transparent tubes in the orchard soil. Root growth a t the soil tube interface is then observed with either a ‘fibrescope’ (Waddington 1974), a lens and mirror (Bohm 1974), or an industrial tank viewing endoscope (Gurung 1979). Results obtained with this method were correlated significantly with those obtainable in a root laboratory (Gurung 1979). The principal disadvantage of the method seems to be the variation in the length of root visible against the tube, necessitating the use of large numbers of tubes.
D. Root Activity T h e determination of root activity or potential for activity is the most frequent objective of root studies. T h e absence of activity a t any given time or place can be due to either an absence of roots or to conditions which prevent their functioning. T h e effects of a low soil water potential can be transient (Huxley et al. 1974), ar.d while estimates of root activity can positively indicate activity a t a given time and place, they do not reflect the system’s potential for activity under all conditions. Root activity most commonly has been measured with radioactive tracers,
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
431
usually ‘12P.Tracer is injected into the soil a t a number of points with fixed geometry (distance, position, depth) in relation to the tree. The activity in similar trees, but with either different treatments or placements, is compared. The method has been used successfully in a number of crops, including citrus, coconut, cocoa, coffee, and rubber (Nethsinghe et al. 1968; Soong et al. 1971; Huxley et al. 1974). I t has not always been completely successful in apple, largely because of the high variability among replicates (Broeshart and Nethsinghe 1972; Atkinson 1974). In apple, Broeshart and Nethsinghe (1972) found a similar pattern of activity using both 32Pand 15N as tracers; variation (as coefficient of variation, 30 days after injection) was 53% for 32P,but only 27% for I5N. As a result of this, a greater than 2-fold difference in the rate of uptake from 2 different depths was not statistically significant using 32P, but was with IsN. In a study of variations between replicate trees of Betula and Fraxinus they found “variation coefficients” of 125% and 10096, respectively. In a study of young apple trees, Atkinson (1974b) also found high variability (cv = 50%), as well as very low rates of uptake for apple, relative to that for grass and weed species. Like Broeshart and Nethsinghe (1972), Atkinson (1977) found a similar pattern but reduced variation and more efficient uptake (Atkinson et al. 1979) when 15N, rather than :{*P,was used as a tracer. Patterns of translocation from root to shoot clearly vary during the season. To use the technique as an assay for root activity, one must either standardize on a particular organ for assay or understand the changes in translocation. Nethsinghe (1970) found statistically significant leaf type X root position interactions for both citrus and cocoa, although the effects of these interactions were relatively small compared with those of placement and time. Differences in the levels of activity absorbed into leaves of different ages have been reported in coconut palm (Nethsinghe 19661, Heuea brasiliensis (Soong et al. 1971), and apple (Atkinson 1974b). Leaf age did not always interact with root position, but sampling of similar aged leaves is advisable. Atkinson and White (1980) found that the pattern of apparent 32Puptake from different depths was different for leaves and fruit, with much less apparent effect on fruit. The number of tracer injections needed around a tree has been discussed by Nethsinghe (1970), Huxley et al. (1974), and Patel and Kabaara (1975). Nethsinghe (1970) found that variation among replicates was as high with 32 as with 16 injection points, although the level of activity in leaves was increased probably because of the larger amount of tracer used. Patel and Kabaara (1975) noted maximum uptake of 32P with 30 injection points per tree, with 45 and 60 points having little additional effect.
432
HORTICULTURAL REVIEWS
T h e pattern of placement of the injection points can be varied. Most workers have used a ring so that all points are equidistant from the trunk, but banding on one side of the tree may be as efficient as a similar quantity of tracer applied in a circular pattern (Pate1 and Kabaara 1975). T o compare activity in herbicide-treated row and grassed interrow areas practically, placements of ,'I2Pand l 5 N along a row, rather than in a circle, have been used with apparently satisfactory results (Atkinson 1977; Atkinson et a l . 1979). Despite the modifications of the tracer method which have been tested, its major limitation remains the high variability among replicates. T h e most probable causes of this variation are: (1) Unequal probability of individual roots containing the applied tracer because of the limited number of injection points. However, the failure to reduce variation by increasing the number of injection points (Nethsinghe 1970) tends to refute this as the main cause, unless the number of points is still too small relative to the volume of the root system. (2) Soil heterogeneity. This is known to occur for P and can have a large effect because of its limited mobility in soil. (3) Variability among trees. This could be a major factor, but large variations occur even where trees are carefully selected for homogeneity (Nethsinghe 1970). (4) Variations among leaves. This is potentially a major factor, although considerable variation can remain even when multiple standardized samples from individual trees are used (Atkinson 1974b).
The use of isotopic placements is probably the most convenient method of directly assessing root activity a t different points within the root volume and over a season. However, like other sampling techniques, it is limited by variation among replicate samples. Root activity also has been determined using the rate of soil water depletion from different zones within the soil as an index of activity. Although the method can indicate activity a t a given time in the season, like the tracer method it does not predict potential for activity. If a plant has a root system which is non-uniformly distributed through the soil (as is normal), but which has more than adequate capacity to supply water to the tree, then the initial pattern of water depletion will reflect root density. This assumes no great variations in soil hydraulic conductivity a t different positions within the profile and low axial resistances of roots, so that roots close to the trunk are not favored. However, as the soil dries, the rate of water depletion will proportion-
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
433
ately and perhaps absolutely increase from those areas of soil with relatively low root densities (which remained relatively moist) and decrease from the drier areas of higher root density. The rate of water depletion from the former areas (per unit root length and possibly per unit soil volume) then will be higher than that found initially and possibly higher than that from the now drier areas of high root density. This is because of the higher flow rates needed from an effectively restricted root system to maintain transpiration in balance with evaporative demand. Despite these potential problems, patterns of water depletion have been used as indicators of root activity by Cahoon and Stolzy (1959), Atkinson (1978), and Atkinson and White (1980). Cahoon and Stolzy (1959) found good agreement between water depletion and root density for citrus, although they obtained different rates of water depletion/unit length of root in different soil types and a t different depths within one soil type. T h e highest rates of depletion were from deep in the profile, a feature attributed by Taylor and Klepper (1973) to differences in the relative ages of roots. Clearly, this also could be due to differences in soil physical properties. Atkinson (1978) showed good general agreement between root distribution and the pattern of water depletion. Water depletion from below 50 cm depth was highest by trees with a high proportion of deep roots. While initial depletion was related to overall root density, the relationship a t any specific time was less exact, probably as a result of the difficulties outlined above.
E. Indirect Root distribution and density have been assessed by a variety of other techniques. The force needed to remove a tree from the ground often has been used (cf. Fraser and Gardiner 1967) as an index of the size of the root system. Obviously the force needed also will vary with soil type and soil water content. Root weight also has been estimated by using a fixed rootlshoot ratio, from measurements of shoot weight. Any type of indirect method will need careful calibration and can be even more prone to difficulties of interpretation than direct methods. Thus, a review of the literature on methods of assessing the size and activity of tree root systems suggests that major problems are the time and destruction involved in total excavation and the high variability encountered with any type of sampling system. Therefore, the best reflection of root activity and distribution may be given by a combination of methods which reinforce one another.
434
HORTICULTURAL REVIEWS
111. THE DEVELOPMENT OF INDIVIDUAL ROOTS A. Growth and Changes with Age The mature fruit tree root system includes roots which differ in age, diameter, and degree of suberization. The development of young roots on fruit trees has been described by Rogers (1939b, 1968), Rogers and Booth (1959), Rogers and Head (1962,1966,1969),Head (1968a, 19701, Mason et al. (1970), Bhar et al. (1970), Hilton and Khatamian (1973), Atkinson, Lewis and Jones (19771, Atkinson and Lewis (1979), and Hilton (1979). The young root, as seen through the windows of an observation laboratory, is initially white and succulent with short root hairs. After between 1 week and 4 weeks, during most of the year, it begins to turn brown and the root hairs shrivel (Rogers 1939b). Browning takes an average of 2 to 3 weeks during the period of May through September, but can be as long as 1 2 weeks during winter (Head 1966). The browning spreads as a wave from older regions toward the tip. The irregular waves, sometimes days apart, can spread a t 2 to 3 mm hr - l (Head 1968). The browning of the cortex is followed by its decay and disintegration, due largely to the feeding of soil fauna such as collembola, millipedes, symphilids, mites, and enchytraeid worms (Head 1968a). After the loss of the cortex, secondary thickening occurs in some roots which become part of the perennial root system. Other roots, usually laterals, either remain unthickened or disappear completely (Head 1968b). Horsley and Wilson (1971) suggested that the fate of a root tip is related to its relative primary xylem diameter (P X D), with only large roots, those where the P X D is '25% of that of their parent root, surviving. In apple, roots usually can be divided (Rogers and Head 1969) into extension roots and lateral roots. The thicker extension roots survive while the thinner lateral roots tend to be ephemeral, although this class of roots can be infected by mycorrhizal fungi (Mosse 1957).Head (1970)has shown that under some circumstances they may branch highly and remain with a brown, but intact, cortex for several years without any further development. Growing white roots of apple vary from 0.3 to 2 mm diameter. Extension roots of cherry can be even larger. The maximum rate of growth for apple roots seems to be approximately 1 cm day - l , although lower rates are more usual (Rogers 1939b). Head (1968a) reported a similar rate for cherry, as did Hilton and Khatamian (1973) for apple, quince, and grape. Rates of growth can be affected by many factors. Atkinson and Lewis (1979) found that old living roots in the path of a new root reduced its growth rate by about half. Head
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
435
(1965) noted that cherry roots grew faster between 1600 and 2400 than a t other times during the day. Hilton and Khatamian (1973) also observed higher rates of root growth during the night, 1800 to 0600, for a range of fruit species. Mason et al. (1970) and Bhar et al. (1970) found that for Mugho pine and plum (Shiro/Myrobalan), respectively, the rates of both elongation and suberization were related to root diameter, with elongation being more rapid in roots of large diameter. The root hairs on apple are much shorter than those found in many other plants, e.g., black currant, rarely being longer than 0.075 mm and more commonly 0.025 to 0.05 mm (Rogers 1939b). In Prunus species (Head 1968a) the root hairs are longer but tend to be irregularly distributed, being most abundant close to soil particles. In apple (Rogers 1939; Head 1964, 1968a) the root hairs appear to exude droplets of liquid, but the mechanism for the liquid’s formation and its function is not known.
B. Root Soil Contact During its life, the contact between a root and the surrounding soil varies substantially. This clearly will affect effectiveness in relation to the uptake of water and mineral nutrients. T h e effect of root contact on radial resistance to water flow has been reviewed by Tinker (1976), and changes in contact and their significance to fruit trees have been discussed by Atkinson and Wilson (1979). Initially, particularly if the root deforms the soil during its growth rather than utilizing an existing channel, contact between the root and soil should be good. However, Sanders (1971) found that 40% of apple roots visible in a root laboratory were not in contact with the soil, while others were in incomplete contact. Atkinson and Wilson (1979) showed that even while roots remained white, the movements of soil fauna, particularly non-parasitic nematodes, adjacent to the root surface could reduce root/soil contact. Water stress caused substantial diurnal fluctuations in the diameter of maize roots (Huck et al. 1970), but was less effective on cherry roots (Atkinson and Wilson 1979). Where shrinkage occurs, it will affect contact, the greatest influence occurring a t times of maximum demand. After the loss of the cortex, contact between root and soil is poor. Rogers (1968) showed that this could cause a 50% reduction in root diameter, leaving an unthickened stele suspended in a root cavity (Head 1968a,b). If the root becomes secondarily thickened, then contact will improve. Head (1968b) found a maximum rate of thickening of 3.7 mm year - I , and Atkinson and Wilson (1979) concluded that within a season an average apple root of diameter 1.5 mm could decrease to 0.75 mm on the loss of the primary cortex and then reestablish contact with the soil. This contact would
436
HORTICULTURAL REVIEWS
probably remain good (Head 1968b) as long as the root continued to function. Tinker (1976) suggested th at when uptake per unit root length was low, i.e., 0.015 cm:l cm d - I , then contact would be unimportant, but that when uptake was high, i.e., 0.3 cm:' c m - ' d - I , then contact would be critical. Because the total root length in a fruit tree is relatively short (Table 9.1), Atkinson and Wilson (1979) calculated th a t rates of uptake, within Tinker's high range, would occur when transpiration was high. TABLE 9.1. VALUES OF LA(ROOT LENGTH UNDER A UNIT AREA OF SOIL SURFACE) AND Lv (LENGTH IN UNIT VOLUME) FOR TREES GROWN UNDER FIELD CONDITIONS
Species APPLE Fortune/M 9 26-vear Herbicide square
Deuth of SaApling L, (cm) (cm cm - l )
L" (cm cm -'I
Reference
75
6.8
0.09
75 30
3.4 1.9-2.2
0.05 0.06-0.07
Atkinson and Wilson 1980 Ibid White 1977
120
0.8-4.3
0.01-0.04
Atkinson etal. 1976
0.05
Krysanov 1969
60 80
2.9-3.4 7.5-9.1
0.04 0.05-0.06 0.08-0.11
Ibid Reckruhm 1974 Farre 1979
120 120
3.6-23.8 5.2
0.03-0.20 0.04
Atkinson 1978 Atkinson 1977
91 or 122 26-69
0.29-0.56
Cockroft and Wallbrink 1966
60
7-8.2
0.12-0.14
Reckruhm 1974
Merton Glory Sweet Cherry/ F 12/1-2-year
120
15.3
0.13
Peach
91 or 122 17-68
0.29-0.56
Atkinson and Wilson 1980 Cockroft and Wallbrink 1966
CONIFERS Loblolly pine
10
5
0.5
Douglas fir Scots pine Sitka spruce
107 183 -
77 126 68
0.72 0.69 -
Grass interrow Cox/M 26 12-year Golden DelicioudM 9 5-year Pepin SafrannyVForest stock Pepin Safrannyll Red-leaved paradise Golden Pearmain/M 4 Cox/M 26 Golden Delicious/M 9 1-3-year* Cox/M 26* PEAR Williams/Keiffer Beurre Bosc, Conference/ Scedling
PR UNUS
* Estimated from root laboratory measurements-maximum
Kramer and Bullock 1966 Reynolds 1970 Roberts 1976 Ford and Deans 1977 values.
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
437
C. Secondary Thickening
The development of secondary root thickening has been discussed by Head (1968b) for fruit trees and by Fayle (1975) for forest trees. Head (196813) found that both apple and cherry roots may thicken for a period of consecutive years and then stop and, once having stopped, may not start thickening again for several more years. He illustrated this with an apple root which increased in diameter 0.52 mm in 1963 and 0.48 mm in 1964, and then showed no further increase between 1964 and 1967. Some roots survive in the soil as isolated steles for many years without visible thickening. Knight (1961) found that activity in old roots moved as a wave from the junction with the stem to the root tip. However, Head (1968b), in a more extensive study, could find no definite pattern; maximum rates of thickening occurred in July through August, the highest measured rate being 1.84 mm in 27 days on a root originally 3.18 mm in diameter. Root thickening coincided with the late season peak of new root growth, but occurred later than either shoot growth or most trunk thickening. D. The Functions of Different Root Types
The absorption of water and mineral nutrients by plants is often assumed to occur exclusively through the younger parts of the root system, i.e., root tips and areas with root hairs. This type of root has been termed “absorbing root” by Kolesnikov (1971) and this logic underlines Weller’s (1971) principle of counting root tips in core samples as a means of determining root activity. Both basal and apical segments of the seminal roots of barley were able to absorb and translocate both and 32P(Clarkson et al. 1968). Subsequent studies on cereals and annual plants (Harrison-Murray and Clarkson 1973; Graham et al. 1974; Ferguson and Clarkson 1975) have shown that, to a greater or lesser extent, most of the root system is able to function as an absorbing surface, although the rate of absorption is greater in apical areas. For forest trees, Kramer and Bullock (1966) showed that the permeability of suberized roots was 7 to 82% of that of comparable unsuberized roots. T h e absorption of water and minerals by fruit tree roots has been discussed by Atkinson and Wilson (1979, 1980) and Wilson and Atkinson (1978, 1979). Atkinson and Wilson (1979) found that woody roots could function in absorption. T h e uptake of 32Pby white and woody roots (which were of a larger diameter) of F12/1 cherry stocks was similar on a basis of surface area (ng P mm - 2 h -*), but higher in white roots on a volume (ng P mm - 3 h - l ) basis. Both types of roots translocated a similar proportion of absorbed material and absorbed similar amounts of water. Sur-
438
HORTICULTURAL REVIEWS
prisingly, they found that the variation between replicate samples of woody roots (on a basis of surface area) was less than that for white roots. This suggested that injury points or lenticels, which had been suggested as possible entry points into old roots (Addoms 1946), were unlikely to be the major pathway because these, being of irregular distribution, would be expected to lead to relatively high variation. Wilson and Atkinson (1979) found that the uptake of 45Cawas higher in woody roots of F12/1 cherry, while that of RGRb was higher in white roots. White roots translocated about half of the amount of both elements absorbed, while woody roots translocated a higher proportion of RGRb, but a very variable amount of 45Ca.Atkinson and Wilson (1980) found that woody roots of both F12/1 cherry and M 27 apple were able to absorb calcium, and suggested that their ability to function in absorption was likely to be general among fruit tree species. T h e ability of different root types to function in absorption is probably related to their anatomy. MacKenzie (1979) found that most, but not all, of the events occurring in the development of the endodermis, a layer critical in relation to absorption, happened nearer to the tip in apple roots than in those of annual species. T h e early stages in the development of the casparian strip occurred simultaneously opposite both xylem and phloem poles 4 to 5 mm from the tip, as in annual species. However, 16 mm from the tip suberin lamellae developed on endodermal cell walls opposite the phloem poles, and 30 mm from the tip an additional cellulosic layer was formed internally to the suberin. Opposite the xylem poles this change occurred 100 mm behind the tip. Both of these occur a t about 320 mm in barley with most wall thickening occurring 50 to 200 mm from the tip. These processes are unrelated to color changes. One hundred to 150 mm behind the tip the root begins to turn brown, coinciding with the early division of the phellogen and the production of secondary xylem. Rosaceous plants develop, in addition to the endodermis, an inner layer of the cortex known as the phi layer. The lignification of its walls occurs simultaneously with that of the casparian strip. These cells have many plasmodesmata in their radial and outer tangential walls but relatively few in the inner tangential wall. The earlier development of the endodermis in apple must influence the balance of apoplastic and symplastic movement in roots of different ages. T h e function of the phi layer is unclear, although it seems well equipped to move substances to the xylem via “gaps” in the endodermis. It may increase root resistance. Taylor and Klepper (1978) suggested that diurnal root shrinkage would not occur if radial resistance to flow was higher in the endodermal zone than in the cortex. T h e phi layer may therefore prevent diurnal shrinkage in cherry (Atkinson and Wilson 19791, and aid in conservation of water. Passioura (1972) showed that a high root resistance helped to conserve water by distributing it
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
439
more equally over the season. Landsberg and Fowkes (1978) suggested that the optimum length and total resistance of a root were functions of the ratio of axial and radial resistances. As roots of most fruit trees are often long (Rogers 1939a) (Tables 9.2 to 9.51, this implies substantial radial resistances, perhaps created by the combination of the phi and endodermal layers. As in apple, the cherry endodermis appears to become suberized within 5 mm of the root tip (Atkinson and Wilson 1980). In this species nutrient uptake appears to decline more rapidly with increasing distance from the tip (Clarkson and Sanderson 1971) than in cereals. In a secondarily thickened root the increase in root diameter following the loss of tissues external to the pericycle is due to production of phellem and phelloderm (bark) and xylem (wood). To reach the xylem of a woody root, water or ions must cross both the periderm (phellem, consisting of approximately four to six suberized cells, phellogen and phelloderm) (Wilson and Atkinson 19791, and the phloem, although the latter is permeated by parenchymatous rays. Clarkson et d.(1978) demonstrated that suberin lamellae alone need not prevent uptake, while Atkinson and Wilson (1980) suggested that the failure of the periderm to act as a barrier to movement might be related to the deposition of the suberin on the inside of the cellulose cell wall, rather than within the wall as in the casparian strip of the endodermis. Therefore, this should leave the apoplastic path viable in the phellogen, although symplastic movement might be affected unless substantial numbers of plasmodesmata are present. The effectiveness, or contribution to nutrient and water uptake, of the different root types will depend upon the relative amounts present, inherent rates of absorption, contact with the soil, and differential environmental effects on different roots (Atkinson and Wilson 1980). However, in tree crops all roots, rather than just those newly produced, are apparently effective to some extent.
E. The Longevity of Roots in the Soil The survival of roots in the soil has been reviewed in detail by Head (1973) and discussed by Kolesnikov (1968). Root death is part of a natural cyclic process which returns mineral nutrients to the soil and feeds the soil flora and fauna, whose activities are important in relation to soil structure. Copeland (1952) found that the proportion of dead roots in Pinus species increased with age, rising from 2.9 to 3.7% a t 15 years to 6.3 to 18% a t 35 years. With younger trees most dead roots were < 6 mm diameter, but on the older trees some roots > 25 mm were dead. For fruit trees, Kolesnikov (1966) found that in apple, pear, and sour cherry seedlings, 2 to 4.8%of root tips were dead. The rate of root
Unworked 5-year-old M2 M3 M4 M9 MM 106 A2 4-year-old MM 102 Boskoop, Zuccalmaglio, Ontario, Ananas Reinette/M 2 mature trees Papirovka, Antonovka/M 3 12-year-old Papirovka, Shafran, Lenii, Golden Winter Pearmain,
Cultivar and Age Cox/M 1, M 2, M 9 16-year-old
Various soil types
Soil Type Fine sandy loam Clay with flints Clay with impeded drainage Compact sand Brick earth over sand
3.8
71 36 (year 6)
0.85 0.80 0.80 0.40 0.50 0.80 0.75
0-30 0-30 30-100
1.0 1%> 1.0
25 34 Range 1.8 (M 9)9.6(M 3)
0-30 30-100
1%>1.0
28 62% 32% 67%
38% 61%
62%
0-40 (2-year-old) 80-100 (12-year-old)
Framework: below 40 cm
Fine roots: 0-50 5% 50-100 48%
0-30
12%>1.0
26
Babuk 1971
Kolesnikov 1971
Weller 1965
Kovall977
Depth of Main Root Zone (cm) and % Roots Contained (When Stated) Reference 0-30 73% Coker 1958
Vertical Spread (m) 6%> 1.0
Radial S read YmZ) 29
TABLE 9.2. THE DISTRIBUTION OF APPLE ROOTS
.p 0
SI
Calcareous Clayey Chernozem
Cox/M 9 6-year-old Boskoop, Golden Winter Pearmain/M 9
Sandy loam
Golden Winter Pearmain/M 4 Golden Delicious. Red Delicious, Jonathan/M 4 10-year-old Pseudopdzolic Newton Pippin, Cinnamon Wellington/M 4 Forest and 20-year-old Alluvial Meadow London Pippin, Reinette de Champagne/M 2, M 4 Pseudopodzolic Newton Pippin (NP), Cinnamon Wellington (Well)/M 4 Forest and Alluvial Meadow Sandy soil Jonathan/M 4 with high water table Cinnamon Golden DelicioudM 7 Heavy clay Jonathan, Ch ern ozem Richared Delicious Mantuaner/M 9 3-year-old Sandy loam Golden Delicious/M 9 5-year-old
White Winter, Calville/M 4 Jonathan/M 4 4-year-old
67% (HDP')50% (LDP2)0.3 Greater than branch spread,
0-25 >50 (LDP)* 0-25 >50 (HDP)' 0-30
2 (high density 1.2 planting')-,5 lower density planting2)
10-30
49% 25%
54% 15%
73%
Diasamidze and Soziashuiti 1976
20-40
Weller 1966
Atkinson 1976
Atkinson 1978
Doichev 1977 Perstneva 1977
Tamasi 1964
Stoichkov et al. 1975
Stoichkov et al. 1974
20-80
0-60 0-60
2.4
3 (NP)-2.6 (Well)
1.4
Reckruhm 1974 Angelov 1976
0-30 10-60 80%
Tanas'ev and Balan 1976
20-80
Most 12.6
Highest coicentration 0.8
1.4
Vertical Spread (m)
Prize Wagener/M 9 Papirovka; Antonovka/Seedling 12-year-old Boskoop/Seedling
Snow Calville,
Deep loam
98-104
Marly Rendzina
Zuccalmaglio/M 9
2
4.2-4.4
1.o
0.8-1.0
Marly Rendzina
20-170
Moderately high density 0-25, moderate density 25-50 Moderate densitv 0-25. lowmoderate 25-50 11-30
Atkinson 1973b
Fine roots: 0-30 75% Main roots: 0-45 90% 20-80
Ananas Reinette/M 9
Atkinson 1973a
0-30
1.5
Weller 1971
Polikarpov and Adaskalilsii 1977 Kolesnikov 1971
Weller 1965
Nurmanbetov and Andronov 1976 Weller 1965
Coker 1959
0-30 59-7596
5%>1.0
4
10-14 67-SO%, (7 3Xbranch spread 47
Weller 1971
0-70
1.5
Weller 1971
Kolesnikov 1971
Reference
10-70
Depth of Main Root Zone (cm) and % Roots Contained (When Stated)
1.6
Pm2) highest density beside trunk 38-43 3.4-3.6
Radial
S read
CultivadM 9
Cultivar and Age Soil Type 6-year-old Seedling (mature) PaDirovka. AntonovkalM 9 12-year-old Golden Winter Pearmain/M 9 Pseudogley 7-year-old Boskooa/M 9 Pseudodev - 7-year-old Cox/M 9 Sandy loam 16-year-old Sandy loam Fortune/M 9 26-year-old Fortune/M 9 Sandy loam 26-year-old
TABLE 9.2. (Continued)
P
z ! L
=!
XI
3:
U
N
4 &
~
Prostrate forms 5-year-old
Reinette de Champagne/ paradise stock Cultivard Malus sieuersii Cultivars 22-year-old Cultivars 5-year-old
Boskoop, Zuccalmaglio, Ontario, Ananas Reinette/Seedling Boskoop, Golden Winter Pearmaidseedling Jonathan/ Malus sylvestris 5 cultivadcrab stock
Jonathan/Seedling
3 cultivadforest stock
Golden Winter Pearmain/Seedling 30-year-old BoskoodSeedlinp
35-year-old
Dernopodzol
Degraded Chernozem Light soil
Drift sand
Loam
Range of soil types
Loess loam with Parabraunerde Pseudogley on clay
Intermittently wet loam Loess loam
36 53% in 1 3
Most 0.8-1.8
64
Most 12.5
2.5 X crown spread 2 X crown spread
8.6
1.5
2
30-60
1
Tamasi 1965
Weller 1966
Weller 1965
Tamasi 1965
Babaev 1968
Weller 1971
Weller 1971
0-40 80-88% (conventional cultivation) 59-81% (deep ploughing) 10-50 69%
20-80
Ryzhkov 1972
Krayushkina et al. 1977
Nurmanbetov and Andronov 1976 Kolesnikov 1966
20-40 (with cover Ghena 1965 crop) 0-40 (no cover) 20-40 Ghena 1964a
Below 25
0-50
Fine roots: 0-50 37% 50-100 33%
0-30 21-42%
20-75
0-50
0-100
0-50
2
2
2
w
rp
51
m
B
z
4
~
1
~~
HDP= High density planting. LDP = Low density planting.
Cultivars
Cultivars
Reinette Simirenko
Delicious/vigorous stock Pepin Shafrannyl 3 cultivars
Cultivar and Age
TABLE 9.2. (Continued)
Terrace
Soil a t 80% water holding capacity 50% capacity 2-3 X crown projection
Inner terrace: 0-20 Outer: 20-40
Deeper than above
20-60
20-90 cm
To impenetrate subsoil
Sandy soil
65%
De th of Main Root &ne (cm) and % Roots Contained (When Stated) 0-40 15-45
Vertical Spread (m)
Terrace
Soil Type
Radial S read ?mz)
Ryhakov and Dzavakjanc 1967 Kairov eta1.1977
Danov et al. 1967
Zerebcov 1966
Luchkov 1971 Potapov 1971
Reference
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
445
TABLE 9.3. THE DISTRIBUTION OF THE ROOTS OF PEAR TREES, SOME ON QUINCE STOCKS
Cultivar Cultivad quince stock, wild pear Williams/ Keiffer Abate Fetel/ quince Beurre Bosc, Conference/ Seedling 6 cultivad Quince A Quince Quince Quince
Soil Type Degraded Chernozem
Radial Spread (m2)
Sandy soil Sandy loam Shallow soil Highest density 0.3
Depth of Main Root Zone Vertical (cm) and % Spread Roots Contained (m) (When Stated) Reference 2-3 20-40 Ghena 1964a 3.5 40-60 1 1.2
Terrace soil 0.6
0-50 0-60 Fine roots: 25-50 0-30
Cockroft and Wallbrink 1965 Manzo and Nicotra 1967 Reckruhm 1974
10-50
Milanov 1977
Inner area: 0-20 Outer area: 20-40
Kairov et al. 1977
Fine: 0-20 40-60
52% 19%
Kovall977 Mursalov 1966
shedding is influenced by environmental conditions. In gooseberry 25 to 72% of the roots are normally shed in a year (Kolesnikov 1968). In a dry year, irrigation reduced the proportion of dead roots from 85 to 75%. In fir and pine trees, Orlov (1966) estimated the average life of a root to be 3.5 to 4 years, while in fruit trees Head (1973) showed that significant numbers of roots survive for over 3 years. There seems to be no available data on the maximum survival of roots or information on the extent to which very old roots are able to continue with either absorption or translocation. IV. THE SEASONAL PERIODICITY OF ROOT GROWTH
Regardless of whether white roots alone or all roots function in absorption and metabolism under field conditions, the growth of new roots is important to the system. All brown and woody roots originate from white roots, so that any factor affecting new root production ultimately will influence total root length. In addition, the presence of a flush of new growth will greatly increase total root length. This may be critical during some periods in the year and allows the possibility, as a result of variation in the position and depth of new growth, for adaptation to prevailing environmental conditions. Studies of the periodicity of new growth have been reviewed by Rogers (1939b1, Rogers and Head (1969), and Lyr and Hoffmann (1967).
446
HORTICULTURAL REVIEWS
A. Variations Among Species
Lyr and Hoffmann (1967) noted considerable variability to exist among tree species. The basic seasonal pattern, apart from the complicating effects of the cultural practices reviewed later, will be influenced by major environmental variables, e.g., soil temperature and soil moisture. Rogers (1934) and Atkinson (1973c), among others, have observed the effects of short-term fluctuations in soil temperature on root growth. Lyr and Hoffmann (1967) concluded that most authors (beginning with Theophrastus 372 to 287 BC) agreed that in the spring, root growth begins before shoot growth. Richardson (1958) found that the roots of Acer saccharinum began growth at 5”C, while bud expansion began a t 10°C, and suggested that a lower temperature optimum for root growth was a partial explanation for this pattern. In apple, the onset of root growth seems to occur a t a temperature of 6.2”C (Rogers 1939b). After its initiation, root growth follows an irregular time course (Lyr and Hoffmann 1967) with periods of active growth alternating with less active periods. Engler (1903) concluded that, in central Europe, all tree species have a maximum period of root growth in May through June, followed by a rest period and then a second growth period in the autumn. However, other work, reviewed by Lyr and Hoffmann (1967), has not always shown this clear two-peak curve. These reviewers, however, concluded that maximum growth most frequently occurred in early summer. The root growth of fruit trees has been studied for many years using observation laboratories a t East Malling Research Station. Rogers (1939b), studying established trees of ‘Lanes’ Prince Albert’ on M 1, M 9, and M 16, found little root growth during the winter and a major peak of growth in June/July. In some years, and with some stocks, there were also peaks in spring (May through June) and autumn (September). For ‘Worcester Pearmain’/MM 104, Head (1966) noted a small peak in May and a larger peak beginning in July and continuing until October. The end of the initial peak corresponded approximately with the beginning of active shoot growth and that of the second peak with leaf-fall. Root growth in ‘James Grieve’ and ‘Crawley Beauty’, both on M 7, exhibited a similar periodicity, with a single peak in June/July (i.e., as usually found by Rogers (1939b)), despite large differences between cultivars in the time of bud burst. Subsequent studies (Head 1967; Rogers and Head 1969) confirmed the general pattern of a peak of growth in May through June ending a t the time of vigorous shoot growth, and a second peak in August through October beginning after shoot growth had ended. Head (1967) also reported that the periodicity of root growth a t a number of different distances from the trunk was similar. This bimodal periodicity for root growth may be due to competition between shoots and roots for carbohydrate reserves. Quinlan (1965) showed that photosynthates from the eight youngest leaves on a shoot
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
447
were exported mainly to the shoot; only when there were more than eight leaves did photosynthates begin to reach the roots. Priestley et ul. (1976) found that when 14C02was fed to the basal leaves of extension shoots virtually none of the 14Cwas transferred to the root region before shoot extension was under way, while 45% of translocated 14Cmoved to the roots during and after the main period of shoot growth. Similarly, Katzfuss (1973), in a study of a number of cultivars on M 4, found little 14C-labelled assimilate moving to the roots, but large amounts to the shoots, in trees of ‘Golden Delicious’ where root dry matter production was poor. In the other cultivars incorporation into roots exceeded that into shoots after July, reaching a maximum in September when incorporation into leaves was minimal. Lucic (1967) found that reducing relative light intensity from 1300 to 740 relative units reduced by 45% the rate of root growth in 1-year-old pear seedlings within 2 to 3 days. T h e growth rate increased again within three days of re-illumination. However, this interrelationship between shoot and root growth is probably not due entirely to carbohydrate reserves, for growth hormones also are likely to be involved (Richardson 1957). As previously reported, Voronova (1965) noted 5 peaks of root growth in apple, Ryhakov and Dzavakjanc (1967) 3 peaks in 1-year-old trees and 2 peaks in 5-year-old trees, and Zakotin and Atanasov (1972) 4 peaks which were related to flowering, seed development, flower initiation, and fruit ripening. Kolesnikov (1966) observed that root growth extended over a period of five to nine months. Like Head (1966) and Abramenko (1977), Koseleva (1962) found in apple a peak of activity in April through May. Head (1967) found that in unpruned plum trees, in contrast to apple, there was only one major peak of root growth which extended from early May until late July. H e attributed this to weaker shoot growth in plum. Atkinson and Wilson (1980) reported a single major peak of root growth, May through August, in unworked trees of the plum stocks St. Julien A and Pixy. Bhar et al. (1970) observed the highest growth in July through September, while Skripka (1977) found two peaks (spring and autumn), and Voronova (1965) four peaks of growth. For trees of ‘Merton Glory’ sweet cherry on both F12/1 and Colt rootstocks, Atkinson and Wilson (1980) reported a single peak of growth extending from May until mid-July (F12/1) or mid-August (Colt). With Prunus cerusifera Ehrh, Bulatovic and Lucic (1972) found one to three peaks of activity, with the main peak in July/August. Here the number of peaks was influenced by soil condition, reduced by drought, waterlogging, and high temperatures. In apricot (Iglanov 1976) root growth continued for most of the year, with maximum activity in June/ July and September/October. The periodicity of root growth in pear trees has been described in detail
448
HORTICULTURAL REVIEWS
by Head (1968a). He found root growth beginning later in the spring than for apple, and with only a single peak of growth as in plum and cherry. Again, Head attributed this to the relatively weak shoot growth that he found in pear. In contrast, Mursalov (1966) found the most active root growth in MarchIApril, MayIJune, and August through October, with its onset preceding shoot growth. Similar patterns of growth to those found in fruit trees have been noted in other tree species. Ovington and Murray (1968) found a single major peak of activity in birch which began after the end of leaf expansion and ended before leaf-fall. In tea, Fordham (1972) described periods of maximum shoot growth associated with minimal root growth. Here root growth was also severely reduced by drought. Mason et al. (1970) showed that in Mugho pine growth extended from April through November, but was most active in the summer, while for Pinus syluestris, Roberts (1976) found the highest activity to be in March through August, earlier than the July through September period given as most active by Ford and Deans (1977) for Sitka spruce. In addition to other internal factors, the pattern of root growth also seems to vary with tree age. Atkinson and Wilson (1980) showed that in newly planted trees of ‘Golden Delicious’IM 9 one major peak of root growth coincided with shoot growth. However, when the same trees were 3 years old the main peak of root growth was delayed until the rate of extension shoot growth decreased. Age effects in addition will be complicated by the effects of cropping. T h e basic patterns of root growth appear to differ among species, perhaps because of the wide range of environmental conditions under which the studies reviewed were conducted. These, and some cultural factors which influence them, are reviewed subsequently.
B. Effects of Pruning and the Vigor of Shoot Growth Head (1967) showed for both apple and plum that the vigor of shoot growth, as influenced by pruning, affected both the periodicity and elitent of new root growth. In plum, late spring pruning stimulated strong shoot growth in JuneIJuly while reducing root growth, and induced a second peak of root growth in AugustISeptember. Similarly, Head found that pruning of apple stimulated shoot growth, reduced root growth during the most active phase in JuneIJuly, and prolonged inactivity in summer. In pear pruning reduced and delayed the onset of root growth (Head 1968a). Similar effects of pruning were reported by Haas and Hein (1973) and Knight (1934) for apple. In black currant shoot removal in late July caused an immediate reduction in the length of white root present (Atkinson 19721, while in tea pruning caused root growth to cease
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
449
for three months (Fordham 1972). Root growth seems to be retarded during active shoot growth. However, the usual balance between tree shoot vs. root weights (Rogers and Vyvyan 1934; Atkinson et al. 1976), implies either increased growth during other periods, or survival of more of the roots produced so as to maintain the overall balance. Schumacher et al. (1972) found th at foliar applications of “Alar” (2,2-dimethylhydrazide of succinic acid) to apple retarded both shoot and root growth. I n raspberry, root growth in the initial year was best in those plants with the best shoot growth (Atkinson 1 9 7 3 ~ ) . C. Effects of Cropping
Head (1969a) investigated the effect of cropping on the periodicity of new root growth. From July onwards even light crops of fruit reduced root growth; in some years fruiting eliminated the major growth peak observed in deblossomed trees in July through September. Weller (1967) noted t ha t cropping reduced the length of fine roots present and th a t variation in root length was reduced in vegetative trees. Ryhakov and Dzavakjanc (1967) observed one peak of growth in cropping trees and two in vegetative trees, while Dzhavakyants (1971) reported root growth in spring-summer in cropping trees and, additionally, in autumn in noncropping trees. Adverse effects of cropping on root growth also have been detailed by Semina (1971), Golikova and Grachev (1973), Atkinson (19771, and Zakotin and Atanasov (1972). Avery (1970) investigated the effect of cropping on growth in a range of rootstocks of varying vigor, including M 2, M 26, 3430 (very vigorous), and 3426 (more dwarfing than M 9). Th e latter had the largest effect, particularly on root weight. In this stock fruiting caused a net decrease in root volume, presumably because roots lost due to natural cycles (Kolesnikov 1968) were not replaced. Chalmers and van den Ende (1975) found t ha t the proportion of the annual increment of dry weight going to the root system decreased from 20% in a young tree to 1% in a mature tree. Corresponding values for percentages of dry weight production going to the fruit were 30 and 70%, respectively. I n addition, the ratio of top to root growth increased from 1 to 4 with increasing age. These studies suggest t ha t cropping is likely to be responsible for much of the yearto-year variation in root growth.
D. Other Factors T h e periodicity of root growth can be affected by a range of other potential factors, both internal and external to the tree. Defoliation of apple trees four to six weeks before natural leaf-fall reduced the length of
Cultivar/Mahaleb
Subkhany, Isfarak/Seedling Cultivars Krasnoscekij 6- 7-year-old Meilleur d'Hongrie, Paviot, Luiset, Tardive de Bucharest/ 6 stocks CHERRY Sour cherry/Mahaleb Germersdorfer/Mahaleb Sour cherry/Mahaleb
Cultivars/Myrobalan
APRICOT Ungarische Beste, Timpurii de Thyrnau, Paviot, Tirzii de Bucuresti/Myrobalan 12-year-old Paviot/Myrobalan, apricot, peach, plum stock
Species and Cultivar ALMOND
Degraded Chernozem
2.1 (1-year-old)10 (5-year-old)
Sandy
1.7-3.4 Few vertical roots Few>O.9
Ghena 1964b
Tamasi 1975 Tamasi 1973
11-40 21-50 0-20 20-60
8%
Tamasi 1976
Iglanov 1976 Popescu 1963 Bespecalnaja and Smykov 1965 Lupescu 1965
Ghena 1965a
Lupescu 1961
Reference Dziljanov and Penkovl964b Ghena and Tertcell962
1-40 87%
Fine roots: 20-40
Superficial
0-25
30%
Fine roots: 19-40 Framework: 20-60
Depth of Main Root Zone (cm) and % Roots Contained (When Stated) 20-60
0-20 2.85-3.90 depending on cultivar 2-2.5
2.4 (1-year-old) 0.8 13.3 (5-year-old)
Most 12.5
Greater than crown
Vertical Spread (m) 97% <0.83
Clay
Degraded Chernozem
Soil Type 4 different soil types Red brown forest
Radial S read (mZP Greater than crown
TABLE 9.4. THE DISTRIBUTION OF PRUNUS ROOTS
n
2
8z
0
cn
.p
Red-brown forest
Calcareous
Chlorosis resistant and susceptible cultivars
Sand
Calcareous organic over limestone Sand over Chernozem Sand Sandy loam
Chernozem over clay
Chernozem
Terrace soil
Louvain Beauty, Tulev grass, Red Nectarine, Anna Spath/Myrobalan Cultivars/Myrobalan
PLUM Besztercei/Myrobalan
Puller, Golden Queen/ Seedling Cultivar 10-year-old
Vladimirskaya/Mahaleb PEACH 10 cultivars/plum stock Cultivars
Cherry, peach, plum,
0.9 (1-year-old) -8.0 (5-yearold)
19.6
1.2 Deeper under grass than mulch
1
5 0.8-0.9 Dziljanov and Penkovl964a
Kolesnikov 1971 Rosati et al. 1976
Kairov et al. 1977
Ghena 964b
20-40 with cover Ghena 965 crop more superficial under cultivation 25-60 cm Molcanov 1966 (susceptible) initially 0-20 then 10-50 (resistant)
Framework: 20-25
Tamasi 1973
Cockroft and 0-15 Wallbrink 1966 0-30 0-15 (under mulch) Hill 1966
All sizes: 20-80
Framework: 40-60
All sizes: 40-60
Fine: 0-80
Inner: 0-20 Outer: 20-40 0-50
r!
i l
m
Acid sand Alluvial meadow 2 Leached 3 cinnamon forest Terrace soil
Forest trees (unmecified)
Walnut
Kazanlik Rose
Slash Pine 12-year-old
Pinus elliotti
Pinus sylvestris
Greater than branches
1.8
1.6 3.4 1.1 2.5
Kairov et al. 1977 Inner: 0-20 Outer: 20-40 0-60 77-90%
Kochenderfer 1973
Roberts 1976 Atanasov 1965
50%
76% 68%
Jacoboni and Cartechini 1964 Inforzata and De Carvalho 1967 Reynolds 1970 Schultz 1977 0-30 0-30 0-15
0-30 0-30 0-46 0-30
0-50
0-50 63% upper soil layer Thagusev 1968
3.1 2.25
1.8 28
Inforzato and Reis 1964
0-50
Aiyoppa and Srivastava 1965
Reference Northwood and Tsakiris 1967 Chiba 1966 Till and Cox 1965 Spina 1966
3.7
1.05
1.4
0-30
Depth of Main Root Zone (cm) and % Roots Contained (When Stated)
Most 2
90% within 3 Greater than branch spread 3
Radial Spread (m2) 63
Podsolized sandstone Coarse sand Deep sand
Leached Chernozem
Terra roxa
Sandy
Under mulch
Soil Type
Papaya/4 month 1-year-old Douglas Fir
Hazel
Coorg Mandarin Seedling 1%-year-old Coffee Yellow Bourbon Coffee Mundo Filbert
Cashew 2Yz-year-old Chestnut Valencia Orange Mandarin, lemon/sour orange
Species
Vertical Spread (m)
TABLE 9.5. THE DISTRIBUTION OF THE ROOTS OF OTHER SPECIES
DISTRIBUTION AND EFFECTIVENESS OF, T R E E ROOTS
453
white root present for the rest of the year and sometimes delayed the onset of root growth the following year (Head 1969a).A reduction due to defoliation also has been reported by Haas and Hein (1973) and Hansen (1972). Root growth of apple trees not receiving an application of nitrogen in the spring showed a greatly reduced peak of root growth in May through June, although the late summer peak of root growth was unaffected (Head 1969b). Thus, new root is not produced a t a constant rate throughout the growing season, and, therefore, both the length of white root present a t any point in the season and total root length are variable. The importance of this variation will depend upon the size of root system and the demands placed upon it. V. THE DISTRIBUTION OF THE ROOTS OF TREE CROPS A. Apple
In one of the earliest published studies of the apple root system, a 7- or 8-year-old ‘McMahom’ apple tree, Goff (1897) described a fairly shallow scaffold of roots with deep vertical roots descending to 9 f t (2.7 m). There was no tap root and the spread of the roots was much greater than that of the branches. These general principles have been confirmed in later studies of a range of rootstocks on a range of soil types (Rogers and Vyvyan 1934; Atkinson 1973; Atkinson et al. 1976). T h e basic form of the root system of a young apple tree is shown in Fig. 9.1. Reviewing the results of a number of studies, Rogers (1939) concluded, “The root system is generally more extensive than the branch system and in trees. . . it may occupy soil layers extending to many feet below the surface. T h e root will in fact grow in any soil area which supplies what it requires, subject to limiting factors.” This does not, however, mean that the root system will be evenly distributed through the potential soil volume. Information from recent studies on root distribution is summarized in Table 9.2. A wider spread of the root system than the branches seems to be general. The surface area of soil exploited seems to range from 2 m2 (Atkinson et al. 1976) to 104 m2 (Kolesnikov 1971) with the most common values being within the range of 10 to 30 m2. Root spread is influenced by rootstock, tree age, and soil type and condition, factors discussed in detail in later sections. Despite the wide potential and actual range of root spread, the highest concentrations of roots seem to occur in a much smaller zone, as small as 0.3 to 1.0 m2,close to the trunk (Angelov 1976; Doichev 1977; Atkinson 1976; Coker 1959; Krayushkina et al. 1977; Ryzhkov 1972).
454
HORTICULTURAL REVIEWS
FIG. 9.1. THE EXCAVATED ROOT SYSTEM OF A 5-YEAR-OLD TREE OF ‘GOLDEN DELICIOUS’/M 9
Rogers and Vyvyan (1934) found that for a tree of ‘Lane’s Prince Albert’/OF5 where the root spread exceeded 65 m2, 36% of the root weight was in the center 1 m2 and 68% in the center 9 m2.Similar trends were found for a range of stocks and soils, with the highest proportion of root in the center 1 mz being 82% for trees on M 9 in a light sandy soil. The distribution differed for roots of different diameters, with a higher proportion of roots < 1 mm diameter being found a t greater distances from the trunk. Although many stocks have the potential to spread widely, they are likely to be restricted by the presence of adjacent trees and thus affected by planting density. Coker (1958) found that the area exploited by the roots of trees of ‘Cox’/M 9 was 8 to 14 m2, depending upon soil type,
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
455
while Atkinson (1976) found that for somewhat younger trees of the same combination the root spread could be as low as 3 m2. Atkinson et al. (1976) reported areas of 1 m2 for very high density plantings of ‘Golden Delicious’/M 9. Reviewing the literature on the intermixing of adjacent root systems, Atkinson et al. (1976) concluded that this occurred only in high density plantings. In their study the root systems of 5-year-old trees a t densities greater than 2000 trees/ha intermixed, while those a t densities below this did not. Schultz (1972) also found a similar effect of planting density on the intermixing of adjacent root systems. This effect may be explained both by inhibitory substances produced by the roots and by gradients of water potential within the root volume. Although the roots of fruit trees may spread over a large area, their distribution within this area is unlikely to be uniform even a t similar distances from the trunk. Rogers and Vyvyan (1934) divided the root system into quarters and found that as much as 51% of root weight could be found in a single quarter and that commonly 60 to 70% was found under half of the soil surface area. A similarly uneven distribution, as shown by Atkinson (1973a) and Atkinson et al. (1976), is illustrated in Fig. 9.1. The depth to which apple roots penetrate is also variable, recent papers (Table 9.2) giving a range of 0.4 to 8.6 m, with 1to 2 m as the commonest range. T h e absolute limit will be fixed by the depth of the bed rock, although some roots (Atkinson 1973a) can penetrate fissures. Penetration is likely to be influenced by rootstock (Koval 1977) and tree density (Atkinson et al. 1976) in the early stages of growth. While a few roots a t very great depth may be of value for survival during prolonged drought, they are likely to be of limited value during normal growth. The zone which contains the majority of roots is much more limited in extent. With a few exceptions most roots are found a t 0 to 80 cm, and approximately 70% of root weight occurs a t 0 to 30 cm depth. Thus, while the total range can be large, a high proportion is found close to the surface. This fraction is influenced by tree age; e.g., Babuk (1971) found most roots a t 0 to 40 cm on 2-year-old trees of a number of cultivars/M 4, but a t 80 to 100 cm in 12-year-old trees. It also can be affected by soil management (Coker 1959; Ghena 1965; Krayushkina et al. 1977), soil type (Coker 1958), and tree density (Atkinson et al. 1976), effects to be discussed in detail later. Rogers and Vyvyan (1934) found that the distribution with depth differed among roots of different diameter; e.g., for trees of ‘Lane’s Prince Albert’/M 9, 48% of total root weight was found a t 0 to 34 cm, but only 28% of roots were < 1 mm diameter. Conversely, a t 100 to 150 cm depth there was 12% of total weight, but 23% of roots < 1mm. Similarly, Atkinson et al. (1976) found over 60% of roots > 2 mm diameter
456
HORTICULTURAL REVIEWS
a t 0 to 25 cm depth, but only 35% of roots < 2 mm. A more superficial distribution of the root framework, as compared with the finer roots, has been described by Atkinson (1973b1, Weller (1965), and Kolesnikov (1971). B. Pear
T h e root distribution of pear trees and pears on quince stocks has been studied less than that of apple, although a thorough description is given by Rogers (1933). In contrast to apple, some pear cultivars have a much more vertically orientated root system. The extent varies among rootstocks and is greater for seedling pear than for quince stocks, although even (pear) stocks lack a true tap root. They have, however, many roots descending to 1 m and a smaller number to greater depths. The horizontal component of the root system is better developed on quince stocks. Information on pear root distribution is given in Table 9.3. Horizontal root spread ranged from 7 to 28 m2 (Rogers 1933), depending upon cultivar, and was 2 to 3 times that of the branches, as in apple. Many roots (62 to 80%) were found in the 1 m2 nearest the trunk and 92 to 100% within 4 m2. Manzo and Nicotra (1967) reported most roots to be in the central 0.3 m2 area. The reported maximum depths of penetration for pear roots range from 0.6 to 3.5 m with, as in apple, the zone containing most roots being much closer to the surface, i.e., 0 to 60 cm depth and with as much as 52% (Mursalov 1966) between 0 cm and 20 cm depth.
C. Prunus Species The form of the sour cherry root system has been described by Kolesnikov (1971) and is similar to that of apple and pear in having both horizontal and vertical components which can vary in their relative development. Information on root distribution in almond, apricot, cherry, peach, and plum is given in Table 9.4. T h e area of soil exploited by sour cherry roots varied from 2 (Tamasi 1973) to 20 m2 (Kolesnikov 1971) and was greater than that of the branch system. Radial spread increased with age and varied among soil types (Tamasi 1973,1976).T h e maximum depth of root growth ranged from 0.8 to 5 m, with values of 1 to 2 m being most common. However, as in other fruit types, the majority of roots were found in a more restricted zone (0 to 60 cm depth), with significant numbers found a t 0 to 25 cm. Again the distribution of the root framework seemed to be more superficial than that of fine roots. There was no large difference in root distribution among the different Prunus types.
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
457
D. Other Tree Crops Information on the root distribution of a wide range of other tree crops, some grown for fruits and some for wood, is given in Table 9.5. Horizontal root spread ranged from 2 to 63 m2 and usually exceeded that of the branches. T h e depth of root penetration varied from 1 to 3.7 m, although most roots seemed to be a t 0 to 50 cm and in many cases, 0 to 30 cm. T h e depth of root growth and that of the zone containing most roots appeared to increase with age (Inforzata and De Carvalho 1967) and to be affected by soil type (Atanasov 1965). E. Conclusions
The root systems of tree crops have many similarities. In the species discussed, the horizontal spread ranged from 2 to 100 m2, most commonly 10 to 20 m2, the vertical spread from 1to 9 m, commonly 1 to 2 m, and the zone containing most roots was 0 to 50 cm depth. However, root distribution merely indicates a potential for activity and need not be the same as effectiveness. Distribution changes with age, differs among varieties, cultivars, and soil types, and can be modified by soil management and orchard factors such as pruning and spacing. These aspects are discussed in detail in the remainder of this review. VI. ROOT DENSITY IN TREE CROPS The density of roots in the soil is important for the absorption of water and mineral nutrients, and has been discussed in relation to annual plants by Newman (1969), Andrews and Newman (1970), and Newman and Andrews (1973), and for tree crops by Atkinson and Wilson (1979, 1980). Root density can be expressed relative to either soil surface area (LA = cm cm - 2 ) or soil volume (Lv = cm cm - 3 ) . Some estimates of these parameters for fruit trees are given in Table 9.1. Reported values of LA for apple range from 0.8 to 23.8, with 2 to 6 being most common. In pear and peach the maximum value reported, 69, was much higher and similar to some reported for conifers (68 to 126). Newman (1969) reviewed data for a wide range of species and found that, in Gramineae, reported values were in the range of 100 to 4000 and in herbs 52 to 310, i.e., both considerably higher than in fruit trees. The consequences of a low L A value have been discussed by Atkinson and Wilson (1979,19801, who described the situation as follows. When a plant transpires, it withdraws water from the soil. This will come initially from soil immediately adjacent to the root with this zone being replenished from bulk soil. If the rate of withdrawal exceeds the rate of water movement through the soil to the
458
HORTICULTURAL REVIEWS
root, i.e., the rate of uptake exceeds soil hydraulic conductivity, then the soil adjacent to the root will become drier than the bulk of soil and the rate of water flow into the root will decrease and may result in water stress. This process is important both to water and nutrient supply. Localized drying, and thus gradients of water potential a t the root surface, will reduce the uptake both of minerals thought to be moved by mass flow, e.g., calcium, and those where the diffusive characteristics of the soil are important, e.g., potassium and nitrate. If root density is high, flow rates always will tend to be low and gradients a t the root surface will be rare. Where root density is low, as in fruit trees, the contrary will be true. Newman (1969) calculated that soil resistance a t the root surface would become high, i.e., > 0.2 MPa, only when LAwas < 10. In orchards this seems likely to occur. In addition, Atkinson and Wilson (1980) emphasize that root density varies with depth, so reduced soil water potentials will not be the same a t all depths and this will, therefore, affect the balance of nutrient uptake from different parts of the soil profile a t different times during the season. When plants compete with one another, as often occurs in an orchard, nitrogen uptake will depend upon the relative amounts of root on different plants (Andrews and Newman 1970). In addition, the uptake of phosphorus, because of its limited diffusion in soil, always will be dependent upon root length. In fruit trees relative root length seems to be limited, and so rates of uptake per unit root length are likely to be high. In a review of nutrient flow rates into roots, Brewster and Tinker (1972) concluded that average rates of nutrient inflow for a range of species were 1 pmol cm - l s - * for N and 0.1 pmol cm - l s - l for P. For fruit trees Atkinson and Wilson (1980) suggested that comparable values would be 8.5 pmol cm - l s - l for N and 0.56 pmol cm - l s -1 for P. As a result of these high flow rates, fruit trees are liable to be more susceptible to both competition, particularly from species with high LA values, and to adverse soil conditions, than species which have lower relative flow rates. VII. ROOT ACTIVITY AND EFFECTIVENESS IN RELATION TO DISTRIBUTION
T h e previously reviewed studies (p. 437) of the ability of woody and other older roots to function in absorption suggest that the whole of the tree root system and all of its roots should be considered with respect to the system’s effectiveness. New growth is, however, important in increasing the size of the root system (so exploiting new soil volumes and re-exploiting others), giving the flexibility to adapt to changing conditions and to the production of growth substances. Atkinson (1974) found a close correlation in 2-year-old apple trees of
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
459
‘Cox’IM 9 between the length of white root present and the uptake of :3zP injected into the soil a t a number of depths, both growth and activity peaking in AugustISeptember. As the season progressed, both the distribution of new growth and relative uptake from depth increased. In 26-year-old apple trees of ‘Fortune’/M 9 a substantial amount of was absorbed from 90 cm depth where excavation showed a substantial root presence. The translocation of absorbed tracer from any given depth seemed to be equally efficient a t different times during the season. Nicolls et al. (1969), Broeshart and Nethsinghe (1972), Atkinson (1974b1, and Shorokhov (1976) all found maximal uptake from relatively superficial placements, 10 to 20 cm depth, in young apple trees. In older trees (Atkinson 1974b; Atkinson and Wilson 1980) there was much more activity a t depth. Atkinson (1977) and Atkinson and White (1976a) showed a good relationship between the horizontal distribution of white apple roots as seen in a root laboratory or by excavation and the distribution of the uptake of both 32P and 15N. Moreover, Atkinson et al. (1979) and Atkinson and White (1980) compared the horizontal distribution of roots exposed by a profile wall technique with the uptake of 15N.Although root distribution was a reasonable guide to root activity averaged over a season, the presence of roots a t any given point in time, even under conditions apparently favorable for activity, did not assure root activity. The mechanism by which activity was switched off and on was unclear. Using similar trees, Farre (1979) found a pattern of root distribution with depth similar to that described by Atkinson and White (1980) on the basis of the uptake of 32P,This relationship was not as strong for trees under herbicide than for those under grass. In coffee the position of maximum root activity within the soil volume can change rapidly within a single season (Huxley et al. 1974). Many workers have tried to relate root distribution to water absorption. Because the amount of water held in soil is finite, the relationship may change as the season progresses (p. 4321, and as trees age. Atkinson (1978) showed that the relationship between new growth and water depletion was good in young trees a t a range of spacings, but poorer for older trees. Detailed results on root activity and water depletion are discussed in later sections with respect to applied treatment effects (p. 464-469). Faust (1980) suggested that new root growth, photosynthesis, and calcium uptake were causally related. H e found that the application of simazine, known to inhibit photosynthesis, to apple seedlings in water culture decreased both new root growth and calcium uptake. These adverse effects were overcome by feeding sucrose to the plants. However, suberized and woody roots are able to absorb calcium (Atkinson and Wilson 1980), and the need for an adequate length of root, energy for
460
HORTICULTURAL REVIEWS
calcium uptake, or an additional factor produced in parallel with photosynthesis may be more important in affecting calcium uptake than photosynthesis itself. T h e relative lengths of white and woody roots present a t different times in a season and on trees of different ages have been discussed by Wilson and Atkinson (1979). The length of white root varies during the season (see p. 445). As a result the relative length of brown root on 2-year-old apple trees could fluctuate from approximately 15% a t the height of the main peak of new growth to approximately 100% in winter or a t times of no new root production, as in mid-summer. Atkinson and Wilson (1979) found no association between the periodicity of new root production and the depletion of soil water, which provides additional evidence for the role of brown roots in the absorption of water. Root growth will be affected by the incidence of pests and diseases in the soil. A detailed review of this is outside the scope of this paper, but the following examples illustrate potential effects and the need to consider the effects of other organisms which are present in real soil situations. Rogers and Head (1969) reviewed the effects of specific apple replant disease, which prevents normal growth on a site where trees of the same species recently have grown. The roots of affected trees are darker in color than healthy roots, grow less vigorously, and develop fewer lateral branches. The effect is most obvious where new trees have been planted, but probably also occurs within the root system of an established tree. Rogers and Head (1969) pointed out that the type of root growth in apple changes, in both amount and morphology, with tree age. Sewell (1979) has shown that species of Pythium, which commonly occur in the soil, can have a major effect on root development, while Zentmyer (1979) has discussed the effect of Phytophthora cinnamomi on Persea indica and Mircetich et al. (1976) the effect of Phytophthora on cherry roots. Pitcher and Flegg (1965) described the effects of nematodes of the species Trichodorus viruliferus Hooper on individual apple roots. The activity of apple roots also can be beneficially influenced by microorganisms. Mosse (1957) showed that apple seedlings infected with an endogenous mycorrhiza grew better than uninfected seedlings, while Atkinson and White (1980) suggested that this might be the cause of the very high rate of phosphorus uptake found with apple trees grown under grass, but with abundant irrigation. T h e effectiveness of roots is influenced by soil temperature. Tromp (1978, 1980) found that apple trees on M 9, M 26, or M M 106 rootstocks had a minimal Ca/K ratio a t 18" to 24"C, as a t this temperature K uptake was maximal, while that of calcium was less affected by temperature. Gur Hepner and Mizrahi (1976) showed that temperatures above 25°C had an adverse effect on both root and total growth, al-
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
461
though some of the adverse effects could be overcome by potassium applications. Gur, Mizrahi and Samish (1976) reported differences among rootstocks in their reactions to supra-optimal temperatures. They found an optimum temperature of 25°C for M 1, M 2, M 9, M 25, MM 109, and some local stocks, and 30°C for M 7. Susceptibility to supraoptimal temperatures was variable and influenced by the scion cultivar. As soil temperature varies both with depth and time of year, under field conditions, this is likely to influence the relative activity of roots a t different depths in the soil and to interact to give changes within a season. Because of their distribution with depth, under field conditions, different parts of the tree root system are exposed to different nutritional conditions. The effect of treating different parts of the root system with different concentrations of nutrient solutions has been discussed for apple by Taylor and Goubran (1976). They found that non-fed root parts could be supplied with enough phosphorus by redistribution to maintain active growth. However, the proportion of the root system fertilized influenced the plants’ P content, although uptake by any part of the system was independent of the activity of other parts. The pattern of P absorption from areas differing in P concentration was related to the relative concentrations, while the concentration of P in non-fed roots remained low irrespective of the concentration in the roots in well fed areas. Atkinson and Wilson (1980) have verified this latter point for N, but not for K under field conditions. Variations in nutrient concentrations among parts of the root system have been studied in Pinus contorta by Coutts and Philipson (1976, 1977) and Philipson and Coutts (1977). They found that when different nutrient concentrations were applied to the two halves of a root system, root growth was stimulated only in the half exposed to the higher concentration, although nutrient concentrations increased in both halves. Thus, translocated nutrients had little effect on growth which differs from Taylor and Goubran’s (1976) results. Philipson and Coutts (1977) found that different parts of the root system seemed to compete for assimilates, with the enhanced growth of one part of the root system being accompanied by the reduced growth of another. Atkinson and White (1980) have suggested that this occurs when different horizontal sections of the root system are subjected to different soil water potentials, while a similar effect with respect to vertical parts of the root system has been demonstrated by Atkinson et al. (1976). Coutts and Philipson (1977) have shown that if gradients of nutrient supply among different parts of the root system are removed, then previously deprived parts are able to respond to improved nutrient supply. Thus, the perennial root system retains the plasticity to respond to changing nutrient conditions. Although one of the major requirements of a tree root system’s ef-
462
HORTICULTURAL REVIEWS
fectiveness is physical support, this seems to have received little attention in recent years. Rootstocks are, however, known to vary in their abilities to support trees (Brase and Way 1959).Rogers and Parry (1968) investigated the effects of deep planting of trees of M 7 on anchorage and performance. They found that deep planted trees developed a new root system a t the surface, but initially maintained enough roots a t depth (although these were replaced by the surface roots) to give good anchorage. These trees were better anchored than the control trees which were planted normally. Root distribution is likely to influence the effectiveness of support. The relationship between root distribution and activity or effectiveness is not simple. Different root distributions will vary in their effectiveness for different purposes. The optimum root system in the field is likely to be a result of a series of interactions. VIII. THE EFFECT OF ENVIRONMENTAL AND MANAGEMENT FACTORS ON THE DISTRIBUTION AND EFFICIENCY OF TREE ROOTS
A. Soil Type Many papers deal with general effects of particular, often local, soils or soil types upon root growth, e.g., Weller (1971). Clearly, soil type can influence the tree root system. Rogers and Vyvyan (1934) described the effects of loam, light sand, and heavy clay soils on trees on a range of rootstocks. Depth of rooting increased from sand to loam to clay. In loam and sand the root system had the same general conformation, a shallow scaffold with vertically descending roots. In clay, most roots sloped down and grew in the subsoil, although with a marked depth boundary (90 cm) where a seasonal water table occurred. The total weight of root on a given scion/stock combination was in the order loam > clay > sand. The ratio of stem to root varied from 2.0 to 2.5 for loam and clay to 0.7 to 1.0 on sand. Coker (1958) also investigated the effect of a range of soil types on a range of rootstocks. Impeded drainage and compaction a t depth checked downward growth of roots. Like Rogers and Vyvyan (19341, he found that the main scaffold was a t greater depth on the heavier soils. Root branching in the top soil was more prevalent in sandy loam than in clay loam. These results have been confirmed by other studies. Dziljanov and Penkov (1964a,b) and Ghena (1966) both found large effects of soil type upon root growth, while Hoekstra (1968) reported poor root development on sandy soils and Tamasi (1964b) the adverse effects of a shallow water table. Weller (1971) studied the distribution of root tips on mature trees of either ‘Golden Winter Pearmain’ or ‘Boskoop’ apple on seedling root-
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
463
stocks in relation to soil type and profile. Root distribution a t depth (below 100 cm) was reduced by impeded drainage. Comparing distribution on a brown loess with that on a similar soil but where clay particles had migrated from the upper layers to the B horizon (Parabraunerde), he found that the number of root tips decreased sharply a t the point of clay accumulation where the minimum percentage of soil, air was found. Webster (1978) investigated the relation between soil physical conditions and root development. He found that the abundance of small apple roots (< 5 mm diameter) was related to porosity. Below a given boundary porosity, roots were sparse or absent; above this they increased with increasing porosity. The boundary porosity was from 29 to 39%, depending upon soil texture. Root growth was poor if less than 10% of soil volume was air-filled a t -10 KPa tension. As the relationship between total porosity and pore size distribution is not constant (Atkinson and Herbert 19791, Webster’s observed relationship may not hold for all soil conditions.
B. Fertilizers Studies of the effects of mineral fertilizers on the root growth of fruit trees probably have been fewer than with some other crops because of the limited response of tree crops to fertilizers (Greenham 1976; Atkinson and White 1980), a feature emphasized since the introduction of herbicides. Rogers (1933) found that pears receiving an application of farmyard manure (FYM) a t planting had a larger root system, a higher ratio of stem to root weight, and a more restricted root spread. Bziava (1966) showed that in the absence of fertilizers, 80% of tea roots occurred a t 0 to 20 cm depth, compared with 57% in plants receiving NPK fertilizer. Farmyard manure, however, promoted growth a t depth to a greater extent. In addition, the fertilizer increased the weight of large roots five to six times and small roots two to three times. Krasnoshtan (1975) found that fertilizers could increase root length by 13 to 170% for apple trees on M 3 stocks, while Tanas’ev and Balan (1977) reported that the combination of FYM and PK produced the longest roots. Weller (1966a) demonstrated that the addition of a mineral fertilizer close to the tree trunk increased root density there, but a t the expense of root growth elsewhere within the system. Similarly, Smith (1965) showed that if only half of a citrus tree’s root system was fertilized, root growth was enhanced in the fertilized part, but that excessively high fertilizer rates and NaN03 reduced root growth. Head (196913) showed that in the absence of applied fertilizers ‘Worcester’IMM 104 apple trees did not show new root activity in the spring. Goode et al. (1978a), however, could detect no effect of either rate or timing of nitrogen application on
464
HORTICULTURAL REVIEWS
root growth of ‘Cox’/MM 104. Response to fertilizers will interact with those to irrigation and soil management.
C. Irrigation T h e reduction in apple root growth under warm conditions in the summer usually coincides with the drying of the soil (Rogers 1939b),with growth reduced a t a soil water potential of -40 to -50 K P a or lower. Similarly, the root growth of peach trees in Australia (Richards and Cockroft 1975) was enhanced by keeping the soil moist by frequent irrigation (every three to four days). They suggested that soil drying determined the growth of roots in the surface soil. Here the high concentration of roots in the surface soil, combined with a low frequency of irrigation and a high transpiration rate, resulted in rapid soil drying and in slower root growth. Conversely, the combination of slow drying and a low root concentration resulted in good root growth. Goode and Hyrycz (1970) found that irrigation increased the weight of black currant roots a t several distances from the bush. There was no effect on distribution and soil moisture deficit was related to root density. Goode et al. (1978a) showed that irrigation increased root density in apple trees ‘Cox’/MM 104, although the effect was significant only a t 0 to 15 cm depth. In contrast (Goode and Hyrycz 1964), there was no significant effect of irrigation on the total amount of fine root ( < 1 mm diameter) on trees of ‘Laxton’s Superb’!M 2, although here the treatments affected root distribution both a t 1 m and 2 m from the tree. Irrigation increased root weight a t 0 to 15 cm and reduced it a t 1 5 to 30 cm depth. Yakushev (1972) and Ponder and Kenworthy (1976) also increased root production by irrigating. Doichev (1977), however, found no effect of irrigation on root distribution, nor did Sidorenko (1973) or Cahoon and Stolzy (1966). Thus, the effects of irrigation are variable, probably as a result of variations in other factors which influence root growth, e.g., tree growth, soil condition. Also, soil water is limiting to a varying extent. T h e method of irrigation can also influence root distribution. Huguet (1976) found that drench irrigation, which was wasteful of water, limited rooting to a superficial zone, while localized irrigation, with one application point a t the tree trunk, resulted in poor root growth because of waterlogging and excessive leaching. His best results came from localized irrigation with 2 application points, each 50 cm from the tree. This gave a dense and regular pattern of root growth. Doichev (1977) compared furrow and sprinkler irrigation with apple trees of ‘Golden Delicious’/ M 7. With both methods, most roots were a t 0 to 60 cm depth, equally distributed 0.5 to 2.0 m from the trunk. Doichev et al. (1974) observed,
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
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however, that the main horizontal roots were deeper and growth was enhanced more with furrow irrigation than with overhead sprinkler irrigation. Taylor (1974) investigated the effect of trickle (drip) irrigation on mature peach trees, and found fine roots in the wetted zone, but only where the drainage was good. Roots were concentrated within a 30- to 40-cm radius, but with none under the drippers. In contrast, Goode et al. (1978b) observed 4 to 5 times more fine root, both in the vicinity of (30 cm radius) and beneath the nozzle. In the absence of irrigation, most roots were present a t 0 to 30 cm depth but with irrigation a t 0 to 60 cm depth. Away from the wetted zone there was little effect on root growth and a t 180 cm from the tree there was an apparent reduction in root density in the irrigated trees. Ponder and Kenworthy (1976) found that trickle irrigation had no effect on root system depth, but increased root weight in sugar maple, honey locust, and pin oak. The effects of trickle irrigation on apple root growth in Israel have been reviewed by Levin et al. (1980). Root distribution depended upon the volume of wetted soil, which was related to soil hydraulic conductivity and the rate and duration of water application. T h e wetted soil volume was usually 30 to 50% of the whole. T h e root system adapted to this by becoming restricted to within 60 cm of the nozzles. A higher root density in a smaller soil volume may necessitate extensive nutrient feeding. Under sprinkler irrigation 80% of the apple root system occurred a t 0 to 60 cm depth (Levin et al. 1980). They attributed this to excessive water a t depth. Root distribution a t 60 to 120 cm depth was greater when a relatively low moisture threshold was maintained in this zone during the main period of root growth. Thus, as for irrigation in general, specific systems interact with growing conditions and climate to affect response. D. Soil Management
Top fruit soil is cultivated, grassed, or treated with herbicides. Coker (1959) studied the effects of grass and cultivation on the root systems of apple trees of ‘Cox’/M 9. The general conformation of the main roots and the depth of root penetration were similar, although with grass the basic form was modified by: (1)the absence of cultivation which allowed tree roots to grow to the soil surface; (2) direct competition for water, nutrients, etc.; and (3) indirect effects on soil structure and nutrient availability. Under cultivation roots growing above 1 2 cm depth were pruned annually. In general, the spread of the root system was wider under grass, and there was more extensive branching, an increase in fine root weight, and a decrease in the larger root weight, a t all depths. Schultz (1972) also found that cultivation reduced the length of roots at 0 to 15
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cm depth. The total root surface area under cultivation and grass was similar. Mitchell and Black (1968) also found a wider distribution of peach roots under a grass sod than under cultivation. In contrast with Coker’s work, Weller (1971) found a reduced number of ‘Boskoop’/M 9 apple roots tips a t 0 to 50 cm depth under grass, compared with bare soil. T h e number of tips a t 0 to 40 cm depth was greatest under a mulch. Sechi (1975), for peach, recorded a reduced number of roots under grass, compared with cultivation, while Ghena (1965) found a deeper root distribution in plum under a cover crop. Weller (1966b) found most roots of mature ‘Boskoop’/seedling apple trees a t 0 to 50 cm under cultivation, compared with 5 to 20 for grass. A deeper root system under a cover crop has been reported by Bjorkman and Lundeberg (1971) for pine and Hill (1966) for peach. Slowik (1962) noted more roots under the cultivated alley, than under the grassed tree row in an apple orchard, although soil was generally less compact under grass (Slowik 19681, which might have been expected to encourage root growth. Goode and Hyrycz (1976) compared the effects of grass and cultivation on irrigated, unworked M 2 rootstocks which received either a heavy soil application of nitrogen fertilizer or urea sprays. Root weight was generally higher under cultivation, where the nitrogen additions had no effect. Under grass the weights of both fine and large roots were increased by supplemental fertilization, while large roots also were increased by urea sprays. Response to cultivation varies with method. Root growth in apple was increased by deep cultivation prior to planting (Druchek and Zakotin 1972) or subsoiling (Kolesnikov 1963). Bogdan (1977) compared different depths of cultivation with cultivating either part or all of the soil. T h e response varied among apple cultivars, but cultivation of only a strip or the surface alone was best. Krayushkina et al. (1977) found that with deep plowing (65 to 70 cm), 59 to 81% of the roots were a t 0 to 40 cm compared with 80 to 88% with conventional cultivation. Morettini (1974) showed that successive cultivations of peach trees had adverse effects, although the roots regrew following cultivation. Gurung (1979) found that apple root density was highest under herbicide, lowest with grass, and intermediate with cultivation. Roots a t 0 to 5 cm and 5 to 10 cm depth were abundant with herbicide and grass, but almost absent under cultivation. Similar results have been reported by Catzeflis (1972). At 0 to 20 cm depth root density was greatest under herbicide, least under cultivation, and intermediate under grass. At 20 to 40 cm herbicide again produced most roots, although numbers were similar under grass and cultivation where density was highest a t 40 to 80 cm depth. Although a grass cover eliminates mechanical damage, it competes with the trees. White and Holloway (1967) showed that 1.44 m2 herbicide-
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treated squares around newly planted trees of ‘Cox’/M 26 apple greatly increased the number of roots (1 mm diameter, compared with trees under grass, although herbicide was less effective than a mulch. However, the herbicide had little effect on distribution with depth. Atkinson and White (197613, 1980) observed that 5-year-old trees of ‘Cox’/M 26 had more roots (both < and > 2 mm diameter) under overall herbicide than under grass, with a herbicide strip treatment being intermediate. Major differences between the treatments were a t the surface. A similar increase in average root density was observed in 12-year-old trees. In contrast Farre (1979) found the root length per unit soil area of trees of ‘Cox’/M 26 to be higher under grass than under herbicide, the differences being greatest a t 50 to 80 cm depth. Subsequently, Atkinson and White (1980) showed a greater uptake of :j2Pfrom 90 cm depth by trees under grass, compared to trees under overall herbicide or a herbicide strip. In western Europe, most fruit trees are grown in weed-free strips of bare soil separated by grassed alleyways. The system presents the trees with two dissimilar environments, one with and the other without interspecific competition. The effect of this type of treatment on root distribution and nutrient uptake from the two areas has been discussed by Atkinson and White (1976a,b), Atkinson (1977), Atkinson et al. (1977, 1979), Gurung (1979), and Atkinson and White (1980). In young apple trees, root growth is higher under the herbicide strip than the grassed alley, and begins earlier in the year. As a result the majority of roots are within the herbicide strip (Atkinson and White 1976a1, which is the major zone of nutrient uptake. Four-year-old trees of ‘Cox’/M 26 apple did not absorb l5No3applied 10 cm deep in the grass alley, while young trees of ‘Cox’/MM 106 absorbed no l5NO3from 15 cm, but a little 32P04 from 25 cm depth late in the season (Atkinson 1977). As the tree ages, more use is made of the grassed alleys, although even a t 12 years (Atkinson et al. 1977, 1979) the uptake of 15N03from under the grassed alley is small compared with that from the herbicide strip. The surface soil (0 to 10 cm depth) becomes less important as the season continues and soil moisture deficits increase. Even with large mature trees of ‘Crispin’/MM 111, uptake of l5NO3from the herbicide strip was much higher than that from the grassed alley (Atkinson and White 1980). In young trees most roots are near the trunk, so little use is made of the grassed alley. The alley is exploited as the trees age, although never to the extent of the herbicide strip. This may be due to the differences in soil water potential which exist under the two management areas for most of the season. In very high density plantings where the herbicide strip becomes drier than the grassed alley, root activity, as indicated by soil moisture depletion, is stimulated under the alley (Atkinson and White 1980).
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The absence of activity under the alley is not due solely to distance from the tree. Atkinson et al. (1979) compared the uptake of 15N0, from 10 cm and 25 cm depth under the alleyway of trees under (1) overall herbicide, (2) overall grass, or (3) herbicide strip with a grassed alley. With overall herbicide there was uptake from both depths, while with the other treatments apparent root activity was limited. Gurung (1979) compared apple root density a t a number of distances from the tree under either a wide herbicide strip or overall herbicide management. H e found that mean density was higher under overall herbicide, mainly as a result of larger tree size. At most distances, but particularly 0 to 50 cm from the trunk and in mid-alley, there were more roots under total herbicide, particularly a t 0 to 10 cm depth. There were more roots a t 150 cm from the trunk in the line of the tree row in the herbicide strip than under the grassed alley. An increased number of roots under a herbicidetreated, rather than a grassed alley, has been observed by Catzeflis (1972), while a number of papers (Duperrex 1964; Mel’nik 1975; Cockroft and Wallbrink 1966; Catzeflis 1972)have reported increased root growth a t the surface. This part of the root system seems to be most sensitive to soil management treatments. Fritzsche and Nyfeler (1974) investigated the effects of sward management on apple root growth. When grass mowings were left on the soil, apple root growth was 32% higher than when mowings were removed. There was no reduction in root growth under the wheel track marks in the orchard. T h e use of mulches as part of orchard management has been widely investigated. Young apple trees under a straw mulch produced more roots, of all diameters, particularly a t 0 to 8 cm depth, than did trees under grass, herbicide, or cultivation (White and Holloway 1967). Similarly, Reckruhm (1974) found in 500 cm3 soil samples 680 mm of pear root under mulch and 580 mm under grass. Comparable values for apple were 280 mm and 240 mm. Three-year-old trees of ‘Jonathan’/seedling apple under mulch had 42% of their roots a t 0 to 30 cm compared with 27% for cultivation, and the trees were 1.8 times the size of the cultivated trees (Tamasi 1965). A mulch increased surface rooting in chestnuts (Chiba 1966) and in peaches (Hill 1966). T h e effect of pre-planting soil management on subsequent tree root growth was investigated by Gurung (1979). Root growth was better where a total herbicide regime was created by killing a grass sward, rather than from cultivation. The presence of a thin layer of straw (not a mulch) after planting improved root growth. Both effects were attributed to better rain penetration resulting from improved soil structure. Rhee (1975) found that adding worms to soil improved soil structure and increased the length of roots < 1mm and 1to 5 mm diameter by 75% and 55%, respectively .
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There have been few studies of the direct effects of weed competition on tree growth compared to the many of grass and cover crops. Bergamini (1965) grew peach trees in tubs with half of the root system bare and half covered by legumes or grass. H e found th a t legumes inhibited root growth. Atkinson and Holloway (1976) looked a t the effect of allowing a number of weeds to become established by manipulation of the herbicide program in the herbicide strip around trees of ‘Cox’/M 26 apple. T h e presence of even small annual weeds like Senecio vulgaris and Poa a n n u a reduced root activity, as indicated by the uptake of 32P a t depths from 5 to 40 cm, but particularly a t 20 cm. Atkinson and White (1980) reported th at competition from grass apparently stopped root activity in apple during a dry summer. Herbicides are of vital importance to modern soil management. There have, however, been few critical studies of their direct effects upon the root systems of trees growing under normal orchard conditions when the effects of weed competition or cultivation damage have been excluded. Gurung (1979) found th at the application of mecoprop to mature apple trees in grass did not affect total root growth, but modified root distribution. No roots were present a t 0 to 5 cm and numbers were reduced a t 5 to 10 cm. There was, however, compensating growth below this depth. With newly planted trees of ‘Cox’/MM 106 in overall grass, total root growth was reduced by mecoprop. T h e elimination of root growth near the surface might, however, improve the balance of calcium to potassium in the tree, with advantages for fruit storage (Delver and Rooyen 1972). Atkinson and Petts (1978) were able to modify the distribution of root activity in grasses (measured as water uptake) by application of growth regulators. This also would be of practical value in tree crops.
E. Planting Density and Orchard Systems Although there have been many studies of the effects of tree density on growth and cropping, and numerous evaluations of training methods, etc., there have been few studies of the impact of these on root distribution and activity. Atkinson et al. (1976) found th a t a t wider tree spacings the root system was composed mainly of horizontal roots with relatively few vertical sinkers (Fig. 9.1), but a t high densities mainly of vertical sinkers. Th e degree of intermingling of adjacent root systems increased with density of planting, while the weight, length, volume, and surface area of roots on an individual tree decreased. T h e relative density of roots in the soil, however, increased with increasing density of planting. T he root/shoot ratio was unaffected by spacing. In addition to effects on total root length, distribution with depth was changed. In a very high density planting 25% of total weight occurred below 50 cm
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depth, compared with 15% a t a wide spacing. At all depths root density increased as spacing decreased. The significance of these changes has been discussed by Atkinson (1978).Trees a t the higher planting densities made greater use of the subsoil a t a much earlier point in their lives. An appreciable number of roots occurred below 80 cm depth at the highest densities in the initial year. At the wider spacings this did not occur until year 3, a t which time as much as 75% of new growth could be found a t this depth in the higher density plantings. Although the amount and distribution of root growth were affected, the time during the year when new growth occurred was not. As a consequence of these effects upon root distribution, root activity (indicated by water absorption) occurred a t relatively greater depths in the high density plantings, and the soil moisture deficits produced a t all depths were much higher. The effect of planting density in ‘Washington’ Navel oranges has been investigated by Kaufmann et al. (1972) and Boswell et al. (1975). They found that root distribution was affected by spacing and that root density was much higher in a high density planting where, for much of the profile, actual root densities seemed close to the maximum density. Intermixing of adjacent root systems occurred only a t high densities. Kemmer (1964) also reported that spacing influenced vertical root penetration in apple, while Fraser and Gardiner (1967) found that sinkers were initiated a t an earlier stage in Sitka spruce planted a t a high density. Spacing also affected lateral extension in both species. Perstneva (1977) found a reduced weight of roots on trees of ‘Jonathan’, ‘Richared Delicious’, and ‘Mantuaner’/M 9 apple a t 4 m X 1 m, in comparison with those a t 4 m X 2.5 m; Potapov (1971) reported that 7-year-old trees of ‘Pepin Shafrannyl’ apple a t 8 m X 4 m had 40% more root per m2 than those a t 8 m X 8 m. In the higher density planting 1.4 times more root was found in the tree row than in the alleyway. Yakushev (1972) recorded an even development of roots in apple trees a t 10 m X 10 m, but a concentration in the interrow areas in trees a t 10 m X 5 m. Manzo and Nicotra (1967) also noted better pear root growth between rows and a relationship between the development in the interrow areas and the vigor of the trees in contiguous rows. This latter effect also has been reported by Atkinson and White (1980) for apple. The effect of the branch training system on the root system has been investigated for palmette grown trees. Both Nicotra (1967) and Ponomarchuk and Golovanov (1973) found that palmette trees had a normal radial root system. The way that the soil around the tree is managed and the orchard laid out obviously has a large effect upon the basic pattern of root distribution and function.
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IX. THE INFLUENCE OF ROOTSTOCK AND SCION GENOTYPE ON THE ROOT SYSTEM A. Rootstock Effects
The effects of rootstock on the root system has been reported on a number of occasions. Rogers and Vyvyan (1934) compared the root systems of apple trees on the rootstocks M 1,M 2, M 9, M 16, and OF 5. For M 9 and M 2 50% of the total weight and 75% of the fine roots were below 33 cm depth. On the more vigorous M 1 and M 16, the root systems were shallower with only 25% of total weight and 50% of the fine roots below 33 cm. The trees on the different rootstocks were planted a t different spacings, related to differences in vigor, and this may have interacted with rootstock effects. On a poor sandy soil the maximum depth of rooting was highest for OF 5 and least for M 9 and M 1. Thus, while root spread and depth can be large for trees on vigorous rootstocks (i.e., M 1 or OF 5), this is not automatically so, and the root systems of trees on dwarf stocks are not always shallow. Coker (1958) found that differences in the depth of rooting appeared only when the soil was sufficiently deep. In a deep soil, M 2 roots were more dense below 120 cm than M 1 roots, with M 9 being intermediate. Root spread was greatest for M 1,least for M 9, and intermediate for M 2. De Haas and Jurgensen (1963) compared 57 apple cultivar/rootstock combinations, and found both rootstock and scion effects on form of the root system. Rootstock also affects the depth of rooting. Ghena and Tertecel (1962) reported a deeper root system which resulted in enhanced drought resistance in apricot trees of ‘Ungarische Besle’/myrobalan than in other combinations. Weller (1965) compared the root systems of four apple cultivars on M 2, M 9, or seedling stocks. With M 9 and seedling, the main roots were horizontal; in M 2 they sloped. For seedling, 37%, 33%, 21%, and 9% of the root system were present a t 0 to 50 cm, 50 to 100 cm, 100 to 150 cm, and 150 to 200 cm depth, respectively. The corresponding values for M 2 were 5%, 48%, 28%, and 19%. In contrast, Ghena (1966) found the deepest root systems to be associated with the most vigorous stocks in several species, while Hoekstra (1968) observed no difference in the distribution of fine roots between M 4 and M 9 apple. Lupescu (1965) measured the sizes of root systems of four apricot cultivars on six rootstocks and determined the following order of vigor: ‘Rosior de Voinesti’ plum > peach > black plum > ‘Rouge de Simlev’ plum > myrobalan > seedling apricot. Tanas’ev and Balan (1977) found that M 4 had double the root weight of M 9, while Pilshchikova and Pilshchikova (1978) found differences between rootstocks in both distribution with depth and the ability to regenerate after root pruning.
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Rogers (1939) compared the periodicity of root growth in apple trees on M 1, M 9, and M 16. H e found little difference in the appearance of individual roots, but M 16 reached peak production more quickly, its distribution of new growth was deeper, and its rate of root browning slower. There were no clear differences among stocks in the rates of growth of individual roots, so differences in root density must have been due to the number of roots developing. Gurung (1979), using ‘Cox’ apple on several rootstocks, found that root growth was generally most vigorous with the stronger stocks, i.e., M M 106 and M M 111greater than M 9 and M 27, with M 26 intermediate. However, in both years of his study M M 106 produced more root than the more vigorous M M 111. Differences in the periodicity of root growth also were apparent, with the stronger stocks showing more growth in the autumn and in distribution with depth, as M M 106 had most growth a t 30 to 50 cm. Various plum and cherry stocks also differ in periodicity of growth (Atkinson and Wilson 1980). Atkinson (1973d) observed that uptake of 32Pper unit weight of root was greater in stocks of M M 111 than in those of M 9 or M 26. Thus, with rootstocks, root system size, distribution, periodicity of growth, and activity appear to be potentially variable.
B. Scion Cultivar Effects Although the choice of scion can influence tree size, few studies have addressed scion effects on the root system. However, scion cultivar has been shown to affect root system form in plum (Ghena 1964a), and root density in apple (Weller 1965), both maximum depth and lateral root spread (Angelov 1976), and formation of fibrous roots (Kemmer 1964) in apple. Head (1966) compared the periodicity of root growth of trees of ‘Crawley Beauty’ and ‘James Grieve’/M 7 which differed greatly in time of bud burst. H e found little difference, although the onset of growth was slightly earlier in the earlier flowering ‘James Grieve’. Atkinson (1973e) compared the root growth of ‘Cox’ and ‘Golden Delicious’/M 9 a t a range of planting densities. H e found only small differences between cultivars, although root growth by ‘Delicious’ seemed to be relatively better a t high densities. Variation in the choice of a scion cultivar may thus affect the root system, although available examples suggest it as having less effect than the rootstock. X. ROOT-SHOOT INTERACTIONS
Rogers and Vyvyan (1934) estimated the ratio of root to shoot (R/S) for ll-year-old trees of ‘Lanes’ Prince Albert’ on M 1, M 2, M 9,and
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M 16 to be 0.5 to 0.4 for a loam soil and 1.0 to 1.4 for a sandy soil. For 16-year-old trees of ‘Cox’/M 9, Coker (1959) gave values of 0.36 to 0.42. For 5-year-old trees of ‘Golden Delicious’/M 9, Atkinson et al. (1976) found a value of 0.13 to 0.16 irrespective of spacing. These lower values may be due to age or to improved cultural conditions. Avery (1970) and Tamasi (1965), however, noted a tendency for R / S to increase with increasing age. For l-year-old trees of ‘Worcester’/M 26, R / S was 0.26, while for 4-year-old trees it was 0.5 (Avery 1970).Comparable values for trees of ‘Worcester’/3430 were 0.30 and 0.59. Avery (1970) found R/S to range from 0.15 (1-year-old ‘Worcester’/M 2) to 0.59 (4-year-old ‘Worcester’/3430). Rootstock also affected R / S with ratios highest for 3430 and lowest for M 2. A comparison of Coker’s (1959) data with that of Atkinson et al. (1976) suggests that R / S changed as a result of changes in cultural practice, i.e., the use of herbicides. Atkinson and White (1976b) showed that R / S was highest for trees under grass and lowest for those under total herbicide. Atkinson and White (1980) have suggested that this relative reduction in root length may partially explain the reduced uptake of phosphorus under total herbicide management trees, i.e., root systems adapted to favorable water supply have an inadequate length of root available for phosphorus uptake, which depends greatly on root surface area. The amount of root extracted from soil has varied with investigator. Although values may be comparable within one study, comparison of the values resulting from different studies is difficult. Cripps (1971) studied the effects of moisture stress, fluctuating soil moisture availability, and waterlogging on R/S. All increased R / S and reduced the total growth of trees of ‘Granny Smith’/MM 115 apple. Gur, Hepner and Mizrahi (1976) found that R/S decreased with an increasing soil temperature. R / S seems likely to increase when trees are in a stress situation. For a range of herbaceous plants, Atkinson (1973f) showed that R / S increased progressively with increasing phosphorus and nitrogen deficiencies. Atkinson and Davison (1973) found that the change in R / S was closely correlated with the reduction in growth produced by nutrient stress. In annual plants, where most of the root and shoot tissue is active in either synthesis or absorption, R / S is related to the balance of activity between root and shoot. Hunt (1975) showed a close relationship between the mass ratio of root and shoot and their activity ratios calculated as: specific absorption rate for potassium (pg K mg root - 1 day - I ) / unit shoot rate (increase in plant weight per unit shoot weight (mg mg - l day -’)). The importance for peach trees in this type of situation has been discussed by Richards (1976) and Richards and Rowe (1977). They showed that the change in plant weight was related to the amount of water
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absorbed by the roots. For a given decrease in R/S there was a n increase in water uptake per unit length of root, indicating that the root system has the capacity to increase uptake as demand increases. They also showed that leaf area was related to water uptake, plant weight to nutrient uptake (in a similar way to water uptake), and leaf number to root number. As a result, shoot demand appeared to control the uptake of many substances. T h e above experiments, however, were conducted on small plants which, in functional terms, approximate annual plants. Using data for root length (Atkinson et al. 1976) and for leaf areas of the same trees (Atkinson 1978), the ratio leaf area (cm')/root length (cm) can be calculated for trees growing a t a range of densities. Values of 1.3 to 1.7 are obtained for trees with leaf area indexes (LAI) of < 1.3. For high density plantings where LA1 is 5.8 to 9.7, comparable values are 2.1 to 3.4. Assuming that a LA1 of only 2 is functional in orchard light interception, i.e., it intercepts most of the available light, these values become 0.4 to 1.2. This implies that in very high density plantings twice the length of root is needed to supply a given amount of evaporative surface. This may be related to the rapid depletion of soil water near the soil surface in trees a t very high densities (Atkinson 1978), which probably makes much of the root system non-functional. Variation in the ratio of leaf area/root length occurs where R/S is constant and it may be, therefore, a more realistic appraisal of activity in trees where much tissue has no synthetic or absorptive activity. Clearly, additional information is needed about the control of the relative amounts of growth and activity in the root and the shoot, and their interrelationships. XI. CONCLUSIONS
Although there are many basic similarities in the root systems of tree crops with respect to patterns of growth, timing, and distribution of growth, and the ways in which they function, there are also major differences. These can arise from genetic variation in the planting material, but also can be brought about by cultural factors, i.e., practices which we can control. To make best use of both of these sources of variation, greater understanding of relationships among root growth, density, and effectiveness is needed. Many of the studies reported here were purely observational and as such often provide little understanding of mechanisms of activity and effectiveness. Based on observed effects, studies of root function in relation to internal metabolic and external factors are needed to raise our understanding of the tree root system to a level already available for many annual and field crops.
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XII. LITERATURE CITED ABRAMENKO, N.F. 1977. Seasonal rhythm of root growth of apple trees in hilly unirrigated orchards (in Russian). Vest. S K h Naoki Katah. 3:58-60. ADDOMS, R.M. 1946. Entrance of water into suberized roots of trees. Plant Physiol. 2 1:109-111. AIYAPPA, K.M. and K.C. SRIVASTAVA. 1965. Studies on root system of Coorg Mandarin seedling trees. Indian J. Hort. 22:122-130. ANDREWS, R.E. and E.I. NEWMAN. 1970. Root density and competition for nutrients. Ecologia Plant. 5:319-334. ANGELOV, T . 1976. Root system distribution in bearing apple trees and methods of irrigation (in Bulgarian). Ovoshcharstvo 55:33-37. ATANASOV, G. 1965. The distribution of the root system of the Kazanlik rose (Rosa damascena Mill.) in diluvial meadow and leached cinnamon forest soils (in Bulgarian). Rasten. Nauki 2:lOl-108. ATKINSON, D. 1972. Seasonal periodicity of black currant root growth and the influence of simulated mechanical harvesting. J. Hort. Sci. 47:165-172. ATKINSON, D. 1973a. T h e root system of Fortune/M 9. Rpt. East Malling Res. Sta. for 1972. p. 72-78. ATKINSON, D. 1973b. Field studies on root systems and root activity. Rpt. East Malling Res. Sta. for 1972. p. 56-58. ATKINSON, D. 1973c. Seasonal changes in the length of white unsuberized root on raspberry plants grown under irrigated conditions. J. Hort. Sci. 48: 413-419. ATKINSON, D. 1973d. Structure and physiology of individual roots and root systems. Rpt. East Malling Res. Sta. for 1972. p. 56. ATKINSON, D 1973e. Root competition in tree spacing experiments. Rpt. East Malling Res. Sta. for 1972. p. 58-59. ATKINSON, D. 1973f. Some general effects of phosphorus deficiency on growth and development. New Phytol. 72:lOl-111. ATKINSON, D. 1974a. Field studies on root systems and root activity. Rpt. East Malling Res. Sta. for 1973. p. 69. ATKINSON, D. 1974b. Some observations on the distribution of root activity in apple trees. P l a n t & Soil 40:333-342. ATKINSON, D. 1976. Preliminary observations on the effect of spacing on the apple root system. Sci. Hort. 4:285-290. ATKINSON, D. 1977. Some observations on the root growth of young apple trees and their uptake of nutrients when grown in herbicide strips in grassed orchards. Plant & Soil 49:459-471. ATKINSON, D. 1978. The use of soil resources in high density planting systems. Acta Hort. 65:79-89. ATKINSON, D. and A.W. DAVISON. 1973. The effects of phosphorus deficiency on water content and response to drought. New Phytol. 72:307-313. ATKINSON, D. and R.F. HERBERT. 1979. A review of long-term effects of
476
HORTICULTURAL REVIEWS
herbicides-effects on the soil with particular reference to orchard crops. A n n . Appl. B i d . 91:125-146. ATKINSON, D. and R.I.C. HOLLOWAY. 1976. Weed competition and the performance of established apple trees. Proc. 1976 British Crop Prot. Conf.Weeds 1:299-304. ATKINSON, D., M.G. JOHNSON, D. MATTAM, and E.R. MERCER. 1979. Effect of orchard soil management on the uptake of nitrogen by established apple trees. J. Sci. Food & Agr. 30:129-135. ATKINSON, D. and J.K. LEWIS. 1979. Time-lapse cinematographic studies of fruit trees root growth. J. Photogr. Sci. 27~253-257. ATKINSON, D., J.K. LEWIS, and E.Y. JONES. 1977. Time-lapse cinematographic studies of root growth using an underground observation laboratory. Zesz. Probl. Postep. Nauk Roln. 188:293-301. ATKINSON, D., D. NAYLOR, and G.A. COLDRICK. 1976. The effect of tree spacing on the apple root system. Hort. Res. 16:89-105. ATKINSON, D. and S.C. PETTS. 1978. Effect of the chemical management of orchard swards on the use of water and mineral nutrients. Proc. 1978 British Crop Prot. Conf-Weeds 1:223-230. ATKINSON, D. and G.C. WHITE. 1976a. The effect of the herbicide strip system of management on root growth of young apple trees and the soil zones from which they take up mineral nutrients. Rpt. East Malling Res. Sta. for 1975. p. 165-167. ATKINSON, D. and G.C. WHITE. 1976b. Soil management with herbicides: the response of soils and plants. Proc. 1976 British Crop Prot. Conf-Weeds 3:873-884. ATKINSON, D. and G.C. WHITE. 1980. Some effects of orchard soil management on the mineral nutrition of apple trees. p. 241-254. In D. Atkinson, J.E. Jackson, R.O. Sharples, and W.M. Waller (eds.) The mineral nutrition of fruit trees. Butterworths, Borough Green, U.K. ATKINSON, D., G.C. WHITE, J.M. FARRE, E.R. MERCER, M.G. JOHNSON, and D. MATTAM. 1977. The distribution of roots and the uptake of nitrogen by established apple trees grown in grass with herbicide strips. Rpt. East Malling Res. Sta. for 1976. p. 183-185. ATKINSON, D. and S.A. WILSON. 1979. The root soil interface and its significance for fruit tree roots of different ages. p. 259-271. In J.L. Harley and R.S. Russell (eds.) T h e soil root interface. Academic Press, London. ATKINSON, D. and S.A. WILSON. 1980. The growth and distribution of fruit tree roots: some consequences for nutrient uptake. p. 259-272. In D. Atkinson, J.E. Jackson, R.O. Sharples, and W.M. Waller (eds.) The mineral nutrition of fruit trees. Butterworths, Borough Green, U.K. AVERY, D.J. 1970. Effects of fruiting on the growth of apple trees on four rootstock varieties. New Phytol. 69:19-30. BABAEV, B.G. 1968. The roots of apple trees on unirrigated plots (in Russian). Sadovodstvo 12:18.
DISTRIBUTION AND EFFECTIVENESS OF T R E E ROOTS
477
BABUK, V.I. 1971. The effect of tree age on the development of the root system, growth, productivity of apple trees (in Russian). Trudy Kishineu. Sel’kokh. Inst. 81:70-76. BERGAMINI, A. 1965. The influence of some herbaceous species on peach root distribution (in Italian). Atti Congr. Pesco Verona 1965. p. 3. BESPECALNAJA, V.V. and V.K. SMYKOV. 1965. The drought resistance of apricots in relation to the characteristics of its root system (in Russian). Sadou. Vinog. i Vinod. Mold. 7:12-15. BHAR, D.S., G.F. MASON, and R.J. HILTON. 1970. In situ observations on Hort. Sci. 95:237-239. plum root growth. J. Arner. SOC. BILAN, M.V. 1971. Some aspects of tree root distribution. p. 69-80. In E. Hacskaylo (ed.) Mycorrhizae. Misc. Publ. USDA Forest Service. BJORKMAN, E. and G. LUNDEBERG. 1971. Studies of root competition in a poor pine forest by supply of labelled nitrogen and phosphorus. Studia Forest a k a Suecica 94:16. BOGDAN, G.K. 1977. The growth of the apple tree root system in relation to pre-planting soil preparation (in Russian). Soderzh i Vdobrpochvy u Plodou Nasazhdemiyakh Kishineu Moldavian SSR 47-56. BOHM, W. 1974. Mini-rhizotrons for root observations under field conditions. Z. Acker und Pflanzenbau 140:282-287. BOHM, W. 1979. Methods of studying root systems. Springer-Verlag, Berlin. BOSWELL, S.B., C.D. MCCARTY, and L.N. LEWIS. 1975. Tree density affects large root distribution of ‘Washington’ Navel orange trees. HortScience 10:593-595. BRASE, K.D. and R.D. WAY. 1959. Rootstocks and methods used for dwarfing fruit trees. N. Y State Agr. Expt. Sta. (Geneva) Bul. 783. BREWSTER, J.L. and P.B. TINKER. 1972. Nutrient flow rates into roots. Soil & Fert. 351355-359. BROESHART, A. and D.A. NETHSINGHE. 1972. Studies on the pattern of root activity of tree crops using isotope techniques. p. 453-463. I n Isotopes and radiation in soil plant relationships including forestry. IAEA, Vienna. BULATOVIC, S. and P. LUCIC. 1972. The effect of moisture and temperature of soil on dynamics of root growth of P r u n u s cerasifera Ehrh. and cv. Pozegaca. J Yugoslav Pornol. 19:469-482. BZIAVA, M.L. 1966. The development of the tea plant root system in relation to fertilizers (in Russian). Subtrop. Kultury 3:3-17. CAHOON, G.A. and L.H. STOLZY. 1959. Estimating root density and distribution in citrus orchards by the neutron moderation method. Proc. Amer. SOC. Hort. Sci. 74:322-327. CAHOON, G.A. and L.H. STOLZY. 1966. Cultural practices change citrus root systems Calif Citrogr. 51:463-466. CARSON, E.W. 1974. The plant root and its environment. The University Press of Virginia, Charlottesville.
478
HORTICULTURAL REVIEWS
CATZEFLIS, J. 1972. Studies on root growth in apple (in French). Revue Suisse Vitic. Arbor. Hort. 4 (3):107-110. CHALMERS, D.J. and B. VAN DEN ENDE. 1975. Productivity of peach trees: factors affecting dry weight distribution during tree growth. Ann. Bot. 39:423-432. CHIBA, T. 1966. Studies on orchard soil management and on the nutrient status, growth, yield and root distribution of chestnut trees under different soil management systems. Bul. Hort. Res. Sta., Hiratsuka, Ser. A 5:l-37. CLARKSON, D.T. 1974. Ion transport and cell structure in plants. McGrawHill, London. CLARKSON, D.T., A.W. ROBARDS, J. SANDERSON, and C.A. PETERSON. 1978. Permeability studies on epidermal-hypodermal sleeves isolated from roots of Alliurn cepa (onion). Can. J. Bot. 56:1526-1532. CLARKSON, D.T. and J. SANDERSON. 1971. Relationship between the anatomy of cereal roots and the absorption of nutrients and water. Rpt. ARC Letcombe Lab. for 1970. p. 16-25. CLARKSON, D.T., J. SANDERSON, and R.S. RUSSELL. 1968. Ion uptake and root age. Nature (London) 220:805-806. COCKROFT, B. and J.C. WALLBRINK. 1966. Root distribution of orchard trees. Austral. J. Agr. Res. 17:49-54. COKER, E.G. 1958. Root studies. XII. Root systems of apple on Malling rootstocks on five soil series. J. Hort. Sci. 33:71-79. COKER, E.G. 1959. Root development of apple trees in grass and clean cultivation. J. Hort. Sci. 34:lll-121. COPELAND, O.L. 1952. Root mortality of short leaf and loblolly pine in relation to soils and little leaf disease. J. For. 50:21-25. COUTTS, M.P. and J.J. PHILIPSON. 1976. The influence of mineral nutrition on the root development of trees. I. The growth of Sitka spruce with divided root systems. J. Expt. Bot. 27:1102-1111. COUTTS, M.P. and J.J. PHILIPSON. 1977. The influence of mineral nutrition on the root development of trees. 111. Plasticity of root growth in response to changes in the nutrient environment. J. Expt. Bot. 28:1071-1075. CRIPPS, J.E.L. 1971. The influence of soil moisture on apple root growth and root:shoot ratios. J. Hort. Sci. 46:121-130. DANOV, G.A., V.I. ABROSIMOV, and D.M. MUSAEV. 1967. Root growth in apples (in Russian). Sadouodstuo 6:17. DE HAAS, P.G. and C. JURGENSEN. 1963. Studies on the form of the root system of apple trees in peat soil (in German). Gartenbauwissenschaft 28: 65-94. DELVER, P. and W.J. VAN ROOYEN. 1972. Should we cultivate tree rows again? Fruitteelt 62:412-415. DIASAMIDZE, SH. S.and M.G. SOZIASHUITI. 1976. Roots of Reinette de Champagne and London Pippin on clonal rootstocks (in Russian). T r u d y Inst. Sadou. Vinogr. i Vinod. Gruz S S R 1975. 24:199-200.
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
479
DOCHEV, D.M., D.V. DONCHEV, and V. BELYAKOV. 1974. Investigations on apple irrigation. 11. The influence of overhead sprinkler irrigation on certain plant growth characteristics and leaf mineral composition (in Bulgarian). Grad. i Lozar Nauka 11:3-10. DOICHEV, K. 1977. Root distribution of M.7 clonal apple rootstocks grafted with Golden Delicious as affected by different methods and rates of irrigation (in Bulgarian). Grad. Lozar. Nauka 14:19-24. DRUCHEK, A.A. and V.S. ZAKOTIN. 1972. The formation of the apple tree root system in relation to pre-planting soil preparation (in Russian). Voprosy In tensifi ha tsii Sel kko k hozyaistvennogo Proizuodstua, Moscow. 141- 144. DUDNEY, P.J. 1972. On the estimation of root biomass in a growth pattern experiment on apples. Rpt. East Mulling Res. Sta. for 1971. p. 66-67. DUPERREX, H. 1964. Observations on the rooting of black currants (in French). Agr. Romande, Ser. A 3:32. DZHAVAKYANTS, ZH. L. 1971. Growth changes in the apple root system (in Russian). Uzbek. Biol. Zh. 6:29-31. DZILJANOV, L. and M. PENKOV. 1964a. The influence of soil conditions on the location and development of the root system of almond trees (in Bulgarian). Grad. Lozar. Nauka 1:29-37. DZILJANOV, L. and M. PENKOV. 1964b. The distribution of the fibrous roots of peach trees grown on different soils (in Bulgarian). Grad. Lozar. Nauka 1:9-18. ENGLER, A. 1903. Examination of the root growth of different species (in German). Mitt. Schweiz. Centralanstalt Forst. Versuchswes. 7:247-272. FARRE, J.M. 1979. Water use and productivity of fruit trees: effects of soil management and irrigation. Ph.D. Thesis, University of London. FAUST, M. 1980. Interaction between nutrient uptake and photosynthesis. p. 193-199. I n D. Atkinson, J.E. Jackson, R.O. Sharples, and W.M. Waller (eds.) The mineral nutrition of fruit trees. Butterworths, Borough Green, U.K. FAYLE, D.C.F. 1975. Distribution of radial growth during the development of red pine root systems. Can. J. For. Res. 5:608-625. FERGUSON, I.B. and D.T. CLARKSON. 1975. Ion transport and endodermal suberization in the roots of Zea mays. New Phytol. 75:69-79. FORD, E.D. and J.D. DEANS. 1977. Growth of a Sitka spruce plantation: spatial distribution and seasonal fluctuations of lengths, weights and carbohydrate concentrations of fine roots. Plant & Soil 47:463-485. FORDHAM, R. 1972. Observations on the growth of roots and shoots of tea (Camellia sinensis L.) in Southern Malawi. J. Hort. Sci. 47:221-229. FRASER, A.I. and J.B.H. GARDINER. 1967. Rooting and stability in Sitka spruce. Forestry Comm. Bul. 40. FRITZSCHE, R. and A. NYFELER. 1974. The influence of soil cultivation on the development and activity of apple tree roots (in German). Schweiz. Landw. Forsc h. 13 :34 1- 35 1. GHENA, N. 1964a. Studies on the structure of the root systems of apple, pear,
480
HORTICULTURAL REVIEWS
apricot and sweet cherry trees grown on a degraded cheonozem soil a t Istrita (in Romanian). Lucr. Stiint. Inst. Agron. N. Balcescu Hort. Ser. B 7:37-45. GHENA, N. 196413. A study of the root systems of plum trees grown in reddishbrown forst soil a t Baneasa (in Romanian). Lucr. Stiint. Inst. Agron. N. Balcescu Hort. Ser. B 7:29-36. GHENA, N. 1965. The structure of apple and plum root systems in brown podsol soils (in Romanian). Lucr. Stiint. Inst. Agron. N. Balcescu Hort. Ser. B 8:37-48. GHENA. N. 1966. Contributions to the study of the behaviour of the root system of some species of fruit trees (in Romanian). Lucr. Stiint. Inst. Agron. N. Balcescu Hort. Ser. B 9:47-74. GHENA, N. and M.A. TERTECEL. 1962. Contributions to the study of the root system of the apricot tree (in Romanian). Lucr. Stiint. Inst. Agron. N Balcescu Hort. Ser. B 6:317-327. GOFF, E.S. 1897. Study of roots of certain perennial plants. Wise. Agr. Expt. Sta. Rpt. 14:286-298. GOLIKOVA, N.A. and V.I. GRACHEV. 1973. Characteristics of root growth in regularly and irregularly bearing apple trees (in Russian). Nauch. Trudy, Voron. Selkhohh. Inst. 55:105-110. GOODE, J.E., K.H. HIGGS, and K.J. HYRYCZ. 1978a. Nitrogen and water effects on the nutrition growth, crop yield and fruit quality of orchard grown Cox’s Orange Pippin apple trees. J. Hort. Sci. 53:295-306. GOODE, J.E., K.H. HIGGS, and K.J. HYRYCZ. 1978b. Trickle irrigation of apple trees and the effect of liquid feeding with NO -:{ and K + compared with normal manuring. J. Hort. Sci. 53:307-316. GOODE, J.E. and K.J. HYRYCZ. 1964. T h e response of Laxton’s Superb apple trees to different soil moisture conditions. J. Hort. Sci. 39:254-276. GOODE, J.E. and K.J. HYRYCZ. 1970. T h e response of black currants to different soil moisture conditions and two levels of nitrogenous fertilizer. J. Hort. Sci. 45:379-391. GOODE, J.E. and K.J. HYRYCZ. 1976. T h e effect of nitrogen on young newly planted apple rootstocks in the presence and absence of grass competition. J . Hort. Sci. 51:321-327. GRAHAM, J., D.T. CLARKSON, and J. SANDERSON. 1974. Water uptake by the roots of marrow and barley plants. Rpt. ARC Letcombe Lab. for 1973. p. 9-12. GREENHAM, D.W.P. 1976. T h e fertilizer requirements of fruit trees. Proc. Fert. Soc. 157:l-32. GUR, A., J. HEPNER, and Y. MIZRAHI. 1976. T h e influence of root temperature on apple trees. I. Growth responses related to the application of potassium fertilizer. J. Hort. Sci. 51:181-193. GUR, A., Y. MIZRAHI, and R.M. SAMISH. 1976. T h e influence of root temperature on apple trees. 11. Clonal differences in susceptibility to damage caused by supraoptimal root temperature. J. Hort. Sci. 51:195-202. GURUNG, H.P. 1979. T h e influence of soil management on root growth and
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
481
activity in apple trees. M.Phil. Thesis, University of London. HAAS, P.G., D E and K. HEIN. 1973. T h e effect of various pruning measures and defoliation on the growth of apple roots (in German). Erwebsobstbau 1 5 (9):137-141. HANSEN, P. 1972. Some effects of ringing, defoliation, sorbital spraying and bending of shoots on the rate of translocation on accumulation and on growth in apple trees. Tidsskr. Planteao. 76:308-315. HARLEY, .J.L. and R.S. RUSSELL. 1979. T h e soil-root interface. Academic Press, London. HARRISON-MURRAY, R.S. and D.T. CLARKSON. 1973. Relationships between structural development and the absorption of ions by the root system of Cucurbita p ~ p o Planta . 114:l-16. HEAD, G.C. 1964. A study of exudation from the root hairs of apple roots by time-lapse cinephotomicrography. Ann. Bot. 28:495-498. HEAD, G.C. 1965. Studies of diurnal changes in cherry root growth and nutational movements of apple root tips by time-lapse cinematography. Ann. Bot. 29:219-224. HEAD, G.C. 1966. Estimating seasonal changes in the quantity of white unsuberized root on fruit trees. J. Hort. Sci. 41:197-206. HEAD, G.C. 1967. Effects of seasonal changes in shoot growth on the amount of unsuberized root on apple and plum trees. J. Hort. Sci.42:169-180. HEAD, G.C. 1968a. Studies of growing roots by time-lapse cinematography. Proc. I X Intern. Congr. Soil Sci. 1:751-758. HEAD, G.C. 196813. Seasonal changes in the diameter of secondarily thickened roots of fruit trees in relation to growth of other parts of the tree. J. Hort. Sci. 43:275-282. HEAD, G.C. 1968c. Seasonal changes in the amounts of white unsuberized root on pear trees on quince rootstock. J. Hort. Sci. 43:49-58. HEAD, G.C. 1969a. The effects of fruiting and defoliation on seasonal trends in new root production on apple trees. J. Hort. Sci. 44:175-181. HEAD, G.C. 1969b. The effects of mineral fertilizer on seasonal changes in the amount of white root on apple trees in grass. J . Hort. Sci. 44:183-187. HEAD, G.C. 1970. Methods for the study of production in root systems. p. 151157. I n Methods of study in soil ecology. UNESCO, Paris. HEAD, G.C. 1973. Shedding of roots. p. 237-293. I n T.T. Kozlowski (ed.) Shedding of plant parts. Academic Press, New York. HILL, R.G. 1966. Relationship of soil management practices and nitrogen fertilizations to the root distributions of the peach. Proc. 17th Intern. Hort. Congr., Maryland 1:24. HILTON, R.J. 1979. Root growth a t the Guelph Rhizotron. In A. Riedacker and J. Gagnaire-Michard (eds.) Root physiology and symbiosis. Proc. IUFRO Symp. Sept. 11-15, 1978, CNRF. Nancy, France. p. 135-142. HILTON, R.J. and H. KHATAMIAN. 1973. Diurnal variation in elongation rates of roots of woody plants. Can. J. Plant Sci. 53:699-700.
482
HORTICULTURAL REVIEWS
HOEKSTRA, C. 1968. Fruit growing on holdings with a marked variation in soil suitability (in Dutch). Fruitteelt 58:482-484. HORSLEY, S.B. and B.F. WILSON. 1971. Development of the woody portion of the root system of B d u l a papyrifera. Arner. J. Bot. 58:141-147. HUCK, M.G., B. KLEPPER, and H.M. TAYLOR. 1970. Diurnal variations in root diameter. Plant Physiol. 45:529-530. HUGUET, .J.G. 1973. New method of studying the rooting of perennial plants by means of a spiral trench (in French). A n n . Agron. 24:707-731. HUGUET, J.G. 1976. Influence of a localized irrigation on the rooting of young apple trees (in French). A n n . Agron. 27:343-361. H U N T , R. 1975. Further observations on root-shoot equilibria in perennial rye grass (Loliurn perenne L.). A n n . Bot. 39:745-755. HUXLEY, P.A., R.Z. PATEL, A.M.KABAARA, andH.W.MITCHELL. 1974. Tracer studies with 3*P on the distribution of functional roots of Arabica coffee in Kenya. A n n . Appl. Biol. 77:159-180. TGLANOV, Y.K. 1976. Dynamics of growth of active apricot roots (in Russian). Izv An Turkrn S S R Biol N a u k 5:29-32. INFORZATO, R. and A.M. DE CARVALHO. 1967. A study on the paw paw root system in the type of podsolized soil found in the Marilia area of Brazil. Braga n t ia 26: 155- 159. INFORZATO, R. and A.J. REIS. 1963. A comparative study of root systems in the coffee varieties Yellow Bourbon and Mundo Novo (in Spanish). Bragantia 22~741-750. JACOBONI, N. and A. CARTECHINI. 1964. A contribution to the study of the Hazel root system in the Cimini region (in Italian). Annuli Fac. Agr. Uniu. Per ugia 19 :32 3- 34 8. KAIROV, A.K., M.N. FISUN, and KH. ZH. BALKAROV. 1977. T h e root systems of fruit trees on terraced slopes (in Russian). T r u d y Kabardino Balkaropyt st Sadovodstua 1:254-258. KATZFUSS, M. 1973. Growth and distribution of I4C in five apple cultivars during one vegetation period (in German). Arch. Gartenb. 21:637-651. KAUFMANN, M.R., S.B. BOSWELL, and L.N. LEWIS. 1972. Effect of tree spacing on root distribution of 9-year-old ‘Washington’ Navel oranges. J. Arner. Soc. Hort. Sci. 97:204-206. KEMMER, E. 1964. Root systems of apple trees as affected by various dominating factors (in German). Zuchter 34:59-67. KNIGHT, R.C. 1934. T h e influence of winter stem pruning on subsequent stem and root development in apple. J. Pornol. 12:l-14. KNIGHT, R.L. 1961. Taper and secondary thickening in stems and roots of the apple. Rpt. East Mulling Res. Sta. for 1960. p. 65-71. KOCHENDERFER, J.N. 1973. Root distribution under some forest types native to West Virginia. Ecology 54 (2):445-448. KOLESNIKOV, V.A. 1963. T h e size and distribution of the apple tree root system as affected by various factors (in Russian). Izu. Tirniryazeu. Sel ’hokh. Ahad. p. 85-100.
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
483
KOLESNIKOV, V.A. 1966. The interrelationship between the aerial portion and the root system of fruit trees (in Russian). Vestnik Sel’ kokh. N a u k i 11:46-51. KOLESNIKOV, V.A. 1968. Cyclic renewal of roots in fruit plants. p. 102-105. I n M.S. Ghilarov, V.A. Kovda, L.N. Novichkova-Juanova, L.E. Rodin, and V.M. Sveshnikova (eds.) Methods of productivity studies in root systems and rhizosphere organisms. Nauka, Leningrad. KOLESNIKOV, V.A. 1971. The root system of fruit plants. MIR Publishers, Moscow. KOSELEVA, R.V. 1962. The structure and dynamics of root growth and the above ground parts of apple trees in the conditions of the Kopet Dag region of the Turkmen SSR. Abstract of Dissert. Acad. Sci. Turkmen SSR. KOVAL, A.T. 1977. Root system of vegetatively propagated rootstocks (in Russian). Sadouod. Vinogr. i Vinod. Mold. 5:33-35. KRAYUSHKINA, N.S., L.P. SOITU, and V.I. DADYKO. 1977. The effect of methods of pre-planting soil preparation on soil physiochemical properties and distribution of apple tree roots (in Russian). Ovoshchevodstvo Sadovodstvo i Tsvetovodstvo V Seu Zap RSFSR, Leningrad, USSR 176-186. KRAMER, P.J. and H.C. BULLOCK. 1966. Seasonal variations in the proportions of suberized and unsuberized roots of trees in relation to the absorption of water. Amer. J. Bot. 53:200-205. KRASNOSHTAN, A.A. 1975. Growth of the root system of semi-dwarf apple trees in relation to different mineral nutrition (in Russian). Navchnye T r u d y Ukrainskoi S-Kh Akademii 15333-76. KRYSANOV, JU. V. 1969. The root system of apples on paradise (in Russian). Sadovodstuo 1:16. LANDSBERG, J.J. and N.D. FOWKES. 1978. Water movement through plant roots. A n n . Bot. 42:493-508. LEVIN, I., R. ASSAF, and B. BRAVDO. 1980. Irrigation water status and nutrient uptake in an apple orchard. p. 255-264. I n D. Atkinson, J.E. Jackson, R.O. Sharples, and W.M. Waller (eds.) The mineral nutrition of fruit trees. Butterworths, Borough Green, U.K. LUCHTOV, P.G. 1971. Growth and distribution of apple roots on terraces (in Russian). Sadovodstvo 10:12-13. LUCIC, P. 1967. The growth of the root system of the pear, Pirus communis var. siluestris, under different illumination of the assimilation organs. Contemp. Agr. -Novi Sad 15:31-37. LUPESCU, F. 1961. A study of the structure of the root system of the apricot variety Paviot grafted on various rootstocks (in Romanian). Lucr. Stiint. Inst. Agron. N. Balcescu Hort. Ser. B 5:231-245. LUPESCU, F. 1965. Contributions to the study of the root systems of some apricot varieties grafted on different rootstocks (in Romanian). Lucr. Stiint. Inst. Agron. N . Balcescu Hort. Ser. B 8:lOl-110. LYR, H. and G. HOFFMANN. 1967. Growth rates and growth periodicity of tree roots. Intern. Rev. For. Res. 2:181-236.
484
HORTICULTURAL REVIEWS
MACKENZIE, K.A.D. 1979. The development of the endodermis and phi layer of apple roots. Protoplasma 100:21-32. MANZO, P. and A. NICOTRA. 1967. Studies on pear root systems (in Italian). Riu. Ortoflorofru ttic. Ital. 5 1:224-232. MASON, G.F., D.S. BHAR, and R.J. HILTON. 1970. Root growth studies on mugho pine. Can. J. Bot. 48:43-47. MEL’NIK, N.M. 1975. Apple tree roots and herbicide treatment (in Russian). Sadouodstuo 5:19-20. MILANOV, B. 1977. The root system of pear trees on Quince A rootstocks trained by the palmette or improved tree system (in Bulgarian). Grad. Lozar. N a u k a 14:37-43. MIRCETICH, S.M., W.R. SCHREADER, W.J. MOLLER, and W.C. MICKE. 1976. Root and crown rot of cherry trees. Calif. Agr. 3O:lO-11. MITCHELL, P.D. and J.D.F. BLACK. 1968. Distribution of peach roots under pasture and cultivation. Austral. J . Expt. Agr. An i m . Husb. 8:106-111. MOLCANOV, E.F. 1966. The formation of root systems on calcareous soils (in Russian). Sadouodstuo 12:13-14. MORETTINI, A. 1974. Regeneration of the peach root system in the cultivated soil layer (in Italian). Riu. Ortoflorofruttic. Ital. 58:25-33. MOSSE, B. 1957. Growth and chemical composition of Mycorrhizal and nonMycorrhizal apples. Nature (London) 179:92%-924. MURSALOV, M.K. 1966. The growth of quince roots in Dagestan (in Russian). Sadouods t uo 2: 14. NETHSINGHE, D.A. 1966. The application of isotopes in fertilizer research on the coconut palm. Ceylon Coconut Q. 17:61-72. NETHSINGHE, D.A. 1970. The validity of assumptions and control of errors in using the 32Psoil injection technique for studying the root activity of trees. Rpt. FAO/IAEA Mtg. Use of Isotopes to Study the Efficient Use of Fertilizers in Tree Culture, Vienna, January 1970. NETHSINGHE, D.A., D.A. RENNIE, and P.B. VOSE. 1968. Radiotracers in tree culture. Agr. Chem., November 1968. p.18-20. NEWMAN, E.I. 1969. Resistance to water flow in soil and plant. I. Soil resistance in relation to amounts of roots: theoretical estimates. J . Appl. Ecol. 6:l-12. NEWMAN, E.I. and R.E. ANDREWS. 1973. Uptake of phosphorus and potassium in relation to root growth and root density. Plant & Soil 38:49-69. NICOLLS, K.D., F.B. ELLIS, and P. NEWBOULD. 1969. Methods for studying the root systems of apple trees. ARC Radiobiol. Lab. Rpt. for 1968. p. 54-55. NICOTRA, A. 1967. Root systems of peach trees killed by asphyxia (in Italian). Proc. Agr., Bologna 13:907-914. NORTHWOOD, P.J. and A. TSAKIRIS. 1967. Cashew nut production in Southern Tanzania. IV. The root system of the cashew nut tree. E. Afr. Agr. For. J. 33233-87.
DISTRIBUTION AND EFFECTIVENESS OF TREE ROOTS
485
NURMANBETOV, T.T. and I.G. ANDRONOV. 1976. Root system of the apple cultivar: apart in relation to different types of dwarfing rootstock (in Russian). Vestnik S - K h N a u k i Kazakhstana 6:57-60. NYE, P. and P.B. TINKER. 1978. Solute movement in the soil-root system. Blackwell, Oxford. ORLOV, A. JA. 1966. Significance of dying feeding tree roots on the organic cycle of the forest (in Russian). Zhurnut Obshch. Biol. 27:40-46. OSKAMP, J. and L.P. BATJER. 1932. Soils in relation to fruit growing in New York. 11. Size production and rooting habit of apple trees on different soil types in the Helton and Morton areas, Monroe Country. Cornell Univ. Agr. Expt. Sta. Bul. 55O:l-45. OVINGTON, J.D. and G. MURRAY. 1968. Seasonal periodicity of root growth of birch trees. p. 146-154. I n M.S. Ghilarov, V.A. Kovda, L.N. NovichkovaJuanova, L.E. Rodin, and V.M. Sveshnikova (eds.) Methods of Productivity Studies in Root Systems and Rhizosphere Organisms. USSR Academy of Sciences. PASSIOURA, J.B. 1972. The effect of root geometry on the yield of wheat growing on stored water. Austral. J. Agr. Res. 23:745-752. PATEL, R.Z. and A.M. KABAARA. 1975. Isotope studies on the efficient use of P fertilizers by Caffea arabica in Kenya. I. Uptake and distribution of PIL from labelled KH2 PO4. Expt. Agr. 11:l-11. PERSSON, H. 1978. Root dynamics in a young Scots pine stand in central Sweden. Oikos 30:508-519. PERSTNEVA, T.A. 1977. The root system of young apple trees on dwarfing rootstocks in an intensive orchard (in Russian). Pouysh Produktiun Plodou Nascz denii u Moldauii Kishineu Moldavian SSR 27-31. PHILIPSON, J.J. and M.P. COUTTS. 1977. T h e influence of mineral nutrition on the root development of trees. 11. The effect of specific nutrient elements on the growth of individual roots of Sitka spruce. J. Expt. Bot. 28:864-871. PILSHCHIKOVA, F.N. and N.V. PILSHCHIKOVA. 1978. Regeneration of roots of different apple rootstocks (in Russian). Izu. Timiryuzeu. Sel’kokh. Ahad. 2:145-150. PITCHER, R.S. and J.J.M. FLEGG. 1965. Observations of root feeding by the nematode Trichodoros viruliferus Hooper. N u t u r London 207:317. POLIKARPOV, V.P. and M.M. ADASKALILSII. 1977. Root systems of bearing palmette apple trees (in Russian). Vestn. Sel’kokh. N u u k i 6:112-114. PONDER, H.G. and A.L. KENWORTHY. 1976. Trickle irrigation of shade trees growing in the nursery. 11. Influence on root distribution. J. Amer. SOC. Hort. Sci. 101:104-107. PONOMARCHUK, V.P. and I S . GOLOVANOV. 1973. The root system of apple trees with flat crowns (in Russian). Vestn. Sel’kokh. N u u k i Kuzakhstana 9:87-91. POPESCU, M. 1963. The effect of planting methods on the development of the root system of apricot trees grown in sand (in Romanian). Grad. via Liu. 12:55-60.
486
HORTICULTURAL REVIEWS
POTAPOV, V.A. 1971. The root system and soil management in young apple orchards with close tree spacing in the rows (in Russian). Sb. Nauch. Rub. Vsesoyuznyi Nauchno-lssledouatel’skiiInst. Sadouod. I. Michurina 15:88-90. PRIESTLEY, C.A., P. B. CATLIN, and E.A. OLSSON. 1976. The distribution of “C labelled assimilates in young apple trees as influenced by doses of supplementary nitrogen. I. Total 14C radioactivity in extracts. Ann. Bot. 40: 1163-1170. QUINLAN, J.D. 1965. The pattern of distribution of I4carbonin a potted apple rootstock following assimilation of 14carbon dioxide by a single leaf. Rpt. East Malling Res. Sta. for 1964. p. 117-118. RECKRUHM, I. 1974. Direct root analysis in orchards with different soil management systems (in German). Archiu f u r Gartenbau 22:17-26. REYNOLDS, E.R.C. 1970. Root distribution and the cause of its spatial variability in PseudotoLga toxifolia (Poir) Brit. P l a n t & Soil 32:501-517. RHEE, J.A. VAN. 1975. T h e effect of earthworms on production in orchards. Fruitteelt 65:204-206. RICHARDS, D. 1976. Root-shoot interactions: a functional equilibrium for water uptake in peach ( P r u n u s persica (L)) Batsch. Ann. Bot. 41:279-281. RICHARDS, D. and B. COCKROFT. 1974. Soil physical properties and root concentrations in an irrigated peach orchard. Austral. J. Expt. Agr. Anim. HUsb. 14:103- 107. RICHARDS, D. and B. COCKROFT. 1975. The effect of soil water on root production of peach trees in summer. Austral. J. Agr. Res. 26:173-180. RICHARDS, D. and R.N. ROWE. 1976. Root-shoot interactions in peach: the function of the root. Ann. Bot. 41:1211-1216. RICHARDSON, S.D. 1957. Studies of root growth of Acer saccharinum L. VI. Further effects of the shoot system upon root growth. Kon Ned. Akad. Wetensch. Ser. C 60:624-629. RICHARDSON, S.D. 1958. Bud dormancy and root development in Acer saccharinum. p. 409-425. In K.V. Thimann (ed.) T h e physiology of forest trees. Ronald Press, New York. ROBERTS, J. 1976. A study of root distribution and growth in a P i n u s syluestris L. (Scots pine) plantation in East Anglia. P l a n t & Soil 44:607-621. ROGERS, W.S. 1933. Root Studies 111. Pears, gooseberry and black currant root systems under different soil fertility conditions with some observations on root stock and scion effect in pears. J. Pomol. Hort. Sci. 11:l-18. ROGERS, W.S. 1934. Root Studies IV. A method of observing root growth in the field; illustrated by observations in an irrigated apple orchard in British Columbia. Rpt. East Malling Res. Sta. for 1933. p. 86-91. ROGERS, W.S. 1935. Root Studies VI. Apple roots under irrigated conditions with notes on use of a soil moisture meter. J. Pomol. Hort. Sci. 13 (3):190-201. ROGERS, W.S. 1939a. Root Studies VII. A survey of the literature on root growth, with special reference to hardy fruit plants. J. Pomol. Hort. Sci. 17:67-84.
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ROGERS, W.S. 1939b. Root Studies VIII. Apple root growth in relation to rootstock, soil, seasonal and climatic factors. J Pomol. Hort. Sci. 17:99-130. ROGERS, W.S. 1952. Fruit plant roots and their environment. Rpt. 13th Intern. Hort. Congr. 1952. p. 1-4. ROGERS, W.S. 1968. Amount of cortical and epidermal tissue shed from roots of apple. J. Hort. Sci. 43:527-528. ROGERS, W.S. 1969. The East Malling root-observation laboratory. p. 361376. I n W.J. Whittington (ed.) Root growth. Butterworths, London. ROGERS, W.S. and G.A. BOOTH. 1959. The roots of fruit trees. Sci. Hort. 14:27-34. ROGERS, W.S. and G.C. HEAD. 1962. Studies of growing roots of fruit plants in a new underground root observation laboratory. Proc. 16th Intern. Hort. Congr. p. 311-318. ROGERS, W.S. and G.C. HEAD. 1966. The roots of fruit plants. J. R. Hort. S I C . 4 1:199-205. ROGERS, W.S. and G.C. HEAD. 1969. Factors affecting the distribution and growth of roots of perennial woody species. I n W.J. Whittington (ed.) Root growth. Butterworths, London. ROGERS, W.S. and M.S. PARRY. 1968. Effects of deep planting on anchorage and performance of apple trees. J Hort. Sci. 43:103-106. ROGERS, W.S. and M.C. VYVYAN. 1934. Root studies V. Root stock and soil effect on apple root systems. J. Pomol. Hort. Sci. 12:llO-150. ROSATI, P., W. FAEDI, and M. FAEDI. 1976. Studies on the root systems of various peach rootstocks in Romagna (in Italian). Frutticoltura 38:9-13. RUSSELL, R.S. 1977. Plant root systems-their function and interaction with the soil. McGraw-Hill, London. RYBAKOV, A.A. and Z.L. DZAVAKJANC. 1967. Root growth and development under irrigation (in Russian). Sudouodstuo 7:34-35. RYZHKOV, A.P. 1972. The characteristics of growth development and distribution of the root system in prostrate forms of apple trees (in Russian). Nauchnife Chteniya Pamyati Akademii MA Lisavenko (Barnaul USSR) 178185. SANDERS, F.E.T. 1971. The effect of root and soil properties on the uptake of nutrients by competing roots. D. Phil. Thesis, University of Oxford. SCHULTZ, R.P. 1972. Root development of intensively cultivated slash pine. Soil Sci. Soc. Amer. Proc. 36 (1):158-162. SCHUMACHER, R., F. FANKHAUSER, and E. SCHLAPFER. 1972. Development of apple roots: influence of the growth retardant Alar on root development (in German). Schweiz. Zeilschrift f u r obst und weinbuu 107:438-452. SECHI, A. 1975. Observations on the root system of peaches under different cultured treatments (in Italian). Centro Regionale Agrario Sperimentale-Cagliari, Publ. 48. p. 1-15. SEMINA, N.P. 1971. The growth characteristics of the active part of the root system in relation to the compatability of the graft components (in Russian).
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Sbornik Nauchnykh Rabot Vsesoyuznyi Nauchno-Issledouatel’<skii Institut Sadovodstua. I V Mich urina 15:112- 119. SEWELL, G.W.F. 1979. Effect of Pythium spp on growth of apple seedlings. Rpt. East Malling Res. Sta. for 1978. p. 92. SHOROKHOV, S.S. 1976. Uptake of 32Pby apple trees from super phosphate placed a t different depths (in Russian). Selektsiya Sortoizuchenie Agrotekhnika Poldouykh i Yagodnykh K u l t u r Ore1 USSR 7:155-161. SIDORENKO, V.M. 1973. The characteristics of distribution of the root system of apple trees in relation to soil management and irrigation (in Russian). Yuzhnoe Stepnoe Sadovodstuo (1973). p. 98-103. SKRIPKA, I.S. 1977. Changes in the growth of plum tree root system in relation to the cultivation and fertilization of orchard soil (in Russian). Soderzhi udobr Pochuy u Plodou Nasazhdeniyakh Kishineu Moldavian SSR. p. 57-86. SLOWIK, K. 1962. The distribution of the root systems of 11 year old apple trees grown in grass strips in the rows with clean cultivation between the rows (in Polish). Prace Inst. Sadow. Skierniew. 6:lOl-117. SLOWIK, K. 1968. The effect of compaction by machinery on the physical properties of the soil and on apple tree growth (in Polish). Prace Inst. Sadow. Skierniew. p. 79. SMITH, P.F. 1965. Effect of nitrogen source and placement, on the root development of Valencia orange trees. Proc. Flu. State Hort. SOC.78:55-59. SOONG, N.K., E. PUSHPARAJAH, M.M. SINGE, and 0. TALIBUDEEN. 1971. Determination of active root distribution of Hevea Brasiliensis using radioactive phosphorus. Proc. Intern. Symp. Soil Fert. Eual. 1:309-319. SPINA, P. 1966. Observations on the root systems of Citrus (in Italian). Tecnica. Agricola 18:31-54. STOICHKOV, I., M. PENKOV, A. ANDREEV, S. KEREMIDARSKA, B. MILANOV, and T.S. TSOLOV. 1974. The influence of pseudopodzolic cinnamon forest and alluvial meadow soils on the root distribution of Newton Pippin and Wellington apple cultivars grafted on M 4 (in Bulgarian). Grad. Lozar. N a u k a 11:ll-25. STOICHKOV, I., T.S. TSOLOV, B. MILANOV, A. ANDREEV, S. KEREMIDARSKA, and M. PENKOV. 1975. Architectonics of the root system of Doucin IV apple rootstock in relation to the soil and the scion cultivar (in Russian). Grad. Lozar. N a u k a 12:3-14. SUTTON, R.F. 1969. Form and development of conifer root systems. Tech. Comm. 7. Commonw. For. Bur., Commonw. Agr. Bur., Farnham Royal, U.K. TAMASI, J. 1964a. The effect of the soil water table on the root system of apple trees (in Hungarian). Magy. T u d . Akad. Kozlem. 23:25-41. TAMASI, J. 1964b. The effect of different cultural practices on the formation of the root system of apple trees (in Hungarian). Kiserl. Kozl. Sect C 57:43-63. TAMASI, J. 1965. Location of the roots of 1-6 year-old Jonathan apple trees grafted wild stock in an orchard on sandy soil (in Hungarian). Novenytermeles 14:115-148.
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TAMASI, J. 1973. Root development in closely planted sour cherry trees grafted on Mahaleb rootstocks in sandy soil in relation to cultural practices (in Hungarian). Gyumolcstermesztes 8:29-50. TAMASI, J. 1974. Cultural practices in relation to root development in young plum trees (in Hungarian). Gyumolcstermesztes 1:23-46. TAMASI, J. 1975. Investigation on the root development of young cherry trees planted in clay soil (in Hungarian). Gyumolcstermesztes 2:47-68. TAMASI, J . 1976. Investigation on early root development in sour cherries on Mahaleb rootstocks closely planted in a clay soil (in Hungarian). Gyumolcstermesztes 3:81-98. TANAS’EV, U.K. and V.V. BALAN. 1976. Development of the root system of palmette trained Jonathan apple trees grafted on M 4 in relation to the rate of tree planting fertilization (in Russian). T r u d y Kishineu. Sel-Khoz Znst. 154: 46-50. TANAS’EV, V.K. and V.V. BALAN. 1977. The effect of rootstock and high rates of deep pre-planting fertilization on the development of the apple tree root system (in Russian). Sadou. Vinogr. Vinod. Mold. 2:17-20. TAYLOR, A. 1974. Trickle irrigation experiments in the Goulburn Valley. Vict. Hort. Dig. 61:4-8. TAYLOR, B.K. and F.H. GOUBRAN. 1976. The phosphorus nutrition of the apple tree 11. Effects of localized phosphate placement on the growth and phosphorus content of split root trees. Austral. J. Agr. Res. 27:533-539. TAYLOR, H.M. and B. KLEPPER. 1973. Rooting density and water extraction patterns for corn (Zea mays L). Agron. J. 65:965-968. TAYLOR, H.M. and B. KLEPPER. 1978. The role of rooting characteristics in the supply of water to plants. Adu. Agron. 30:99-128. THAGUSEU, N.A. 1968. On the root systems of filberts (in Russian). Sel’ kokh. Biol. 3:623-626. TILL, M.R. and J.B. COX. 1965. A guide to cultural practices for young citrus trees. J. Agr. Sci. Austral. 68:232-233. TINKER, P.B. 1976. Roots and water: transport of water to plant roots in soil. Phil. Trans. R. SOC.London, Ser. B 273:445-461. TORREY, J.G. and D.T. CLARKSON. 1975. The development and function of roots. Academic Press, London. TROMP, J. 1978. The effect of root temperature on the absorption and distribution of K, Ca and Mg in three rootstock clones of apple budded with Cox’s Orange Pippin. Gartenbau. 43:49-54. TROMP, J. 1980. Mineral absorption and distribution in young apple trees under various environmental conditions. p. 173-182. Zn D. Atkinson, J.E. Jackson, R.O. Sharples, and W.M. Waller (eds.) The mineral nutrition of fruit trees. Butterworths, Borough Green, U.K. VORONOVA, T.G. 1965. The rhythm of root growth in fruit crops in relation to the development of their aerial parts (in Russian). Agrobiologija 2:291-293.
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WADDINGTON, J . 1971. Observation of plant roots in situ. Can. J. Bot. 49: 1850-1852. WEBSTER, D.H. 1978. Soil conditions associated with absence or sparse development of apple roots. Can. J. Plant Sci. 58:961-969. WELLER, F. 1965. Some observations on root distribution in the soil in relation to rootstock and scion variety (in German). Erwobstbsobstbau 7:165-169. WELLER, F. 1966a. Horizontal distribution of absorbing roots and the utilization of fertilizers in apple orchards (in German). Erwobstbsobstbau 8:181184. WELLER, F. 1966b. T h e vertical distribution of the absorbing roots of apple trees in some south west German soils with different water/air economies (in German). Erwobstbsobstbuu 8:28-32. WELLER, F. 1967. The periodic variability of the density of absorbing roots on apple trees (in German). Erwobstbsobstbau 9:167-170. WELLER, F. 1971. A method for studying the distribution of absorbing roots of fruit trees. Expt. Agr. 7:351-361. WHITE, G.C. 1977. Herbicide strip width/nitrogen trial. Rpt. East Malling Res. Sta. for 1976. p. 106. WHITE, G.C. and R.I.C. HOLLOWAY. 1967. The influence of simazine on a straw mulch on the establishment of apple trees in grassed down on cultivated soil. J. Hort. Sci. 42:377-389. WILSON, S.A. and D. ATKINSON. 1978. Water and mineral uptake by cherry roots. p. 570-571. In Abstr. Inaug. Mtg. Fed. European SOC.Plant Physiol. SOC.Expt. Biol., Edinburgh. WILSON, S.A. and D. ATKINSON. 1979. Water and mineral uptake by fruit tree roots. p. 372-382. In A. Riedacker and J. Gagnaire-Michard (eds.) Root physiology and symposia. Proc. IUFRO Symp. Sept. 11-15, 1978, CNRF. Nancy, France. YAKUSHEV, V.I. 1972. Asymmetry in the development of apple roots (in Russian). Vest Sel’kokh. Nuuki. 17 (8):84-88. ZAKOTIN, V.S. and A.T. ATANASOV. 1972. The inter-relationships of growth and the development of apple root and shoot systems in the annual cycle (in Russian). Zzu. Timiryazeu. Sel’hokh. Ahud. 5:117-131. ZENTMYER, G.A. 1979. Effect of physical factors, host resistance and fungicides on root infection a t the soil-root interface. p. 315-329. In J.L. Harley and R.S. Russell (eds.) Soil root interface. Academic Press, London. ZEREBCOV, F.F. 1966. The formation of root systems on deep soils (in Russian). Sudouodstuo 12:14-15.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
10 Light and Lighting Systems for Horticultural Plants Henry M. Cathey and Lowell E. Campbell U.S. Department of Agriculture, Beltsville, Maryland 20705 I. Introduction 492 11. Measurement of Radiation and Temperature 493 A. Radiant Energy 493 1.Wavelength Classification 494 2. Wavelength Characteristics of Sources 494 3. Irradiance-Quantities, Units and Symbols 495 B. Measuring Units 500 1.Photon Units 500 2. Solar Radiation Units 504 3. Radiometric Units 504 4. Photometric Units 504 C. Measurement Methods 505 1. Basic Requirements for Measurement 505 2. Types of Light and Radiation Meters 508 3. Types of Sensors and Detectors 508 4. Calibration 511 5. Guidelines 51 1 6. Recommended Methods 512 a. Illumination Meter-Photometric-($50, $150 and Up) 512 b. Irradiance Meter-Radiornetric-($500 and Up) 512 c. Photon Meter-($750 and Up) 512 7. Spectral Distributions 512 D. Infrared and Thermal Radiation 513 111. Spectral Radiant Power of Lamps 514 A. Photometric Data (Table 10.4) 515 B. Wavelength Intervals (Table 10.4) 516 IV. Generic Responses of Plants to Lamps 516 V. Selection of Efficient Light Sources by Plant Responses 520 A. Practical Plant Lighting 521 1.Display: 0.3 W/m2 521 2. Photoperiod: 0.9 W/m* 524 3. Survival: 3.0 W/m2 524 491
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4.Maintenance: 9.0 W/m2 524 5. Propagation: 18.0 W/m2 525 a. Greenhouse: 24.0 W/m2 526 527 b. Growth Chamber: 50.0 W/mZ 527 VI. Comparison of Light Sources A. Incandescent Lamps 527 B. Fluorescent Lamps 528 528 C. High Intensity Discharge Lamps VII. Summary 529 VIII. Literature Cited 532
I. INTRODUCTION
Intervention of the signals exerted by nature and the interposing of desired plant growth through the use of light and temperature manipulation have been one of the earliest concerns of horticulturists (Bailey 1893).I t began when estate gardeners developed growing methods which permitted flowering or harvesting of horticultural plants out or ahead of season. Forcing was added as a modifier to greenhouses and low temperature storage facilities to identify accelerated or year-round culture. The assumption was made that the previous growth cycle acted as a reservoir for storing sufficient energy (carbohydrates and other compounds in stems, roots, leaves) to ensure the development of green leaves and flowers without additional photosynthetic activity. Only a few woody and bulbous plants responded to these procedures. Many other plant species had to be held in glass-covered, sun-heated pits to ensure their survival over winter. They were expected to grow and flower only during the bright, long, warm days of spring to fall. Plant and engineering scientists have done much to bring about major changes as to which plants are grown, what structures are to be used for their production, and where the new plant products are to be consumed. We use the word Photo-regulation to describe these new procedures of growing plants (Garner and Allard 1920). We assume the use of pestfree, clonal material which is grown in environments which exert nearmaximum control of photosynthesis and photomorphogenesis. This review deals with an area of research where most of the physical environment, particularly radiation, has not been regulated previously. Artificial lamps used in plant studies previously have been regarded primarily as light sources in the region of 400 to 700 nm; the other regions of radiation often were neglected or ignored (Gaastra 1959). We will present tables listing the electrical, photometric, and radiometric characteristics of various types of lamps. We will offer suggestions as to how the properties of various types of lamps can be measured when utilized in various environments. We will describe the plant responses (seed ger-
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mination, photoperiod control, growth) to various types of lamps. And, we will review recent research and offer an overview of how the various kinds of lamps can be utilized to create energy-efficient growing systems by controlling the distance, intensity, duration, absence, or presence of sunlight . This review is written to bridge the many engineering activities designed to conserve energy in growing structures and the theoretical actions of the two major photo-triggering pigments-chlorophyll and phytochrome. T he structural engineering aspects have been covered in detail by Aldrich and White (1969) and White (1979); the horticultural aspects have been covered by Cathey and Campbell (1975); and the plant physiology aspects have been reviewed by Meijer (1971) and Bickford and Dunn (1972). These research areas (engineering, physiology) have used many different methods of measuring the energy output and uses from the various light sources. Th e measurements are further complicated by the interactions among the lamps, the fixtures, and the environment (Carlson et al. 1964). In this review we have attempted to treat the lamps and the plant responses generically and to avoid the minor variations among lamps from various manufacturers. We also wish to provide a basis for the rapid evaluation of any new light source a s a n energy source for growing any specific species. Measurements of research findings must be compatible with or transferable to engineering and architectural design. Since measurements require some correction for plant regulation, we have attempted to show t ha t such corrections for spectral power distributions can be made on the basis of generic types of lamps with established instruments and units. For each generic-type lamp a conversion factor will be given. 11. MEASUREMENT OF RADIATION AND TEMPERATURE
A. Radiant Energy T he radiation of major concern to biologists is optical or non-ionizing radiation to distinguish it from the remainder of the electromagnetic spectrum. Measurements are concerned with intensity and spectral distribution. I t is nearly impossible in practical observations to distinguish between the effects of direct radiation and the indirect effects of heat resulting from the radiation. This difficulty is minimum a t low radiation levels and increases in proportion to the intensity of radiation. For many years the pyroheliometer which measures total radiation and illumination meters (light meters) which measure light in terms of human eye response were the main instruments of measurements. In recent years new instruments have been developed. These new units vary widely in characteristics and price.
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Careful review and evaluation of the existing literature on light and plants reveal contradictory claims and hypotheses, obvious errors in light and radiation measurement and evaluation, observation attributed to hypothesis without valid experimental data, and lack of consideration of ultraviolet, infrared, and heat radiation in the environment. Some of the confusion can be attributed to the inherent difficulties of measurement. Different interest groups (biologists, engineers, manufacturers) approach the measurement problem with varying disciplines and with different instruments, resulting in variations in measurement procedures and in reported results. Several systems of terminology are used. 1. Wavelength Classification.-The regions of the electromagnetic spectrum are arbitrarily divided as follows:
Classification U1traviole t (UV)
uv-c
UV-B UV-A Visible Infrared (IR) or Infrared (IR) Thermal
Wavelength 100-380 nm 100-280 nm 280-320 nm 320-380 nm 380-780 nm 780-lo5 nm 780-2500 nm 2500 + nm
Traditionally engineers and physics authorities divided the ultraviolet spectrum into 100 nm bands from 100 to 400 nm. The classification of UV into A, B, and C is from the International Commission on Illumination (CIE) from use by photo-biologists. The spectral limits vary with authorities. The biological response is a gradual transition or overlap among regions without sharp delineation. The A, B, C system fits the peak emission of light sources better than 100 nm bands point, wherein the light sources often may peak a t the wavelength division between point between two bands. UV and UV-A bands frequently use 400 nm as a limit. This is inconsistent with the established definition of visible light (380 to 780 nm); however, the biological response continues from UV-A into the visible region above 400 nm. Many portions of these regions are referred to as “light” at times. Strictly speaking the term “light” refers only to the visible portion of the electromagnetic spectrum, but all regions, ultraviolet, visible, and infrared, are electromagnetic radiation. 2. Wavelength Characteristics of Sources.-The sources of radiation, both natural and artificial, are not limited to the individual limits of the regions’ wavelength. The sun emits energy throughout all the wavelength
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regions, although not a t the same level. Fluorescent lamps emit mainly in the visible region but have some energy in adjacent ultraviolet and infrared bands (Campbell et al. 1975). Incandescent lamps emit relatively more infrared and a lower amount of visible than sunlight or fluorescent lamps. Figure 10.1illustrates the spectral emission of radiant power from the sun. Figure 10.2 shows the spectral power emission of typical light sources used in horticulture. I t should be noted that all lamps have infrared and thermal radiation not shown in the visible spectral power distributions. Figure 10.3 shows both the visible and infrared radiation from high pressure sodium lamps. A graphic display of the power conversion of cool-white fluorescent and the HID lamps, highpressure sodium, metal halide, and mercury, is shown in Fig. 10.4. 2.5
h C iI&
2 . 0 t
1.5
SOLAR SPECTRAL IRRADIANCE OUTSIDE ATMOSPHERE SOLAR SPECTRAL IRRADIANCE AT SEA LEVEL (m = 1)
1 , CURVE FOR BLACKBODY AT 5900 K
, -03
H10
w d
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4 1.6 1.8 WAVELENQTH ( p m )
2.0
2.2
2.4
2.6
2.8
3.0
C
FIG. 10.1. SOLAR SPECTRAL IRRADIANCE
The shaded areas indicate absorption at sea level due to the atmospheric constituents shown.
3. Irradiance-Quantities, Units and Symbols.-We should first consider several concepts which may help in the comprehension of radiant power measurement. Radiometry and radiometric terms are valid throughout the entire electromagnetic spectrum. “Light,” photometry, and photometric terms are restricted to the measurement of light in the
HORTICULTURAL REVIEWS
496
100
-
RADIANT POWER PER LUMEN INSECT CONTROL
50 -
-
200
WAVELENGTH (NANOMETER)
400
600
860 '
'
I
1000
WAVELENGTH (NANOMETER)
U
+
RADIANT POWER PER LUMEN FLUORESCENT COOL WHITE (FCW)
9
94 F
RADIANT POWER PER LUMEN FLUORESCENT WARM WHITE (FWW)
v)
t
400
600
800
1000
WAVELENGTH (NANOMETER)
WAVELENGTH (NANOMETER)
1 5 0 ~
E~a
RADIANT POWER PER LUMEN PLANT GROWTH A (PGA)
100 +
= I w
RADIANT POWER PER LUMEN PLANT GROWTH B (PGB)
!toot ?
F
e C 0
c 200 WAVELENGTH (NANOMETER)
WAVELENGTH (NANOMETER)
From Campbell et al. (1975) FIG. 10.2. SPECTRAL RADIANT POWER CURVES FOR HORTICULTURAL LAMPS
LIGHT AND LIGHTING SYSTEMS
150
r
497
150
U
+ RADIANT POWER PER LUMEN MERCURY (CLEAR) (Hg)
5 100
RADIANT POWER PER LUMEN MERCURY DELUXE WHITE (Hg /DX)
z
F
Llg +
sp
600
400
800
50
2
1000
WAVELENGTH (NANOMETER)
WAVELENGTH (NANOMETER)
150
5
U
2 100
RADIANT POWER PER LUMEN METAL HALIDE A (MHA)
s
+
Y P
F
?
I-
+
5
u)
4
0
50
50
0 2
,
,
I
I 400
'
I
600
800
1
1000
WAVELENGTH (NANOMETER)
RADIANT POWER PER LUMEN LOW PRESSURE SODIUM (LPS)
RADIANT POWER PER LUMEN METAL HALIDE B (MHB)
WAVELENGTH (NANOMETER)
150,-
I 5 O F
f
t WAVELENGTH (NANOMETER)
FIG. 10.2. (Confinued)
WAVELENGTH (NANOMETER)
498
HORTICULTURAL REVIEWS
n
HIGH PRESSURE SODIUM 400W
E
c
0
cu
II
w
a. [r
5
:
740- 2500nrn
80W
W
L I-
2500nrn+ 142W
n
4w
II I
700
1000
1500 2000 WAVELENGTH (nm)
2500
HIGH PRESSURE SODIUM 400W
E
7
II W
a. II
5
380 -740nm
2
118W
w
L I-
4W
a 250
300
350
”
400
450 500 550 WAVELENGTH (nrn)
600
650
700
Adapted from Jack and Koedam (1974)
FIG. 10.3. SPECTRAL POWER DISTRIBUTION HIGH PRESSURE SODIUM 400 WATT LAMP 250 TO 2500 NM
region from 380 to 780 nm. Light is a weighted response based on the relative stimulation of the human eye. Figure 10.5 shows the response for photopic vision (luminous efficiency, V) known as the “CIE (Commission Internationale de 1’Eclairage) curve” or eye sensitivity curve. The three systems of units for irradiance per unit area are: Illumination E, lumen per square meter = lux (1x1 Irradiance E, watt per square meter (W/mz) or (W em - 2 )
(photometric) (radiometric)
LIGHT AND LIGHTING SYSTEMS
C.
INPUT 400W POWER IN ARC COLUMN
I/
499
INPUT 18OW POWER IN ARC COLUMN
ELEC-
ELEC-
DISCHARGE RADIATION
DISCHARGE RADIATION
59W
60W OUTERJACKET
I
1
I
281W
74W
1\
207W
A i
\ D.
Adapted from Jack and Koedam (1974) FIG. 10.4. POWER CONVERSION OF LAMPS A. Fluorescent. B. High Pressure Sodium. C.Metal Halide. D. Mercury. E.Low Pressure Sodium.
500
HORTICULTURAL REVIEWS
FIG. 10.5. STANDARD LUMINOUS EFFICIENCY CURVE (CIE)
Photon-flux density E, quantum per second and square meter (q s - 1 m - z )
(photon radiome try)
Notes Subscript refers to photometric quantities wherein luminous efficiency is included. Subscript refers to radiometric quantities. Subscript refers to photon quantities. The recommended SI units for these systems of measurement are shown in Tables 10.1 to 10.3, developed by the National Bureau of Standards, U.S. Department of Commerce. B. Measuring Units Considerable confusion and disagreement exist about what units should be used to measure radiation for plant science. Photometric units (lux, foot-candle) are used by lighting engineers for describing irradiance of radiation sources and in specification or evaluation of lighting applications. This system is widely used by manufacturers and design engineers. It is generally agreed that plant response to radiation is different from that of humans and that these photometric units are unsuitable for directly describing photosynthetic response. However, photometric measurements can be converted to useful units. 1. Photon Units.-Photon units are based on number of photons or quanta which vary in energy with wavelength. For example, 4 photons at 400 nm have the same energy as 7 photons a t 700 nm. Photon meters’ response thus approximates the number of photons a t each wavelength.
Symbol
Definition1
I
dQ/dX dL/dX
d*+/(dA.cose.dw); d*@/da-dw) dL,/ds; dI,/dV
f L-dw
d+/da;
f LcosO.dw
d@/dA;
dQ/dV dQ/dt d@/dw
f +.dt dQ/dA; f f
[email protected] dQ/da; f f L.dw.dt
watt per square meter and steradian watt per cubic meter and steradian joule per nanometer watt per square meter, steradian, and nanometer
watt per square meter
watt per square meter
joule per cubic meter watt watt per steradian
joule per square meter
Unit joule joule per square meter
[W-m - 2 1
Unit Symbol
Source: Adapted from Nicodemus (1978). dA = element of (directed) surface; da = cross-sectional area of spherical element; dL, = element of generated (emitted or scattered into ray) radiance; dI, = element of generated radiant intensity; ds = element of distance along ray; dV = element of volume; and dt = element of time. * I n September 1977 a t Berlin, the CIE Technical Committee TC 1.2 on Photometry and Radiometry adopted a number of recommendations for additions and changes in the upcoming edition of the International Lighting Vocabulary. Among those recommendations, the terms “spherical exposure” and “spherical irradiance” were given as the preferred terms for what have been called here, respectively, “fluence” and “fluence rate,” although the latter also were recognized as acceptable alternates, widely used in photobiology.
(Other soectral auantities are similarlv treated)
spectral radiant energy spectral radiance
radiant sterisent
radiant exitance radiant (omni-directional) fluence rate* radiance
irradiance
Quantity radiant energy radiant (directedsurface) exposure radiant (omni-directional) fluencez radiant (volume) density radiant power or flux radiant intensity radiant flux (directedsurface) density
TABLE 10.1. SI DERIVED UNITS FOR RADIOMETRY
Symbol
Unit lumen-second; (candela-steradian-second) lumen-second; (talbot) lux-second (candela-steradian-secondper square meter) lumen-second per square meter lux-second (candela-steradian-second per square meter) lumen-second per square meter lumen; (candela-steradian) lumen candela lumen per steradian lumen (candela-steradian) per square meter lumen per square meter lux; (candela-steradian per square meter) lumen per square meter lumen (candela-steradian) per square meter lumen per square meter lux; (candela-steradian per square meter) lumen per square meter candela per square meter lumen per square meter and steradian candela per cubic meter lumen per cubic meter and steradian [cd.m -3] L1m.m -3-sr - 1 1
Unit Symbol
Source: From Nicodemus (1978). Note: The first entry or entries for each quantity give the SI units, including, in every case, units in terms of the candela [cd] as the base unit. The last entry for each quantity is the same unit in terms of the lumen llml or lumen-second llm.sl, that parallels the corresponding radiometric unit in terms of the watt [W] or joule [Jl, respectively, for the corresponding quantity in Table 10.1. The definitions (defining expressions) in that table, and the footnotes there, also apply to the corresponding quantities listed here.
luminous sterisent
luminous (omni-directional) fluence rate luminance
luminous exitance
luminous flux (directedsurface) density illuminance (illumination)
luminous intensity
luminous flux
luminous (omni-directional) fluence
Quantity luminous energy; quantity of light luminous (directedsurface) exposure
TABLE 10.2. SI DERIVED UNITS FOR PHOTOMETRY E3 0
cn
Symbol
[q.s -1.m - 2 1 [q.s-l.m-z.sr -11 [qs-l.m-3.sr-l]
quantum per second and square meter quantum per second, square meter, and steradian quantum per second, cubic meter, and steradian
-21
[q.s -1.m
'1
quantum per second and square meter
[qs
[q.s-'.sr-1]
[ql [ q m -'I [qm-']
Unit Symbol
quantumZ quantum per square meter quantum per square meter quantum per second quantum per second and steradian
Unit
Note: The einstein [El = NA*[q] (where N, is the Avogadro constant, the number of molecules [particles] per mole [moll of any substance) and is widely used as a (much larger) unit of photon flux. (The latest value of the Avogadro constant in NBS Pub'. 398 is given as N, = (6.022045 f 0.000031) X loz3[particle~mol-~l.) efinitions (defining expressions) are the same as for corresponding quantities in Table 10.1. Also, spectral quantities are formed as shown in that table. The number of photons or quanta in a beam of radiation is frequently regarded as a pure (dimensionless) number, the ratio between the energy in that beam and the energy (hu) of an individual photon or quantum. However, that number is certainly a measure of the "amount of radiation" in the beam and it is not just a number, but is a number of a distinctive physical quantity, just as the number of joules is a physical quantity. Accordingly, it is useful to assign the quantum per second [q.s-'] as the unit of photon flux. Then all of the other geometrical quantities and their interrelationships and units parallel exactly those for radiant flux, luminous flux, or any other flux of a physical quantity propagated in rays that obey the laws of geometrical optics.
:r.,
Quantity' photon-flux energy; number of photons photon-flux exposure photon-flux fluence photon-flux photon-flux intensit photon-flux (surfacer density incident photon-flux density photon-flux exitance photon-flux fluence rate photon-flux sterance (radiance) photon-flux sterisent
TABLE 10.3. UNITS FOR PHOTON-FLUX RADIOMETRY
W
0
cn
504
HORTICULTURAL REVIEWS
In 1976 the Crop Science Society of America (Shibles 1976) defined the following:
Photosynthetically Active Radiation (PAR): Radiation in the 400 to 700 nm waveband (McCree 1971, 1972a,b). Photosynthetic Photon F l u x Density (PPFD): Photon flux density of PAR. The number of photons (400 to 700 nm) incident per unit time on a unit surface. (Suggested units: nE(einsteins1 * s - l * cm - 2 ) . Photosynthetic Irradiance (PI): Radiant energy flux density of PAR. The radiant energy (400 to 700 nm) incident per unit time on a unit surface. mW * cm - 2 . (Suggested units compatible with the SI convention would be Wm - 2 and Es - l m -z.) These definitions permit PAR to be reported in either quantum or energy units (McCree 1971, 1972a,b). In the past and in some current literature PAR usage does not conform to these definitions. 2. Solar Radiation Units.-Measurement of outdoor solar radiation (in Langleys), reported periodically by the U.S. Weather Bureau (now NOAA) from 1950 until 1972, was discontinued when errors of up to 100% in reported values were discovered. With improved calibration this reporting was reinstated in 1978 in both W/m2 and Langleys. This radiation information is needed for all solar energy utilization. NOAA also reports percentage of sunshine, temperature, and other environmental parameters. (A large package describing available information is available from the National Climatic Center, Federal Climatic Center, National Oceanic and Atmospheric Administration, Asheville, North Carolina 28801.)
3. Radiometric Units.-Irradiance or radiometric units which indicate energy in watts per square meter (W/m2) have equal response a t all wavelengths. This is an absolute measurement but not easily accomplished in a simple direct measurement because sensors with the appropriate spectral response usually are not available. Radiometric units are sometimes referred to as energy units. Nearly all standards and basic calibrations are in radiometric units (watt). Spectral power distributions of lamp manufacturers are also in radiometric units. We have adopted the viewpoint of using radiometric units W/m2 for photoregulation of plants in the subsequent portions of this chapter. 4. Photometric Units.-Lamp manufacturers rate lamps’ output in lumens. On request, most manufacturers will provide a visual spectral power distribution which shows the emitted radiation in microwatts per nanometer per lumen emission. With this information, the absolute radiation in W/m2 can be determined by summing the radiation over the interval desired.
LIGHT AND LIGHTING SYSTEMS
505
C. Measurement Methods We define and use photoregulation to denote plant response to all wavelengths of radiation, UV, visible, and infrared. Outdoors we are concerned with wavelengths from 300 to about 3000 nm. High intensity discharge lamps (HID) and incandescent emit radiation extending over about the same wavelength region but with different spectral power distribution. Fluorescent lamps emit mainly in the visible region but have some longer wave radiation. No single measurement or instrument is adequate to describe the radiant energy of light sources in relation to crop production. Pyranometers or solarimeters will measure the total radiation but take no account of the spectral distribution. Other meters such as illumination and photon quantities have spectral limitations. 1. Basic Requirements for Measurement.-In any measurement, if the spectral sensitivity of the sensor or detector and the spectral power distribution of the source are known, both the spectral and total radiation can be calculated. At each wavelength relative values of the sensor sensitivity and source emission multiplied together give the weighted radiant flux density. These are summed for all wavelength bands within the limits of the known wavelength response. Since most light sources including the sun have almost a generic spectral power distribution, projections can be accurately calculated beyond the sensor wavelength limits. This permits the use of standard measuring instruments wherein the measurement can be converted to total radiation in whatever wavelength region is desired. Table 10.4 was developed to determine the radiation in various wavelength bands using illumination meters. Basic rules to be followed with measurements include:
a. Make measurements once a month. b. Check measurements occasionally with another meter. c. Check meter calibration a t least once a year. In addition, certain information always must be recorded and reported: type and number of lamp (as etched on lamp); distance of sensor from lamp; make and model of meter; sensor type or model number. Ambient temperature a t point of measurement and date and time of measurement also should be reported. PAR measurements, by definition, whether PPFD or PI, reflect the total radiation between 400 nm and 700 nm and do not indicate differences in the spectral emission of sources. The differences between PI and PPFD are less than 10%. This is less than the normal instrument total error, not including user error.
LampIdentification Incandescent (INC) lOOA Fluorescent Cool white FCW Cool white FCW Warmwhite FWW PlantgrowthA PGA PlantgrowthB PGB Infrared FIR HID Discharge Clearmercury HG Mercurydeluxe HG/DX Metalhalide MH High-pressure sodium HPS Low-pressure sodium LPS
3
4 Output
5
6
7 8 9 Radiation per Unit of Luminous Flux
10
40 3200 70 215 15700 64 40 3250 71 40 925 20 40 1700 37 40 170 3.7 400 21000 50 400 22000 50 400 40000 85 400 50000 105 180 33000 143
46 245 46 46 46 46
440 440 460
470
230
1740 17
100
100
183
125
52 55 100
80 73 81 23 42 4.2
17
1.92
2.45
2.60 2.62 3.05
2.93 2.93 2.81 6.34 3.96 4.30
3.97
2.18
3.38
2.77 2.81 3.42
2.99 2.99 2.86 6.41 4.37 24.00
8.63
1.89
1.58
0.14 0.73 1.17
1.02 1.02 1.23 3.39 1.95 0.56
2.53
0.26
0.93
0.17 0.19 0.37
0.06 0.06 0.05 0.08 0.41 20.00
4.66
0.25
0.72
0.06 0.05 0.25
0.009 0.009 0.006 0.007 0.03 2.10
1.69
Total Lamp Total Total Lamp 400-700 nm 400-850 nm 580-700 nm 700-850 nm 800-850 nm mW/lm mW/lm W W lm Im/W lm/W mW/lm mW/lm mW/lm
1 2 Input Power
TABLE 10.4. ELECTRICAL, PHOTOMETRIC AND RADIOMETRIC CHARACTERISTICS OF SELECTED LAMPS
Column Number
11
12
13 Radiation Output
14
15
16
17 18
Efficiency
19
20
Source: Radiation data revised April, 1980 by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md.
Lamp 400-700 nm 400-850 nm 580-700 nm 700-850 nm 800-850 nm 400-700 nm 400-850 nm 580-700 nm 700-850 nm 800-850 nm Identification W W W W W mW/W mW/W mW/W mW/W mW/W Incandescent lOOA 6.90 15.00 4.41 8.11 2.94 69 150 44 66 29 F1 uorescen t FC W 9.38 9.56 3.27 0.18 0.03 204 208 71 4 0.6 FC W 46.00 47.00 16.00 0.88 0.14 188 192 65 4 0.6 FWW 9.13 9.28 4.00 0.15 0.02 199 202 87 3 0.4 PGA 5.86 5.93 3.13 0.07 0.01 127 129 68 2 0.1 PGB 6.73 7.42 3.32 0.69 0.05 146 161 72 15 1 FIR 0.73 4.13 0.10 3.40 0.35 16 90 2 74 8 HID Discharge 3 HG 55 58 3 3.6 1.2 124 132 6 8 3 36 9 HG/DX 58 62 16 4.1 1.1 131 140 22 MH 122 137 47 14.8 10.0 265 297 102 32 ___ ~. 77 168 99 261 360 79 46.5 36.0 123 169 HPS 36 271 37 8.3 276 313 62 8.6 63 72 LPS
Column Number
>
X c3
0
E:
508
HORTICULTURAL REVIEWS
If measurements are determined in units other than W/m2 or lux, conversions must be available for engineering or design specifications. Some published conversions assume a flat spectral distribution of the source rather than actual source spectra (Biggs and Hansen 1979). When fluorescent lamps alone are used in a growth chamber, PAR measurements from 400 to 700 nm will correlate reasonably well with crop production. This is because fluorescent lamps have very low emission beyond 700 nm. However, when HID lamps such as high-pressure sodium, metal halide, and incandescents are used either alone or in combination with other sources, crop production correlates more closely with radiation if the wavelengths from 700 to 850 nm are included. This is believed to be a response combining photomorphogenesis and photosynthesis along with other undefined photo responses. It is consistent with our observations that plants in the greenhouse and outdoors have increased performance (growth rates, flowering time) that cannot be attributed solely to the energy measurements in the 400 to 700 nm region. 2.
Types of Light and Radiation Meters.-
Type of Meter Illumination Photon Irradiance Pyranomometer (solarimeter) Ultraviolet Infrared Solar cells Total irradiance Spectroradiometers
Unit -
lux (foot-candle) quantum watt per square meter watt per square meter watt per square meter watt per square meter watt per square meter watt per square meter watt per square meter and nanometer
Wavelength (nm) 380-780 400-700
*
320-4200 250-400*
*
400-800
*
300-1100
Low sensitivity and poor stability are no longer an inherent problem in meters (sensors not included) due to the advent of solid state electronics. With proper design there should be little or no temperature instability of the meter. Battery operation is feasible and desirable except for meters used in continuous recording. Electrically, the basic parts of all meters are essentially the same. The differences are in the sensors and the calibration units used. 3. Types of Sensors and Detectors.-There are four basic types of sensors or detectors. Their characteristics are briefly noted. Spectral response curves for typical sensors or detectors are shown in Fig. 10.6 through 10.10. *No accepted standard-variance in spectral sensitivity and wavelength range.
LIGHT AND LIGHTING SYSTEMS W
v)
z
2
-
SCANNER
v)
CIE OBSERVER CURVE
W
I__
U
W
I I-
d
i W
U
400
600
800
1000
WAVELENGTH (NANOMETERS) FIG., 10.6. PHOTOMETRIC DETECTOR CIE CURVE
100
-
IDEAL QUANTUM RESPONSE
W
a W I Id
i W
I
U
I
400
I
I
I
I
I
I
I
600 800 WAVELENGTH (NANOMETERS)
I
I
I
I
J
1000
FIG. 10.7. COMMERCIAL PHOTON DETECTOR SPECTRAL RESPONSE (PHOTON-FLUX DENSITY)
W
v)
2
2 v)
W W
I I-
3
w
U
100 -
-
\
-
1
60 -
20 I
I
I
I
I
I
I
FIG. 10.8. COMMERCIAL VISIBLE-IR SPECTRAL RESPONSE
I
1
1
1
I
I
I
RADIOMETRIC DETECTOR
I
509
510
HORTICULTURAL REVIEWS
z
W
8
100
v)
W
a W 2 I-
4
W
60 20
a WAVELENGTH (NANOMETERS) FIG. 10.9. COMMERCIAL DETECTOR FOR IR NARROW BANDWIDTH
z
W
8
100
v)
w
a
60
W
2 c
5
20
W
a WAVELENGTH (NANOMETERS) FIG. 10.10. COMMERCIAL SILICON PYRANOMETER CALIBRATED FOR TOTAL SOLAR IRRADIANCE
Not useable for other sources without correction.
a. Thermopile or bolometer-flat response to all wavelengths; low signal level, slow response, requires ambient temperature correction. b. Photovoltaic cells-Selenium or silicon; range: 300 to 900 nm, response varies with wavelength, medium to high signal output, used with filters, temperature stable a t low impedance. c. Phototubes-photomul tipliers-200 to 1000 nm-response varies with wavelength. No single tube covers entire wavelength. Requires DC power supply, temperature sensitive, high sensitivity. Used mainly in laboratory instruments and spectroradiometers.
LIGHT AND LIGHTING SYSTEMS 511
d. Photodiodes-Similar to photovoltaic-some respond in IR region, long time stability unknown, high temperature coefficient, may require bias voltage or current.
For measurements to be reported on an absolute basis, only the following sensors can be used readily with sources of different spectral content: a. Photometric-silicon or selenium-calibrated in lux or foot-candles. b. Flat response sensors-calibrated in quanta or watts per square meter. When either of these sensors is used and the generic type of light source is reported, the radiation a t various wavelengths can be calculated and comparisons can be made with other reports. 4. Calibration.-Radiation sources used in calibration are known as standard lamps or standard sources. A primary standard is a source from which the values of other standards are derived. Primary standards usually are found in national physical laboratories such as a National Bureau of Standards. A secondary standard or reference standard is a radiation source calibrated from a primary standard. Secondary standards also are maintained in national physical laboratories and photometric and radiation laboratories, and by meter manufacturers. Working standards are sources calibrated from secondary standards for regular day-to-day use. These are usually special incandescent lamps. Standard lamps may be calibrated in total irradiance (watts per square meter) with wavelength limits, or in watts per square meter per nanometer, or both. Calibrated accuracy is f3% in the visible region, f8% in the UV region, and f4% in the IR region. Standard lamps require a precise power supply accurate to 5 ppm. Most plant scientists have neither time nor resources for precise calibration checks. Return of meters to the manufacturer or utilization of calibration labs may be a simpler way to check on equipment operation. There are several methods to approximately check calibration: (1)compare with other meters, preferably one recently calibrated; (2)purchase a second meter and keep it on the shelf as a standard; or, (3) for the meter alone without sensor, make voltage checks according to the manufacturer’s calibration instructions.
5. Guidelines.-Uncertainty with any meter will be about f5% and is likely to be f10% or more in practical day-to-day measurements. There are several recognized causes: a. Calibrations traceable to National Bureau of Standards have up to f5% uncertainty . b. Sensors and meters are seldom entirely free of temperature error. c. Cosine diffusion will vary with wavelength of source.
512
HORTICULTURAL REVIEWS
d. Meter and sensor are calibrated with an incandescent lamp as a point source. Measured sources differ in both spectral power distribution and extension in space. Radiation in growth chambers or in sunlight is almost never constant. Measurements show conditions a t a particular moment. In growth chambers with fluorescent lamps, lamp output may change f5% over a few minutes, and in the sun irradiance may vary considerably more than this. Sensors without cosine correction (incident light correction) result in relative values that cannot be compared to cosine corrected measurements. A 360” correction also will be confusing. Radiation measurements of the same growth chamber requirements taken independently by 2 individuals with the same equipment are likely to be different by 5 to 10%. 6. Recommended Methods.-In
order of complexity and cost.
a. Illumination Meter-Photornetric-($50, $150 and Up).-Meter measures radiation emitted in lux (foot-candle) for each generic type source, and converts to irradiance (watts per square meter) from tables for the wavelength region desired. (See Table 10.4.) b. Irradiance Meter-Radiornetric-($500 and Up).-Meter is used directly with any available sensor for specific wavelength intervals. Narrow bandwidth sensors which have interference filters which change calibration with change of direction of radiation and temperature are available. Wide band sensors may not have flat spectral response. Field of view is frequently only a 10 degree cone since cosine correction introduces a wavelength error. Pyranometer (Eppley type) thermopile has flat response but drifts with temperature. c. Photon Meter-($750 and Up).-These meters have the same basic silicon sensor and electrical circuit of other meters but have filters for approximate desired spectral response of 400 to 700 nm. Calibration check is difficult because standard sources are calibrated in watts. It is best to return to manufacturer for calibration. 7. Spectral Distributions.-Spectroradiometers are used to determine spectral distributions as in Fig. 10.2 and 10.3. In years past, the required equipment and expertise limited spectral measurements to a few lamp manufacturers and commercial testing laboratories. Commercial portable units in the past have lacked the precision and accuracy needed for characterizing the radiation environment of plant growth environments “in situ.” Recent developments of an automated spectroradiometer by the Instrumentation Research Laboratory a t the Beltsville Agricultural Research Center are promising for obtaining spectral irradiance as com-
LIGHT AND LIGHTING SYSTEMS
513
mercial models are developed. Spectroradiometric measurements are extremely difficult and time-consuming. Even with the anticipated improvement in equipment, the time and attention to calibration will limit spectroradiometric measurements to larger facilities where a part or fulltime individual can be assigned this responsibility. Additional information on spectroradiometry is contained in the Self-study Manual of Optical Radiation of the National Bureau of Standards (Nicodemus 1978).
D. Infrared and Thermal Radiation It is convenient to divide the IR region into a region from 780 to 2500 nm as Infrared and 2500 to 10 - 5 nm as Thermal, since the 2500 and above is not transmitted by glass. Solar radiation is mainly below 2500 (Fig. 10.1) and transmitted by glass. Transparent plastic materials transmit some of the thermal wavelengths. The plant response to this IR radiation is mainly unknown except that heating results from the radiation. Table 10.5 shows the emitted radiation of various sources in the visible, infrared, and thermal regions per 100 watts of input power. TABLE 10.5. RADIATION POWER DISTRIBUTION OF LIGHT SOURCES PER 100 WATT OF TOTAL RADIATION
uv
Light Source FC W HG/DX MH
1 4 0 0 nm W 2 3 4
IR 400-850 nm 850-2500 nm W W 36 19 41
1 18 8
Thermal 2500 + nm W 61 60 47
Total Radiation
W
100 100
100
Source: Radiation data developed or revised by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md.
In a growth chamber, radiant energy including the visible region, 100 watts of radiation raises the temperature of 300 cfm (150 literdsec) of air 0.5"C. Thus, in a growth chamber (1 mz) with 20,000 lux CWF and 5000 lux INC and 150 l i t e d s e c (300 cfm) the air temperature will rise nearly 2°C. If no glass barrier exists between the lamps and the chamber, the rise will be nearly 3°C. Outdoors, in similar light levels and similar air movement, the air temperature rise would be about 1°C from sunlight. Table 10.6 shows the radiation in a typical growth chamber with and without a glass barrier. The method and location of temperature sensors for either measurement or control have been a problem. With the lights on and the sensor
514
HORTICULTURAL REVIEWS
TABLE 10.6. RADIATION FROM LIGHT SOURCES
Through Glass Light Source FC W INC FCW+INC SUN HPS LPS
klx 20 5 25 20 20 25
400-850 nm W/m2 60 43 103 110 68 55
850-2500 nm 3 192 195 63 17 3
No GlassTotal 166 260 426 186 136 98
Source: Radiation data developed or revised by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md.
unshielded, the temperature indicated in a growth chamber will rise 4" to 6°C. If the sensor is shielded and aspirated, the circulated air temperature will be indicated. This may not be as near the effective plant temperature as an unshielded sensor in the direct radiation. When the circulated air is exhausted a t the top of a chamber which has a physical barrier between the lamps and the chamber, the temperature of the exhaust air may more closely reflect the effective plant temperature. The fact must be faced that in a radiation environment transpiring plants have an effective temperature which is somewhere between that of the ambient air and that of radiation-absorbing mass. Remote sensing as well as contact methods of temperature has not indicated a precise relation to plant response. At present, due to the lack of definitive precedent 'measurements or equipment, the investigator should consider possible effects of plant temperature due to radiation. Temperature measurements, in a chamber without barriers, tend to be misleading even in shielded enclosures. Plastic barriers are less effective than glass in shielding plants from thermal radiation since they transmit greater amounts of infrared than glass.
111. SPECTRAL RADIANT POWER OF LAMPS The spectroradiometric system was used to determine the light-source emissions in graphic form (Campbell et al. 1975). The graphs then were normalized to a per-lumen basis. The curves were compared with manufacturers' data and with published information. Most such comparisons were made within the wavelength region of 500 to 600 nm, since this region provides the most sensitive and accurate measurement. Published information and manufacturers' data on wavelengths above 700 nm are extremely limited because these wavelengths are less important than are those in vision lighting. After the data in graphic displays were determined to be in agreement with other known information a t as many points as possible, data were
LIGHT AND LIGHTING SYSTEMS
515
compiled on irradiances in the wavelength intervals that are of concern in plant response. The data shown in the graphs and tables are essentially extensions of existing information, but they are presented in a manner that should be useful in horticultural lighting. Table 10.4 shows the electrical, photometric, and radiometric properties of a range of lamps that are important in horticultural lighting. The lamps selected are typical of commercially available light sources that have high efficiency or spectral radiation unique to plant lighting. Table 10.7 shows the energy balance in the lamps. Input energy equals the sum of visible radiation, heat radiation, conduction, convection, and ballast loss. The power conversions are for lamps without luminaires or enclosures. Enclosures are expected to decrease slightly visible radiation and to increase heat radiation, conduction, and convection. TABLE 10.7. INPUT POWER CONVERSION OF LIGHT SOURCES'
Lamp Identification Incandescent (INC) lOOA Fluorescent Cool white FC W Cool white FCW Warm white FWW Plant growth A PGA Plant growth B PBB Infrared FIR Disc ha rge HG Clear mercury Mercury deluxe HG/DX Metal halide MH High-pressure sodium HPS Low-pressure sodium LPS
Total Input Radiation Other Power (400-850 nm) Radiation (Watts) (%) (%I
Conduction and Convection
Ballast Loss
(%)
(%)
100
15
75
10
00
46 225 46 46 46 46
21 19 20 13 16 09
32 34 32 35 34 39
34 35 35 39 37 39
13 12 13 13 13 13
440 440 460
13 14 30
61 59 42
17 18 15
09 09 13
470
36
36
13
15
230
31
25
22
22
Source: Radiation data developed or revised by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md. 1 Conversion efficiency is for lamps without luminare. Values com iled from manufacturer data, published information, and unpublished test data by W.W. Thimijan, USDASEA-AR, Beltsville, Md.
A. Photometric Data (Table 10.4) Columns 1 through 5 give the standard electrical and lumen ratings of the lamps. The lumen rating shown for the lamp FIR is an estimated value (de Boer 1974; Kaufman and Christiensen 1972; Kaufman 1973). Columns 6 through 20 list 5 repetitive wavelength intervals that describe the emission in 3 ways. Columns 6 through 10 are given in milliwatts per
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HORTICULTURAL REVIEWS
lumen, which can be used with illumination-meter measurements (footcandle or lux) to determine radiation in milliwatts per unit of area. Lux times milliwatts per lumen equals milliwatts per square meter. Footcandles times milliwatts per lumen equals milliwatts per square foot. When generic types of lamps are used in combination, measurements must be taken individually, with only one type of lamp in operation a t a time; the measurements are then summed. Columns 11 through 15 give the total radiation output in the indicated wavelength interval for each lamp. The values should be rounded off to two significant figures for practical use. The overall efficiency of the lamps-watts emitted per watt of electrical energy used, including ballasts-is shown in columns 16 through 20 for the wavelength interval indicated. These columns allow a comparison of the lamps’ relative efficiency for emissions a t specific wavelength intervals.
B. Wavelength Intervals (Table 10.4) The 400 to 70 nm wavelength interval is similar to the region of plant response in photosynthesis. The commonly accepted photosynthesis action spectra peaks in the blue and red region of the spectrum. Recent reports indicate that all wavelengths between 400 nm and 850 nm may be effective in photosynthesis (Cathey and Campbell 1977; Meijer 1971). In photomorphogenesis plants respond to emissions in the red and far red portions a t wavelengths of 580 to 700 nm (red), 700 to 850 nm (far red), and 400 to 500 nm (blue). These wavelength intervals are important in photoperiod control and/or in the control of flowering, bulbs, and other light-mediated plant responses (Cathey and Campbell 1974). The information on radiation emitted in the 800 to 850 nm wavelength interval, shown in Table 10.9, permits comparisons to be made of lamps that have emissions above 800 nm with those which do not. The importance of emissions above 800 nm is not known. IV. GENERIC RESPONSES OF PLANTS TO LAMPS All human vision lamps can be used as an additional source to grow plants. All lamps, however, have inherent limitations in their use as a sole source for growing. The limitations are: (1) Irradiance source and its distribution over an area. (2) Irradiance without the creation of a cone of heat or other growthmodifying radiation.
LIGHT AND LIGHTING SYSTEMS
517
(3) Irradiance insufficiency or surplus which modifies growth responses. (4) Irradiance lacking energy in essential region(s) or the photoconver-
sion of factors regulating growth. ( 5 ) Irradiance performance (output and maintenance) in various environments. (6) Irradiance capability in space available for installation of lamps and fixtures. (7) Irradiance level and duration sensitivity based on growth stage and responses desired. When these limitations and others are considered, many lamps can be eliminated for use in many lighting situations. I t also means that the variations among special lamps can be extremely difficult to identify when so many kinds of plants and plant responses are considered. Sunlight, unlike all of the lamps described, is a continuous spectrum source (Fig. 10.1) from the ultraviolet into the infrared. The photo-action of sunlight is not described in Table 10.8. Experiments with sunlight often use neutral filters to reduce the intensity in the comparable energy range of artificial light sources. These experiments are complicated by hourly, daily, and seasonal shifts in intensity, heat, and light quality (Frankland and Letendre 1978; deLint and Klapwijk 1973). The information from such experiments often is not transferrable from one section of the country to another and has led to many disappointing or inefficient facilities for growing plants (Hammer et al. 1978; Morris 1973; Enoch et al. 1973). The effects of sunlight on plants are similar to the ones suggested for INC and associated lamps. The paling of foliage, the lengthening of stems, the expansion of leaf blades, and the suppression of lateral branching are extremely sensitive interactions between sunlight and temperature, moisture-stress, and mineral ions. Sunlight in this review is considered to be an everchanging energy source for which artificial light can substitute or supplement (Holmes and Smith 1975). The regulating action of intense sunlight and its effects on phytochrome in tissue filled with chlorophyll still await analysis (Morgan and Smith 1976). Table 10.8 describes how the different types of lamps regulate seed germination, photoperiod control, and growth. The standard light source for many years has been cool white (CWF) or warm white (WWF) fluorescent and is used as the standard to which the other sources are compared. The lamps are described in generic types. Special lamps combining the features of several of the lamps are available. In our experience, these lamps cost the most, are less efficient, and require more complex equipment to operate them than standard, widely available lamps.
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HORTICULTURAL REVIEWS
TABLE 10.8. LAMPS AND PLANT RESPONSE
Lamp Fluorescent - Cool White(CW)
Plant Responses Growth Green foliage which expands to parallel to the surface of the lamp Stems elongate slowly Multiple side shoots develop Flowering occurs over a long period of time
Seed Germination Prompt uniform response Photoperiod Short Day Plants: Interruption, 4 to 8 hours Long Day Plants: Relatively ineffective Fluorescent Gro Lux (GL) and Plant Light
Growth Deep green foliage which expands, often larger than on plantsgrownunderCWor WW Stems elongate very slowly, extra stems develop Multiple side shoots develop Flowering occurs late, flower stalks do not elongate Seed Germination Prompt, seedlings shorter than those grown under CW or WW Pho toperiod Short Day Plants: Interruption 4 to 8 hours Long Day Plants: Relatively ineffective
Fluorescent Gro Lux WS Plant Light WS(GL-WS) Vita-lite (VITA) Agro-lite (AGRO),and Wide Spectrum Lamps
Growth Light green foliage which tends toward thelamp Stems elongate rapidly, distances between the leaves Suppresses development of multiple side shoots Flowering occurs soon, flower stalks elongated, plants mature and age rapidly Seed Germination Prompt, seedlings taller than those grown under CW or WW Photoperiod Short Day Plants: Interruption 3 to 6 hours Long Day Plants: Extension of 8-hour day to 18 to 20 hours daily
High Intensity Discharge Mercury (HG)or Metal Halide (MH)
Growth Similar to CW and WW fluorescent lamps compared on equal energy Green foliage which expands Stemselongate slowly Multiple side shoots develop Flowering occurs over a long period of time Seed Germination Prompt, seedlings similar to ones germinated under CW andWW Photoperiod Short Day Plants: Ineffective Long Day Plants: Ineffective
LIGHT AND LIGHTING SYSTEMS TABLE 10.8. (Continued) Lamp
519
Plant Responses
Growth High Intensity Discharge High Pressure Sodium (HPS) Similar to Gro-Lux and other improved fluorescent compared on equal energy Deep green foliage which expands, often larger than on plantsgrown under HG and MH Stems elongate very slowly, extra thick stems develop Multiple side shoots develop Flowering occurs late, flower stalks do not elongate Seed Germination Prompt, seedlings shorter than those grown under HG and MH Pho toperiod Short Day Plants: Extension or interruption for 4 to 16 hours Long Day Plants: Ineffective Low Pressure Sodium (LPS)
Growth Extra deep green foliage, bigger and thicker than on plantsgrown under other light sources Stem elongation is slowed, very thick stems develop Multiple side shoots develop even on secondary shoots Floweringoccurs, flower stalks do not elongate Exceptions: Saintpaulia, lettuce, and Impatiens must have supplemental sunlight or incandescent to ensure development of chlorophyll and reduction of stem elongation Seed Germination Prompt, uniform response Pho toperiod Short Day Plants: Ineffective Long Day Plants: Ineffective
Incandescent (INC) and Incandescen t-Mercury (INC-HG PLANT LIGHT) (TUNGSTEN-HALOGEN)
Growth Paling of foliage, thinner and longer than on plants grown under other light sources Stem elongation is excessive, eventually becomes spindly and breaks easily Side shoot development is suppressed, plants expand only in height Flowering occurs rapidly, the plants mature and senescence occurs Exceptions: Rosette and thick leaved plants such as S a n seueria may maintain themselves for many months. The new leaves which eventually develop will elongate and will not have the typical characteristics of the species Seed Germination Inhibitsgermination of some species Photoperiod Short Day Plants: Effective as extension or interruption, given continuously or intermittently (6 sec/min to 3 m i d 3 0 min for 4 to 8 hours) Long Day Plants: Effective as extension or intermittently (12 sec/min for 4 to 8 hours)
Note: Mention of a trademark name or a proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture, and does not imply approval of it to the exclusion of other products that also may be suitable.
520
HORTICULTURAL REVIEWS
V. SELECTION OF EFFICIENT LIGHT SOURCES BY PLANT RESPONSES Plants are widely adapted to growing in highly varied light levels. We seldom see them growing, however, under optimum conditions. The technology developed in growth chambers which combined the simultaneous enhancement of light, temperature, humidity, water, and nutrition is seldom transferred into our traditional growing facilities. We have been forced to adapt the use of light-transmitting structures and neutral filter to reduce the energy available to the plants to a workable intensity. However, the true energy level under which we have grown the plant is extremely difficult to decipher when so much energy is applied and removed simultaneously. A clue to our problem is that most plants cannot be grown in unshaded and unventilated transparent structures, but yet can be grown out-ofdoors. The growers’ dilemma of plants exposed to the so-called “greenhouse effect” of the visible light energy (short wavelengths) entering but being trapped as heat (long wavelengths) or not being irradiated in covered structure is still unresolved. Plants must have visible radiation, but we must design systems to eliminate or utilize the surplus long wavelength radiation. In the approaching age of energy shortages and conservation, all energy must be trapped from the sun and must be utilized to produce acceptable plants for commercial growers, biomass converters, small farm producers, and urban (home-grown) gardeners. Lighting to substitute for or supplement the available sunlight can be used to accomplish some goals: (1) Reduce the time required to produce the desired stage of growth. (2) Utilize the lamps as energy sources rather than just for their light-use several criteria for measurement and installation of lamps. (3) Establish the light intensity and duration required for the plant processes to proceed. Overlighting (called “overshoot”) wastes energy (visible light and heat). (4) Utilize light properly throughout the growth so that the plants will not require “acclimatization” for their successful use by the consumer. (5) Learn how to compare one light source to another to create equally effective lighting systems for growing plants. ( 6 ) Develop alternative and lowered-energy-requiring structures for growing plants. We have arranged the energy requirements for displaying, handling, and growing plants into six levels. All are well below what is recorded (whatever sensor and value system) when plants are grown out-of-doors
LIGHT AND LIGHTING SYSTEMS
521
(McCree 1971, 1972a,b). Much of the energy in the out-of-doors occurs in “overshoot,” supra-optimal levels of natural light (Menz et al. 1969). Due to the constantly changing light intensities resulting from clouds, rain, daylength, and the orientation of the sun, these levels are seldom sustained over extended periods of time (Evans 1963). Further, re-radiation of the shortwave energy from the plants back into space occurs without interference from the covering (glass, plastic, films), thus effectively reducing the total energy that plants must tolerate. We do not believe that any growth systems for plants should or can be designed to mimic out-of-door conditions in its spectral or energy distribution (Balegh and Biddulph 1970; Singh et al. 1974). Supplemental or substitute lighting systems are thus, a t best, a simulation of only part of what actually occurs in nature. We are fortunate, however, that lighting systems for plants can be designed which afford, in many cases, simpler and easier environments to standardize and to regulate. Horticultural research scientists must maintain the perspective, however, that they are still creating only an approximation of the natural environment (Evans 1963). One then should anticipate that some species, cultivars, or breeding lines will exhibit aberrant growth characteristics when grown in a regulated photo-environment which may not be apparent when the same plants are grown in the natural environment. Even the traces or the absence of one or several parts of the spectrum (290 to 2500 nm) may limit the growth of a few species or several subtypes. The majority of species tested, however, did not exhibit abnormal growth characteristics and developed plants typical for the type (Canham 1974; Cathey and Campbell 1977). As we wander away from our three traditional light systems-INC for photoperiod (Downs and Borthwick 19561, CWF for acclimatization chambers (Biran and Kofranek 1976; Cathey et al. 19781, and CWF + INC for growth chambers (Tibbitts et al. 1976)-we can expect more and more examples of unusual growth problems (Brown, Cathey, Bennett and Thimijan 1979; Brown, Foy, Bennett and Christiansen 1978). First we shall discuss the lighting from a generic sense-when the various types of lamps can be used interchangeably. Then, we shall discuss energy-efficient lighting systems which satisfy specific spectral requirements and/or combinations of lamps for most prompt and rapid growth.
A. Practical Plant Lighting 1. Display: 0.3 W/mz.-Plants will exist a t an intensity of 0.3 W/mZ (Table 10.9). By tradition, the lamp of preference has changed with technological advances in efficiency and distribution. The emphasis, how-
Lamp Type, Illumination, l l o l u x Lamps per Square Meter and Distance from Plants, Meters Fluorescent-Cool White 40W single lamp 4 f t 3.2 klm Illumination, kilolux Lamps per square meter Distance from plants, meter 40W 2-lamp fixtures (4f t ) 6.4 klm Illumination, kilolux Fixtures per square meter Distance from plants, meter 215 W 2-8 ft lamps 31.4 klm Illumination, kilolux Fixtures per square meter Distance from plants, meter High Intensity Discharge Mercury (1)400W Parabolic Reflector Illumination, kilolux Lamps per square meter Distance from plants, meter 0.30 0.36 1.7 0.30 0.18 2.4 0.30 0.04 5.1 0.32 0.05 4.4
0.10 0.12 2.9 0.10 0.06 4.1 0.10 0.01 + 8.8 0.1 0.02 7.6
0.3
1.1 0.17 2.4
3.2 0.52 1.4
3.0 0.39 1.6
3.0 1.8 0.75
1.o 0.60 1.3
1.0 0.13 2.8
3.0 3.6 0.53
1.o 1.2 0.92
6.4 1.o 1.o
6.0 0.77 1.1
NA
NA
8.6 1.4 0.8
8.0 1.o 1.o
NA
NA
Radiant Power 400-850 nm a t Plant Level Watts per Square Meter, W.m - 2 0.9 3 9 18 24
TABLE 10.9. LIGHTING DESIGN GUIDE FOR RADIANT ENERGY LEVELS 0.3 TO 50 W.m-2
18.0 2.9 0.6
16.7 2.2 0.7
NA
NA
50
u,
r
m
z
N N
cn
1.4 0.088 3.4 0.33 0.56 1.3 0.33 0.35 1.7 0.50 0.74 1.2
0.41 0.026 6.2 0.10 0.17 2.4 0.098 0.10 3.1 0.15 0.22 2.1 0.16
0.14 0.009 10.7 0.033 0.056 4.2 0.033 0.035 5.4 0.050 0.07 3.7 0.054 0.54
0.89 0.05 4.5
0.27 0.015 8.2
0.089 0.005 14.2
0.88 0.08 3.6
0.26 0.02 6.5
0.09 0.01 11.3
1.6
1.5 2.2 0.67
3.2
3.O 4.5 0.47
2.0 2.1 0.7
2.0 3.4 0.54
1.o 1.7 0.77
1.0 1.0 1.o
8.3 0.53 1.4
5.3 0.30 1.a
5.3 0.47 1.5
4.1 0.26 2.0
2.7 0.15 2.6
2.6 0.24 2.1
Source: Radiation data developed or revised by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md.
Metal Halide (1) 400W Illumination, kilolux Lamps per square meter Distance from plants, meter High Pressure Sodium 400W Illumination, kilolux Lamps per square meter Distance from plants, meter Low Pressure Sodium 18OW Illumination, kilolux Lamps per square meter Distance from plants, meter Zncandescen t Incandescent lOOW Illumination, kilolux Lamps per square meter Distance from plants, meter Incandescent 150W Flood Illumination, kilolux Lamps per square meter Distance from plants, meter Incandescent-Hg 160W Illumination, kilolux Lamps per square meter Distance from plants, meter Sunlight Illumination, kilolux 4.3
4.0 6.0 0.41
2.6 2.8 0.6
2.7 4.5 0.47
11.0 0.70 1.2
7.1 0.39 1.6
7.0 0.63 1.3
8.9
8.3 12.0 0.28
5.5 5.8 0.4
5.6 9.4 0.33
23.0 1.46 0.83
15.0 0.82 1.1
15.0 1.3 0.87
524
HORTICULTURAL REVIEWS
ever, always has been directed toward color rendering and the type of atmosphere created in the living spaces. Low wattage INC and FLUOR have been the lamps of preference. At this intensity the plants can be displayed (seen), but little or no significant impact on plants can be expected. Also, timing (light-dark durations) and temperature interaction would not be of concern.
Photoperiod: 0.9 W/mz.-Plant growth can be regulated a t an intensity of 0.9 W/m2 (Table 10.9). By tradition, this intensity has been tagged as the so-called “low light intensity” systems which are triggered by the photo-reversible blue pigment-phytochrome (Downs and Borthwick 1956; Downs et al. 1958; Deutch and Deutch 1978; Downs and Piringer 1958; Whalley and Cockshull 1976; Jose and Vince-Prue 1978). The range of plant responses (promote or delay flowering, promote growth) which can be regulated is extensive and is widely demonstrated and practiced by commercial growers (Nitsch 1957a,b; Perry 1971; Withrow 1958; Withrow and Richman 1933; Withrow and Withrow 1947). Cathey and Campbell (1975) reported the relative order of activity in regulating photoperiod responses as incandescent (INC) > high-pressure sodium (HPS) >> metal halide (MH) = cool white fluorescent (F)>> clear mercury (Hg) from the major types of sources tested. Later they found (unreported) that LPS was as effective as F in photoregulation of the daylength responses of plants. The effectiveness of any lighting system was increased by the use of reflective aluminum soil mulch (Cathey et al. 1975). 2.
3. Survival: 3.0 W/mz.-Plants can survive a t an intensity of 3.0 W/m2 (Table 10.9). By tradition, this intensity creates an environment where many green plants can maintain their green color. Stem lengthening and reduction of leaf size and thickness, however, occur almost immediately following placement of plants under this intensity. In time, the overall development of the plants falls behind that of other plants grown under higher intensities. Photoperiod responses do not function well a t this intensity since all plants lengthen and seldom develop green foliage. There are, however, strong interactions between this intensity and temperature, watering frequency, and nutrition. Cooler temperatures (less than 17°C)tend to help conserve the previously stored material while frequent watering and fertilization aggravate the stem lengthening and aging of the older foliage.
4. Maintenance: 9.0 W/mz.-Plants can maintain growth over many months when exposed to an intensity of 9 W/m2 (Table 10.9). By tradition, this is the intensity a t which many indoor gardeners (Boodley 1970; Dunn 1975) (professional or hobbyist) grow their plants when
LIGHT AND LIGHTING SYSTEMS
525
starting them from seeds, cuttings, or meristems. It has become a convenient base and energy balance, particularly for those who use fluorescent lamps as a sole source for growing plants (Biran and Kofranek 1976; Boodley 1970). As anticipated, interactions with the environment (temperature, airflow, relative humidity, pollutants) may vary greatly from installation to installation. When the concentration of lamps is limited and air exchange is provided for, simple facilities to grow a wide range of plant species can be constructed (Stoutemyer and Close 1946). The rate of development, particularly as the plants grow in size, can be slow, compared to plants grown a t higher intensities (Cathey et al. 1978). During the development of the seedling and the rooting of the cutting, there appears to be little response to photoperiod. In fact, for most plants during the initial phases of development, continuous light (and heat) should be used to help compensate, in some part, for the limited irradiance. Most plant species develop deep green foliage and large leaves, and may accelerate the transfer of nutrients and stored materials from their older to their younger, rapidly developing leaves. The plants eventually begin to drop or lose an old leaf for every new leaf that develops. Adjustment of the lighting regime to a 12-hour light-12-hourday cycle, coupled with reduced frequencies of watering and fertilization, creates an environment where growth is slowed and few new leaves are formed while most older leaves are retained. Most container-grown foliage plants are now “acclimatized” for 4 to 16 weeks under an intensity of 9 W/m2 and are sold to the consumer (Fonteno and McWilliams 1978; Cathey et al. 1978). An “acclimatizated” plant can be readily identified by its slowed growth, few if any new leaves, deep green leaves which are broad and flat, and persistent leaves to the soil line. 5. Propagation: 18.0 W/mZ.-Plants can be propagated rapidly when exposed to an intensity of 18 W/m2 for a minimum of 6 to 8 hours daily (Table 10.9). By tradition, this is the intensity a t which many propagators attempt to shade their greenhouses with one or several layers of neutral filters (films on coverings, plastic or other fabrics) to restrict the entry of light (and heat) into the propagation area. At least 50% of the incident sunlight already has been lost by reflection of the covering (glass, plastic, polyethylene) and by absorption or interference of the framing and supports of the greenhouse. Cuttings rooted at this intensity maintain a growth rate similar to that of the cuttings attached to the stock plant. Stem length, branching, and leaf color, however, can be regulated by manipulating the temperature, moisture stress, and nutrients (Klueter and Krizek 1972). Most plants grown for their flowers and fruits can be brought to maturity, usually by increasing the daylength to 16 to 18 hours for flower initiation (or rapid growth) and then reducing
526
HORTICULTURAL REVIEWS
the daylength to 8 to 12 hours for development. The growth rate, however, is relatively slow (Krizek et al. 1968, 1972). For most prompt development (leaf number, number of branches, early initiation of flower initiation), the plants must be transferred to a lighting regime which is higher-24 to 50 W/m2. a. Greenhouse: 24.0 Wlm'.-Plants can be grown year-round in a greenhouse in which the natural light is supplemented with 24 W/m2 for 8 to 16 hours daily (Table 10.9). By tradition, this is the intensity, when coupled with the ambient sunlight (shaded by clouds, greenhouse structures, and lamp fixtures), which can stimulate many of the growth responses and rates which have been associated with growth chamber studies (Cathey and Campbell 1979; Duke et al. 1975). The photomorphogenetic activity of sunlight, even under dim light conditions of midwinter, is essential to regulate many unknown or yet-to-be detected growth responses. The supplementary intensity of 24 W/m2, from a wide range of artificial light sources, is sufficient to boost growth rates and create a growing environment for rapid growth and early flowering (Carpenter 1976; Carpenter and Beck 1973; White 1974; Carpenter and Anderson 1972). The different phototypes (short-, long-, and dayneutral) and growth systems (regulation of flowering and dormancy) exhibit a wide array of responses. Since the most widely grown species and cultivars are quantitative in their responses to daylength, supplemental lighting tends to lump the growth responses into one type of response-accelerated growth and early flowering (Austin and Edrich 1974). The plants grown in the greenhouse without the supplemental lighting grow much more slowly and flower much later than the lighted ones. Duration (in hours) and placement (day-night) are extremely critical (Downs et al. 1973). Supplemental lighting for 8 hours during the day (0800 to 1600) is nowhere near as effective as lighting a t night (2000 to 0400) (Cathey and Campbell 1979). Neither of these lighting regimes, however, is as effective as lighting for 16 hours from morning to midnight (0800 to 2400). Lighting of the short-day plants such as soybeans, chrysanthemum, and poinsettia is relatively inefficient because they can be lighted only during the 8- to 12-hour day, followed by the obligatory 12- to 16-hour daily dark period (Anderson and Carpenter 1974). Deciduous trees lighted with INC (at 0.9 W/m2) maintain vegetative growth over many months. On the other hand, deciduous trees lighted with HID lamps, regardless of spectral composition, go dormant or develop abnormally colored leaves. Species vary widely in their sensitivity to lighting with INC and HID lamps. Continuous lighting of most plants initially induces a paling of the foliage, then an abrupt loss of all visible pigments in the top-most leaves. The plants, however, do not die but survive many
LIGHT AND LIGHTING SYSTEMS
527
weeks under such bleached conditions. The condition is corrected in part by giving the plants a t least 4 hours of dark each day, by increasing and/ or lowering the temperature 2" to 4"C, by maintaining high relative humidity, and by spraying the foliage with minor element solutions.
b. Growth Chamber: 50.0 Wlrn*.-Plants can be grown in growth chambers if the light intensity is a minimum of 50 W/m2 (Table 10.9). This intensity is approximately one-fourth of that recorded out-of-doors. This intensity can be used to simulate many growth conditions (daylength, temperature range, relative humidity, airflow, carbon dioxide concentrations), and has become the standard growth chamber (Krizek and Zimmerman 1973; Zimmerman et al. 1970; Krizek et al. 1968; Krizek 1972; ASHS Special Comm. Growth Chamber Environments 1977). There is no one source used to light these chambers (Frank and Barker 1976; Wilson et al. 1978). For convenience, cool white fluorescent lamps have been widely used for more than 30 years (Patterson et al. 1977; Tibbitts et al. 1976). More recently, HID lamps have been substituted for fluorescent lamps (Buck 1973; Roper and Thomas 1978). All require, for most consistent results, a barrier of glass or other material between the lamp and the plants and separate ventilating systems to help remove the heat which can build up rapidly in such enclosed spaces. Since water filters or airflow cannot completely remove IR (infrared), the chambers are difficult to standardize from different manufacturers (Downs and Bonaminio 1976). It often leads to confusing information on plant growth and flowering in relation to what is observed with plants grown in greenhouses and out-of-doors (Tibbitts et al. 1977). When the total irradiance is 50 (80) W/m2 and 10 to 20%of the total watt input is provided with INC lamps, we find that most kinds of plants can be grown successfully (Bailey et al. 1970; Tibbitts et al. 1976). We observe the typical plant forms and flowering and fruiting responses when the plants are subjected to daylength (8 to 24 hours), temperature (9" to 35"C), carbon dioxide (300 to 5000 ppm), relative humidity (20 to loo%), and airflow. Growing plants in chambers constructed to provide intensities greater than 50 W/m2 becomes progressively more difficult, and the uncontrolled aspects become too complex to solve (Wareing et al. 1968; Measures et al. 1973). VI. COMPARISON OF LIGHT SOURCES A. Incandescent Lamps The standard light source to regulate the photoperiod responses of plants is INC, providing equal red (660 nm) and far red (730 nm) (Lane et
528
HORTICULTURAL REVIEWS
al. 1965; Piringer 1962) (Table 10.10). We are unable to detect differences in the plant responses to the INC when its basic 120 volt-frosted covering is modified (Downs 1977). Similar photoperiodic effects are observed when the covering is changed from the traditionally frosted one to clear, ceramic-coated (yellow, bug, orange, red) and colored glass (red, ruby, blue). These changes alter the human vision aspects in the yellowgreen region, but have a slight effect on the red (600 nm)-far red (730 nm) regions or ratio. The lamps of rated lives of 750 hours, 2500 hours, and 8000 hours also are equally effective as a light interruption or given as cyclic lighting. Most photoperiod responses could be regulated with 0.9 W/m2 for 1 or 2 to a t most 4 hours given continuously or cyclic (1 to 30 minutes) during the middle of a 12- to 16-hour dark period. Other light sources (fluorescent or HID) were never as effective (intensity) or efficient (rapid cycling and long life) as INC lamps.
B. Fluorescent Lamps Extensive testing has been conducted to determine the relative effectiveness of fluorescent lamps which emit more red, blue, infrared, and ultraviolet radiation than the traditional cool white and warm white lamps (Pallas 1964). Although there are reports of exceptional performance of a specific plant under a special lamp (Corth et al. 1973), the prevailing conclusion is that total lumen output is a much better criterion for plant growth than any special spectral distribution in the visible range (Table 10.10). Evaluating the effectiveness of a new fluorescent lamp can become very complex (Cathey et al. 1978). Fluorescent tubes are extremely sensitive to interactions with the environment. The lamps are coated with phosfors which create the fluorescence. They vary greatly in their spectral output, shift, and life. The glass used to make the lamp can alter the light emitted to the plants (LaCroix et al. 1966). Overall cool white and warm white fluorescent lamps are anticipated to be the standard fluorescent light source (Biran and Kofranek 1976; Dunn and Went 1959; Helson 1963; Newton 1973; Cathey et al. 1978).
C. High Intensity Discharge Lamps The high intensity discharge lamps (HID) were generally ignored for plant lighting until the insides of mercury lamps were coated with phosfors. The efficiency of these lamps (color improved mercury) finally equalled or exceeded that of tubular fluorescent lamps (Swain 1964). They were soon superseded with lamps enriched with various metals. No single type of lamp was satisfactory for plant growth. Finally, the sodium lamps (HPS and LPS) with much greater efficiency (as measured by
LIGHT AND LIGHTING SYSTEMS
529
lumens per watt) than the other types of HID lamps were made available for plant lighting (Buck 1973; Cathey and Campbell 1974). We have observed that many kinds of plants may be grown under HPS and LPS lamps as a sole source or as a supplement in greenhouses. When there was a special requirement for spectral composition for plant growth, the HPS lamps were more satisfactory than LPS lamps (Morgan and Cooke 1971). The abnormal growth characteristics observed in plants growing under LPS could be reduced by adding INC lamps and/or increasing the ambient temperature (Brown et al. 1979). HPS lamps apparently provided the required visible and infrared radiation to grow a wide range of plants. Even plants lighted with HPS benefit from the addition of INC. Again, the mixture of visible and IR more successfully simulates the action of sunlight .
VII. SUMMARY People always have been willing to test new light sources for growing plants, anticipating that different and accelerated cultural systems can be developed. This review presents the “no nonsense view” that most “human vision’’ light sources can be used for regulating or growing plants. We have described the anticipated growth-regulating performances of various artificial light sources. With the basic information on the use of sensors to measure irradiation, we have suggested conversion factors with which to convert numbers into various systems. We believe, however, that these measurements alone, without a detailed analysis of the variations without the lighted area, can lead to very confusing results. We urge workers to continue to present the physical measurements of distance and spacing employed for the different types of lamps. We also recommend utilizing W/mz in the region of 400 to 850 nm as the basis for 6 intensities for showing, maintaining, propagating, and growing plants. We believe that these six base-line intensities should serve as the beginning of the construction of any facilities for plant growth studies. In one table we have shown how to achieve these intensities with most of the basic types of lamps (Table 10.9). Coupled with the statements on how the lamps regulate plants (Table 10.71, we believe that research workers and growers can systematically decide which lamps would be the most energy-efficient system for a specific growing situation. We need to build lighting (plus energy) facilities to provide for plant growth. In Table 10.9 we have shown the design information to estimate the lighting required to achieve the various energy levels. For each type of lamp in each column is shown: (1)the equivalent illumination in kilolux (1000 lux); (2) the number of lamps per unit area; and (3) approximate distance from lamp fixture to plants. These are approximate values
CWF, WWF MH
available available available available
Pretransplanted Seedlings and Cuttings
Interior Survival
CWF, WWF MH LPS INC
CWF, WWF MH HPS LPS
none (and/or available) none none none
none (and/or available) none none available daylight
CWF, WWF MH HPS LPS
available available available available
Daylength and photosynthesis supplement (propagation)
Pre-interior Preparation
INC
available
Transplanted Seedlings and Cuttings Daylength only
LPS
HPS
Artificial Light CWF, WWF
Natural Light available
Growth Stage Seed Germination
TABLE 10.10. LIGHTING BY STAGE OF GROWTH
45 40 65 25
280 245 245 385
560 490 490 770
20
280 245 245 385
1.5
9
18
20
9
Intensity fc W/m2 140 4.5
-
0800-1600 (0800-1600 or any 8-hour period)
0600- 1800 (0600-1800 or any 12-hour period)
2000-0400 2000-0400 2000-0400 2000-0400
2 m i d 1 0 min)
2000-0400
( 12 sec/min or
0800-2400 0800-2400 0800-2400 0800-2400
Duration (hours) 0000-2400
cn
8
z
0
X
0
w
INC HPS
available
available
HPS
available
25
10
25
10
1565 1390 2175
710
560 490 490
280 245 245 385 150
0.9
0.9
0.9
0.9
50
18
9
Source: Radiation data developed or revised by R.W. Thimijan, USDA-SEA-AR, Beltsville, Md. Note: Lamp Code CFW = Cool White Fluorescent WWF = Warm White Fluorescent M H = MetalHalide HPS = High Pressure Sodium LPS = Low Pressure Sodium INC = Incandescent
Daylength and photosynthesis supplement (cover soil with reflecting aluminum coated DaDer)
INC
CWF,WWF HPS LPS
none none none
Growth Chamber
available
CWF,WWF MH HPS LPS
none none none none
Propagation
Field Daylength only
CWF,WWF MH HPS LPS -
none (and/or available) none none none available
Maintenance
2000-0400 (12 sec/min or 2 m i d 1 0 min) 2000-0400
2000-0400 (12 sec/min or 2 m i d 1 0 min) 2000-0400
Any period required
0600-1800 (0600-1800or any 12-hour period)
-
0600-1800 (0600-1800 or any 12-hour period)
532
HORTICULTURAL REVIEWS
based on multiple lamp installations of four or more lamps. For a single lamp or fixture, the kilolux and distance from plants will be reduced by one-third to one-half. This table is intended as a planning guide only. Actual installations should be planned using photometric data from the fixture (luminair) manufacturer. VIII. LITERATURE CITED ALDRICH, R.A. and J.W. WHITE. 1969. Solar Radiation and Plant Growth in Greenhouses. Trans. Amer. SOC. Agr. Eng. 12:l. ANDERSON, G.A. and W.J. CARPENTER. 1974. High intensity supplementary lighting of chrysanthemum stock plants. HortScience 9:58-60. ANON. International lighting vocabulary, 1970, 3rd edition. Commission International de l'Eclairage, Paris. ASHS SPECIAL COMM. GROWTH CHAMBER ENVIRONMENTS. 1977. Revised guidelines for reporting studies in controlled environment chambers. HortScience 12:309-310. AUSTIN, R.B. and J.A. EDRICH. 1974. A comparison of six sources of supplementary light for growing cereals in glasshouses during winter time. J.Agr. Eng. Res. 19:339-345. BAILEY, L.H. 1893. Greenhouse notes: Third report upon electrohorticulture. Cornell Uniu. Agr. Expt. Sta. Bul. 55:127-238. BAILEY, W.A., H.H. KLUETER, D.T. KRIZEK, and N.W. STUART. 1970. COz systems for growing plants. Trans. Amer. SOC. Agr. Eng. 13(3):263-268. BALEGH, S.E. and 0. BIDDULPH. 1970. The photosynthetic action spectrum of the bean plant. Plant Physiol. 46:l-5. BICKFORD, E.D. and S. DUNN. 1972. Lighting for plant growth. Kent State Univ. Press, Kent, Ohio. BIGGS, W.W. and M.C. HANSEN. 1979. Instrument letter on radiation measurements. LI-COR, Lincoln, Neb. BIRAN, I. and A.M. KOFRANEK. 1976. Evaluation of fluorescent lamps as an energy source for plant growth. J. Amer. SOC. Hort. Sci. 101(6):625-628. BOODLEY, J.W. 1970. Artificial light sources for gloxinia, african violet, and tuberous begonia. Plants & Gardens 26:38-42. BROWN, J.C., H.M. CATHEY, J.H. BENNETT, and R.W. THIMIJAN. 1979. Effect of light quality and temperature on Fe3+ reduction, and chlorophyll concentration in plants. Agron. J. 71:1015-1021. BROWN, J.C., C.D. FOY, J.H. BENNETT, and M.N. CHRISTIANSEN. 1978. Two light sources (LPS & FCW) differentially affected Fe3+ and growth of cotton. Plant Phvsiol. 63:692-695. BUCK, J.A. 1973. High intensity discharge lamps for plant growth application. Trans. Amer. SOC. Agr. Eng. 16(1):121-123.
LIGHT AND LIGHTING SYSTEMS
533
CAMPBELL, L.E., R.W. THIMIJAN, and H.M. CATHEY. 1975. Spectral radiant power of lamps used in horticulture. Trans. Amer. SOC. Agr. Eng. 18(5):952-956. CANHAM, A.E. 1974. Some recent developments in artificial lighting for protected crops. Proc. XIX Intern. Hort. Congr., Warsaw. Sept. 11-18, 1974. p. 267-276. CARLSON, G.E., G.A. MOTTER, JR., and V.C. SPRAGUE. 1964. Uniformity of light distribution and plant growth in controlled environment chambers. Agron. J. 56 2 4 2 -243. CARPENTER, W.J. 1976. Photosynthetic supplementary lighting of spray pompom, Chrysanthemum morifolium. Ramat. J. Amer. SOC. Hort. Sci. 101: 155-158. CARPENTER, W.J. and G.A. ANDERSON. 1972. High intensity supplementary lighting increases yields of greenhouse roses. J. Amer. SOC. Hort. Sci. 97:331-334. CARPENTER, W.J. and G.R. BECK. 1973. High intensity of supplementary lighting of bedding plants after transplanting. HortScience 8(6):482-483. CATHEY, H.M. and L.E. CAMPBELL. 1974. Lamps and lighting-a horticultural view. Lighting Design & Application 4(11):41-51. CATHEY, H.M. and L.E. CAMPBELL. 1975. Effectiveness of five visionlighting sources on photo-regulation of 22 species of ornamental plants. J. Amer. SOC. Hort. Sci. 100(1):65-71. CATHEY, H.M. and L.E. CAMPBELL. 1977. Plant productivity: new approaches to efficient sources and environmental control. Trans. Amer. SOC. Agr. Eng. 20(2):360-371. CATHEY, H.M. and L.E. CAMPBELL. 1979. Relative efficiency of high- and low-pressure sodium and incandescent filament lamps used to supplement natural winter light in greenhouses. J. Amer. SOC. Hort. Sci. 104:812-825. CATHEY, H.M., L.E. CAMPBELL, and R.W. THIMIJAN. 1978. Comparative development of 11 plants grown under various fluorescent lamps and different duration of irradiation with and without additional incandescent lighting. J. Amer. SOC. Hort. Sci. 103:781-791. CATHEY, H.M., G.G. SMITH, L.E. CAMPBELL, J.G. HARTSOCK, and J.U. MCGUIRE. 1975. Response of Acer rubrum L. to supplemental lighting reflective aluminum soil mulch, and systemic soil insecticide. J. Amer. SOC. Hort. Sci. 100:234-237. CORTH, K., G.M. JIVIDEN, and R.J. DOWNS. 1973. New fluorescent lamp growth applications. J. Illurn. Eng. SOC. 9(2):139-142. DE BOER, J.B. 1974. Modern light sources for highways. J. Zllum. Eng. SOC. 3(4):142-152. DELINT, P.J.A.L. and D. KLAPWIJK. 1973. Observations on growth and development of tomato seedlings. Acta Hort. 32:161-172. DEUTCH, B. and B.I. DEUTCH. 1978. Spectral dependence of a single and a subsequent second light pulse inducing barley leaf unfolding. Photochem. & Pho tobiol. 27 :14 1- 146.
534
HORTICULTURAL REVIEWS
DOWNS, R.J. 1977. Incandescent lamp maintenance in plant growth chambers. HortScience 12:330-332. DOWNS, R.J. and V.P. BONAMINIO. 1976. Phytotron procedural manual for controlled-environment research a t the Southeastern Plant Environment Laboratory. North Carolina Agr. Expt. Sta. Tech. Bul. 244. DOWNS, R.J. and H.A. BORTHWICK. 1956. Effects of photoperiod on growth of trees. Bot. Gaz. 117:310-326. DOWNS, R.J., H.A. BORTHWICK, and A.A. PIRINGER, JR. 1958. Comparison of incandescent and fluorescent lamps for lengthening photoperiods. Proc. Amer. SOC. Hort. Sci. 71:568-578. DOWNS, R.J. and A.A. PIRINGER, J R . 1958. Effects of photoperiod and kind of supplemental light on vegetative growth of pines. For. Sci. 4(3):185-195. DOWNS, R.J., W.T. SMITH, and G.M. JIVIDEN. 1973. Effect of light quality during the high-intensity period of growth of plants. ASAE Pap. 73-4525. ASAE, St. Joseph, Mich. DUKE, W.B. et al. 1975. Metal halide lamps for supplemental lighting in greenhouses. Crop response and spectral distribution. Agron. J. 67:49-63. DUNN, S. 1975. Lighting for plant growth or maintenance. Flor. Rev. 156 (4054):41, 86-90. DUNN, S. and F.W. WENT. 1959. Influence of fluorescent light quality on growth and photosynthesis of tomato. Lloydia 22:302-324. ENOCH, H.Z., V. ZIESLIN, Y. BIRAN, A.H. HALEVY, M. SCHWARZ, B. KESLER, and D. SHIMSI. 1973. Principles of COz nutrition research. Acta Hort. 32:97-117. EVANS, L.T. 1963. Extrapolation from controlled environments to the field. p. 421-437. I n L.T. Evans (ed.) Environmental control of plant growth. Academic Press, New York. FONTENO, W.C. and E.L. MCWILLIAMS. 1978. Light compensation points and acclimatization of four tropical foliage plants. J. Amer. SOC.Hort. Sci. 103:52-56. FRANK, A.B. and R.E. BARKER. 1976. Rates of photosynthesis and transpiration and diffusive resistance of six grasses grown under controlled conditions. Agron. J. 68:487-490. FRANKLAND, B. and R.J. LETENDRE. 1978. Phytochrome and effects of shading on growth of woodland plants. Photochem. & Photobiol. 27:223-230. GAASTRA, P. 1959. Photosynthesis of crop plants as influenced by light, carbon dioxide, temperature, and stomata1 diffusion resistance. Meded v.d. LBHS to Wageningen 59(13):11. GARNER, W.W. and H.A. ALLARD. 1920. Flowering and fruiting of plants a s controlled by the length of day. USDA Yearb. 1920, U.S. Dept. Agr., Washington, D.C. p. 377-400. GOVINDGEE, R. 1974. The absorption of light in photosynthesis. Sci. Amer. 231(6):68-80, 82.
LIGHT AND LIGHTING SYSTEMS
535
HAMMER, P.A. and R.W. LANGHANS. 1972. Experimental design considerations for growth chamber studies. HortScience 7:481-483. HAMMER, P.A., T.W. TIBBITTS, R.W. LANGHANS, and J.C. MCFARLANE. 1978. Base-line growth studies of Grand Rapids lettuce in controlled environments. J. Amer. SOC. Hort. Sci. 103:649-655. HELSON, V.A. 1963. Comparison of gro-lux and cool-white fluorescent lamps with and without incandescent as light sources used in plant growth rooms for growth and development of tomato plants. Can. J. Plant Sci. 45:461-466. HOLMES, M.G. and H. SMITH. 1975. The function of phytochrome in plants growing in the natural environment. Nature 254:512-514. JACK, A.G. and M. KOEDAM. 1974. Energy balances for some high pressure discharge lamps. J. Illum. Eng. SOC. 3(4):323-329. JOSE, A.M. and D. VINCE-PRUE. 1978. Phytochrome action: A reappraisal. Pho tochem. & Photobiol. 27 :209-216. KAUFMAN, J.E. 1973. Optimizing the uses of energy for lighting. Lighting Design & Application 3(10):8-11. KAUFMAN, J.E. and J.F. CHRISTIENSEN (eds.) 1972. IES lighting handbook, 5th edition. Illuminating Engineering SOC. of North America, New York. KLEUTER, H.H. and D.T. KRIZEK. 1972. How to use controlled lighting to propagate and grow plants. p. 205-209. I n J. Hayes (ed.) Landscape for living. USDA Yearb., 1972. US. Dept. Agr., Washington, D.C. KRIZEK, D.T. 1972. Accelerated growth of birch in controlled environments. Proc. Intern. Plant Prop. SOC. p. 390-395. KRIZEK, D.T., W.A. BAILEY, and H.H. KLUETER. 1972. A “head start” program for bedding plants through controlled environments. Proc. 3rd Natl. Bedding Plant Conf., Rochester, N.Y. Oct. 2-4, 1972. p. 43-56. KRIZEK, D.T., W.A. BAILEY, H.H. KLUETER, and H.M. CATHEY. 1968. Controlled environments for seedling production. Proc. Intern. Plant Prop. SOC.18:273-280. KRIZEK, D.T. and R.H. ZIMMERMAN. 1973. Comparative growth of birch seedlings grown in the greenhouse and growth chamber. J. Amer. SOC. Hort. Sci. 98(4):370-373. LACROIX, L.J., D.T. CANVIN, and J. WALKER. 1966. An evaluation of three fluorescent lamps as sources for plant growth. Amer. SOC. Hort. Sci. Proc. 89:714-721. LANE, H.C., H.M. CATHEY, and L.T. EVANS. 1965. The dependence of flowering in several long-day plants on the spectral composition of lighting extending the photoperiod. Amer. J. Bot. 523006-1014. MCCREE, K.J. 1971. The action spectrum absorptance and quantum yield of photosynthesis in crop plants. Agr. Metrord 9:191-216. MCCREE, K.J. 1972a. Test of current definitions of photosynthetically active radiation against leaf photosynthesis data. Agr. Metrord 10:443-453. MCCREE, K.J. 1972b. Significance of enhancement for calculation based on
536
HORTICULTURAL REVIEWS
the action spectrum for photosynthesis. Plant Physiol. 49:704-706. MEASURES, M., P. WEINBERGER, and H. BAER. 1973. Variability of plant growth within controlled-environment chambers as related to temperature and light distribution. Can. J. Plant Sci. 53:215-220. MEIJER, G. 1971. Some aspects of plant irradiation. Acta Hort. 22:103-105. MENZ, K.M., D.N. MOSS, R.Q. CANNELL,and W.A. BRUN. 1969. Screening for photosynthetic efficiency. Crop Sci. 9:692-694. MORGAN, S.F. and J.I. COOKE. 1971. Supplementary light sources for greenhouse crops. 1-lettuce. Rpt. Ref. ECRC/R392. Elec. Counc., London. MORGAN, D.C. and H. SMITH. 1976. Linear relationship between phytochrome photsequilibrium and growth in plants under simulated natural radiation. Nature 262:210-212. MORRIS, L.G. 1973. Enclosures for research on control of aerial environment for protected crops. Acta Hort. 32:73-88. NEWTON, P. 1973. Growing rooms. Symposium on greenhouse climate: Evaluation of research methods. Acta Hort. 32:89-95. NICODEMUS, F.E. (ed.) 1978. Self-study manual of optical radiation measurements part 1. Tech. Notes 910-2 and 910-4, National Bureau of Standards, U S . Dept. Commerce, Washington, D.C. NITSCH, J.P. 1957a. Growth responses of woody plants to photoperiodic stimuli. Proc. Amer. Soc. Hort. Sci. 70:512-525. NITSCH, J.P. 1957b. Photoperiodism in woody plants. Proc. Amer. SOC. Hort. Sci. 70:526-544. PALLAS, J.E. 1964. Comparative bean and tomato growth and fruiting under two fluorescent lamp sources. Bioscience 14:44-45. PATTERSON, D.T., M.M. PEET, and J.A. BUNCE. 1977. Effect of photoperiod and size at flowering on vegetative growth and seed yield of soybean. Agron. J. 69:631-635. PERRY, T.O. 1971. Dormancy of trees in winter. Science 171(3966):29-36. PIRINGER, A.A. 1962. Photoperiodic response of vegetable plants. p. 173185. I n Proc. Plant Sci. Symp., Mar. 5-10, 1962. Campbell Soup Company, Camden, N.J. ROPER, C.D., JR. and J.F. THOMAS. 1978. Photoperiodic alteration of dry matter partitioning and seed yield in soybeans. Crop Sci. 18:654-656. SHIBLES, R. 1976. Committee report terminology pertaining to photosynthesis. Crop Sci. 16:437-439. SINGH, M., W.L. OGREN, and J.M. WIDHOLM. 1974. Photosynthetic characteristics of several Cs and C4 plant species grown under different light intensities. Crop Sci. 14:563-566. STOUTEMYER, V.T. and A.W. CLOSE. 1946. Rooting cuttings and germinating seeds under fluorescent and cold cathode lighting. Proc. Amer. SOC. Hort. Sci. 48:309-315. SWAIN, G.S. 1964. The effect of supplementary illumination by mercury va-
LIGHT AND LIGHTING SYSTEMS
537
por lamps during periods of low natural light intensity on the production of chrysanthemum cuttings. Proc. Amer. SOC. Hort. Sci. 85:568-573. THOMAS, J.F. and C.B. RAPER, JR. 1978. Effect of day and night temperatures during floral induction on morphology of soybeans. Agron. J. 70: 893-898. TIBBITTS, T.W., J.C. MCFARLANE, D.T. KRIZEK, W.L. BERRY, P.A. HAMMER, R.H. HODGSON, and R.W. LANGHANS. 1977. Contaminants in plant growth chambers. HortScience 12:310-311. TIBBITTS, T.W., J.C. MCFARLANE, D.T. KRIZEK, W.L. BERRY, R.W. LANGHANS, R.A. LARSON, and D.P. ORMROD. 1976. Growth chambers. J. Amer. SOC. Hort. Sci. 101:164-170. WAREING, P.F., M.M. KHALIFR, and K.J. TREHERNE. 1968. Rate-limiting processes in photosynthesis a t saturating light intensities. Naturwissenschaften 220:453-457. WHALLEY, D.N. and K.E. COCKSHULL. 1976. The photoperiodic control of rooting, growth and dormancy in Cornus alba L. Sci. Hort. 5:127-138. WHITE, J.W. 1974. Supplemental lighting for rose production. ASAE Pap. 74-4043. WHITE, J.W. 1979. Energy efficient growing structures for controlled environment agriculture. p. 141-171. In J. Janick (ed.) Horticultural reviews, vol. 1. AVI Publishing Co., Westport, Conn. WILSON, D.R., C.J. FERNANDEZ, and K.J. MCCREE. 1978. COz exchange of subterranean clover in variable light environments. Crop Sci. 1829-22. WITHROW, A.P. 1958. Artificial lighting for forcing greenhouse crops. P u r due Univ. Agr. Expt. Sta Bul. 533. WITHROW, A.P. and R.B. WITHROW. 1947. Comparison of various lamp sources for increasing growth of greenhouse crops. Proc. Amer. SOC. Hort. Sci. 49:363-366. WITHROW, R.B. and M.H. RICHMAN. 1933. Artificial radiation as a means of forcing greenhouse crops. Purdue Univ. Agr. Expt. Sta. Bul. 380. WOLFE, W.L. and G.J. ZISSIS (eds.). 1978. The infrared handbook. IRIA Center, Environ. Res. Inst. of Michigan for the Office of Naval Research, Dept. Navy. GPO, Washington, D.C. ZIMMERMAN, R.H., D.T. KRIZEK, W.A. BAILEY, and H.H. KLUETER. 1970. Growth of crabapple seedlings in controlled environments: Influence of seedling age and COz content of the atmosphere. J. Amer. Soc. Hort. Sci. 95:323-325.
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
Index (Volume 2)
Adzuki bean,genetics, 373 Aluminum, deficiency and toxicity symptoms in fruits and nuts, 154 Apple, and light, 240-248 replant disease, 3 root distribution, 453-456 Arsenic, deficiency and toxicity symptoms in fruits and nuts, 154 Asexual embryogenesis, 268- 3 10
Bacteria, and tree short life, 46-47 Boron, deficiency and toxicity symptoms in fruits and nuts, 151-152
Calcium, deficiency and toxicity symptoms in fruits and nuts, 148-149 Chlorine, deficiency and toxicity symptoms in fruits and nuts, 153 Cold hardiness, 33-34 injury, 26-27 Controlled-atmosphere storage, seeds, 134135 Copper, deficiency and toxicity symptoms in fruits and nuts, 153 Cowpea, genetics, 317-348
Deficiency symptoms, in fruit and nut crops, 145-154 Disease, in lettuce, 187-197 Dormancy, 27-30
Embryogenesis, 268- 3 10
Fertilizer, in lettuce, 175-176 nitrogen, 401-404 Fruit crops, nutritional ranges, 143-164 roots, 453-457 short life and replant problem, 1-116 Fungi, and tree short life problem, 47-49
Genetics and breeding, in lettuce, 185-187 and tree short life, 66-70 nitrogen nutrition, 410-411 of Vigna, 311-394 Germination, seed, 117-141, 173-174 Growth substances, 60-66 in embryogenesis, 277-281
Harvesting, in lettuce, 176-181
In uitro embryogenesis, 268-310
propagation, 268-310 Insects, in lettuce, 197-198 short life problem, 52 Iron, deficiency and toxicity symptoms in fruits and nuts, 150 Irrigation, in lettuce industry, 175 root growth, 464-465
Lamps, for plant growth, 514-531 Lettuce, industry, 164-207 Light, and nitrogen nutrition, 406-407 for plant growth, 491-537 in orchards, 208-267 Lighting, for plant growth, 491-537
539
540
HORTICULTURAL REVIEWS
Magnesium, deficiency and toxicity symptoms in fruits and nuts, 148 Manganese, deficiency and toxicity symptoms in fruits and nuts, 150-151 Metabolism, seed, 117-141 Moisture, and seed storage, 125-132 Moth bean, genetics, 373-374 Mung bean, genetics, 348-364 Mycoplasma-like organisms, short life problem, 50-51
Nematodes, in lettuce, 197-198 short life problem, 49-50 Nitrogen, deficiency and toxicity symptoms in fruits and nuts, 146 in embryogenesis, 273-275 nutrition of horticultural crops, 395-423 Nut crops, nutritional ranges, 143-164 Nutrient, concentration in fruit and nut crops, 154-162 media in embryogenesis, 273-281 Nutrition, fruit and nut crops, 143-164
Orchards systems, and light, 208-267 and root growth, 469-470
Peach, short life, 4 Pear, decline, 11 root distribution, 456 short life, 6 Phosphorus, deficiency and toxicity symptoms in fruits and nuts, 146-147 Photosynthesis, and light, 237-238 Physiology, of embryogenesis, 268-310 of seed, 117-141 Phytotoxins, 53-56 Plant protection, short life, 79-84 Postharvest physiology, in lettuce, 181-185 seed, 117-141 Potassium, deficiency and toxicity symptoms in fruits and nuts, 147-148 Pruning, and light interception, 250-251 Prunus, root distribution, 456
Replant problem, deciduous fruit trees, 1116 Rice bean, genetics, 375-376 Roots, and tree crops, 424-490 Rootstock, and light interception, 249-250 and root systems, 471-474 and short life, 70-75
Seed, research in lettuce, 166-174 viability and storage, 117-141 Short life problem, fruit crops, 1-116 Sodium, deficiency and toxicity symptoms in fruits and nuts, 153-154 Soil management, and root growth, 465-469 Storage, of seed, 117-141 Stress on plants, 34-37 Sulfur, deficiency and toxicity symptoms in fruits and nuts, 154 Symptoms, deficiency and toxicity of fruits and nuts, 145-154
Temperature, plant growth, 36-37 and seed storage, 132-133 Tissue culture, 268-310 Toxicity symptoms, in fruit and nut crops, 145-154 Tree crops, roots, 424-490 Tree decline, 1-116
Urd bean, genetics, 364-373
Vigna, genetics, 31 1-394 Viruses, short life problem, 50-51
Water, and light in orchards, 248-249 Weed in lettuce, lg8
Zinc, deficiency and toxicity symptoms in fruits and nuts, 151
Horticultural Reviews Edited by Jules Janick © Copyright 1980 The AVI Publishing Company, Inc.
Cumulative Index (Volumes 1-2 Inclusive)
Abscission, anatomy and histochemistry, 1: 172-203 Adzuki bean, genetics, 2:373 Alternate bearing, chemical thinning, 1: 285-289 Aluminum, deficiency and toxicity symptoms in fruits and nuts. 2:154 Anatomy and morphology, embryogenesis, 1:4-21, 35-40 fruit abscission, 1:172-203 fruit storage, 1:314 petal senescence, 1:212-216 Angiosperms, embryogenesis in, 1:l-78 Apple, CA storage, 1:303-306 chemical thinning, 1:270-300 fertilization, 1:105 fire blight control, 1:423-474 light, 2:240-248 replant disease, 2:3 root distribution, 2:453-456 yield, 1:397-424 Apricot, CA storage, 1:309 Arsenic, deficiency and toxicity symptoms in fruits and nuts, 2:154 Artichoke, CA storage, 1:349-350 Asexual embryogenesis, 1:1-78; 2:268-310 Asparagus, CA storage, 1:350-351 Avocado, CA storage, 1:310-311
Bacteria, short life problem, 2:46-47 Bacteriocides, fire blight, 1:450-459 Bacteriophage, fire blight control, 1:449450 Banana, CA storage, 1:311-312 fertilization, 1:105 Bean, CA storage, 1:352-353 Bedding plants, fertilization, 1:99-100 Beet, CA storage, 1:353 Begonia (Rieger), fertilization, 1:104 Boron, deficiency and toxicity symptoms in fruits and nuts, 2:151-152
Broccoli, CA storage, 1:354-355 Brussels sprouts, CA storage, 1:355
Cabbage, CA storage, 1:355-359 fertilization, 1:117-118 Calcium, deficiency and toxicity symptoms in fruits and nuts, 2:148-149 Carnation, fertilization, 1:100 Carrot, CA storage, 1:362-366 Cauliflower, CA storage, 1:359-362 Celeriac, CA storage, 1:366-367 Celery, CA storage, 1:366-367 Cherry, CA storage, 1:308 Chicory, CA storage, 1:379 Chlorine, deficiency and toxicity symptoms in fruits and nuts, 2:153 Chrysanthemum fertilization, 1:100-101 Citrus, CA storage, 1:312-313 fertilization, 1:105 rootstock, 1:237-269 Cold hardiness, 2:33-34 injury, 2:26-27 Controlled-atmosphere storage, fruits, 1: 301-336 seeds, 2:134-135 vegetables, 1:337-394 Copper, deficiency and toxicity symptoms in fruits and nuts, 2:153 Cowpea, genetics, 2:317-348 Cranberry, fertilization, 1:106 Cucumber, CA storage, 1:367-368
Deficiency symptoms, in fruit and nut crops, 2:145-154 Delicious apple, 1:397-424 Disease, in lettuce, 2:187-197 Dormancy, 2:27-30
541
542
HORTICULTURAL REVIEWS
Embryogenesis, 1:l-78; 2:268-310 Energy, efficiency in controlled environment agriculture, 1:141- 171 Environment, controlled for energy efficiency, 1:141-171 fruit set, 1:411-412 in embryogenesis, 1:22, 43-44 Erwinia amylouora, 1:423-474 Ethylene, CA storage, 1:317-319, 348
Fertilizer, controlled-release, 1:79-139 in lettuce, 2:175-176 nitrogen, 2:401-404 Fire blight, 1:423-474 Floricultural crops, fertilization, 1:98-104 postharvest physiology, 1:204-236 senescence, 1:204-236 Flower, senescence, 1:204-236 Foliage plants, fertilization, 1:102-103 Frost, and apple fruit set, 1:407-408 Fruit, abscission, 1:172-203 set (apple), 1:397-424 size and thinning, 1:293-294 Fruit crop fertilization, 1:104-106 nutritional ranges, 2: 143-164 roots, 2:453-457 short life and replant problem, 2:l-116 Fungi, short life problem, 2:47-49 Fungicide, and apple fruit set, 1:416
In uitro embryogenesis, 1:l-78; 2:268-310
Insects, in lettuce, 2:197-198 short life problem, 2:52 Iron, deficiency and toxicity symptoms in fruits and nuts, 2:150 Irrigation, in lettuce industry, 2:175 root growth, 2:464-465
Lamps, for plant growth, 2:514-531 Leek, CA storage, 1:375 fertilization, 1:118 Lemon, rootstock, 1:244-246 Lettuce, CA storage, 1:369-371 fertilization, 1:118 industry, 2:164-207 Light, and fruit set, 1:412-413 and nitrogen nutrition, 2:406-407 for plant growth, 2:491-537 in orchards, 2:208-267
Magnesium, deficiency and toxicity symptoms in fruits and nuts, 2:148 Mandarin, rootstock, 1:250-252 Manganese, deficiency and toxicity symptoms in fruits and nuts, 2:150-151 Mango, CA storage, 1:313 Metabolism, flower, 1:219-223 seed, 2:117-141 Moisture, and seed storage, 2:125-132 Moth bean, genetics, 2:373-374 Mung bean, genetics, 2:348-364 Mushroom, CA storage, 1:371-372 Muskmelon, fertilization, 1:118-119 Mycoplasma-like organisms, short life problem. 2:50-51
Garlic, CA storage, 1:375 Genetics and breeding, and embryogenesis, 1:23 and short life, 2:66-70 fire blight resistance, 1:435-436 flower longevity, 1:208-209 in lettuce, 2:185-187 nitrogen nutrition, 2:410-411 Nectarine, CA storage, 1:309-310 of Vigna, 2:311-394 Nematodes, in lettuce, 2:197-198 Germination, seed, 2:117-141, 173-174 short life problem, 2:49-50 Grape, CA storage, 1:308 Nitrogen, deficiency and toxicity symptoms Greenhouse, energy efficiency, 1:141-171 in fruits and nuts, 2:146 Growth substances, 2:60-66 in embryogenesis, 2:273-275 apple fruit set, 1:417 nutrition of horticultural crops, 2:395-423 apple thinning, 1:270-300 Nursery crop, fertilization, 1:106-112 CA storage in vegetables, 1:346-348 Nut crops, fertilization, 1:106 in embryogenesis, 1:41-43; 2:277-281 nutritional ranges, 2:143-164 Nutrient, concentration in fruit and nut crops, 2:154-162 media, in embryogenesis, 2:273-281 Nutrition, and embryogenesis, 1:40-41 Harvesting, flower stage, 1:211-212 and fire blight, 1:438-441 in lettuce, 2:176-181 and fruit set, 1:414-415 Histochemistry, fruit abscission, 1:172-203 fruit and nut crops, 2:143-164 Horseradish, CA storage, 1:368 slow-release fertilizers, 1:79-139
CUMULATIVE INDEX (VOLUMES 1-2 INCLUSIVE) Okra, CA storage, 1:372-373 Onion, CA storage, 1:373-375 Orange, sour, rootstock, 1:242-244 sweet, rootstock, 1:252-253 trifoliate, rootstock, 1:247-250 Orchard systems, and light, 2:208-267 and root growth, 2:469-470 Ornamental plants, fertilization, 1:98-104, 106-116
Papaya, CA storage, 1:314 Parsley, CA storage, 1:375 Peach, CA storage, 1:309-310 short life, 2:4 Pear, CA storage, 1:306-308 decline, 2: 11 fire blight control, 1:423-474 root distribution. 2:456 short life, 2:6 Pecan, fertilization, 1:106 Pepper, CA storage, 1:375-376 fertilization, 1:119 Persimmon, CA storage, 1:314 Pest control, fire blight, 1:423-474 Pesticide, and fire blight, 1:450-461 Phosphorus, deficiency and toxicity symptoms in fruits and nuts, 2:146-147 Photosynthesis, and light, 2:237-238 Physiology, cut flower, 1:204-236 of embryogenesis, 1:21-23; 2:268-310 of seed, 2:117-141 Phytotoxins, 2:53-56 Pigmentation, flower, 1:2 16-219 Pineapple, CA storage, 1:314 Plant protection, short life, 2:79-84 Plum, CA storage, 1:309 Poinsettia, fertilization, 1:103-104 Pollination, and embryogenesis, 1:21-22 apple, 1:402-404 Postharvest physiology, cut flower, 1:204236 fruit, 1:301-336 in lettuce, 2:181-185 seed, 2:117-141 vegetables, 1:337-394 Potassium, deficiency and toxicity symptoms in fruits and nuts, 2:147-148 Potato, CA storage, 1:376-378 fertilization, 1:120-121 Pruning, and light interception, 2:250-251 and training, on apple yield, 1:414 on fire blight, 1:441-442 Prunus, root distribution, 2:456
Radish, fertilization, 1:121 Replant problem, deciduous fruit trees, 2: 1-116
543
Respiration, fruit in CA storage, 1:315-316 vegetables in CA storage, 1:341-346 Rice bean, genetics, 2:375-376 Roots, and tree crops, 2:424-490 Rootstock, and fire blight, 1:432-435 and light interception, 2:249-250 and root systems, 2:471-474 and short life, 2:70-75 apple, 1:405-407 citrus, 1:237-269 Rose, fertilization, 1:104
Scoring, and fruit set, 1:416-417 Seed, abortion, 1:293-294 research in lettuce, 2:166-174 viability and storage, 2:117-141 Senescence, cut flower, 1:204-236 petal, 1:212-216 Short life problem, fruit crops, 2:l-116 Small fruit, CA storage, 1:308 Sodium, deficiency and toxicity symptoms in fruits and nuts, 2:153-154 Soil management, and root growth, 2:465469 Storage, of seed, 2:117-141 Strawberry, fertilization, 1:106 Stress on plants, 2:34-37 Sulfur, deficiency and toxicity symptoms in fruits and nuts, 2:154 Sweet potato, fertilization, 1:121 Symptoms, deficiency and toxicity of fruits and nuts, 2:145-154
Temperature, and apple fruit set, 1:408411 and CA storage of vegetables, 1:340-341 and fire blight forecasting, 1:456-459 and seed storage, 2:132-133 plant growth, 2:36-37 Thinning, apple, 1:270-300 Tissue culture, 1:l-78; 2:268-310 Tomato, CA storage, 1:380-386 fertilization, 1:121-123 Toxicity symptoms, in fruit and nut crops, 2:145-154 Tree crops, roots, 2:424-488 Tree decline, 2:l-116 Turfgrass, fertilization, 1:112-117 Turnip, fertilization, 1:123-124
Urd bean, genetics, 2:364-373
544
HORTICULTURAL REVIEWS
Vegetable crops, CA storage, 1:337-394 fertilization, 1:117-124 Vigna, genetics, 2:311-394 Viruses, short life problems, 2:50-51
Water, and light in orchards, 2:248-249
Watermelon, fertilization, 1:124 Weed research, in lettuce, 2:198
Zinc, deficiency and toxicity symptoms in fruits and nuts, 2:151
