Plant Breeding Reviews (Volume 35)

PLANT BREEDING REVIEWS Volume 35

Plant Breeding Reviews is sponsored by: American Society of Horticultural Science International Society for Horticultural Science Society of American Foresters National Council of Commercial Plant Breeders

Editorial Board, Volume 35 I. L. Goldman C. H. Michler Rodomiro Ortiz

PLANT BREEDING REVIEWS Volume 35

edited by

Jules Janick Purdue University

Copyright Ó 2012 by Wiley-Blackwell. All rights reserved. Published by John Wiley & Sons, Inc., Hoboken, New Jersey. Published simultaneously in Canada. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientific, Technical, and Medical business with Blackwell Publishing. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400, fax 978-750-4470, or on the web at www.copyright.com. Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, 201-748-6011, fax 201-748-6008, or online at http://www.wiley.com/go/permission. Limit of Liability/Disclaimer of Warranty: While the publisher and author have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives or written sales materials. The advice and strategies contained herein may not be suitable for your situation. You should consult with a professional where appropriate. Neither the publisher nor author shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. For general information on our other products and services or for technical support, please contact our Customer Care Department within the United States at 877-762-2974, outside the United States at 317-572-3993 or fax 317- 572-4002. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic formats. For more information about Wiley products, visit our web site at www.wiley.com. Library of Congress Cataloging-in-Publication Data ISBN 978-1-118-09679-6 (cloth) ISSN 0730-2207 Printed in the United States of America eBook ISBN: 978-1-118-10048-6 oBook ISBN: 978-1-118-10050-9 ePub ISBN: 978-1-118-10049-3 10 9 8 7 6 5 4 3 2 1

Contents

Contributors 1. Dedication: Molly M. Jahn Plant Breeder and Geneticist

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I. L. Goldman I. Biographical Sketch II. Research Program III. Teaching IV. Administration V. Awards and Recognition VI. The Woman Literature Cited Selected Publications of Molly M. Jahn Germplasm Releases and Patents

2. History, Evolution, and Domestication of Brassica Crops

1 5 7 7 9 9 10 10 16

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Shyam Prakash, Xiao-Ming Wu, and S. R. Bhat I. Introduction II. Archetypes and Evolution of Basic Genomes and Derived Allopolyploids III. Ethnobotany, Origin, and Domestication IV. Concluding Remarks Acknowledgments Literature Cited

21 25 36 67 70 71

v

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CONTENTS

3. Melon Landraces of India: Contributions and Importance Narinder P. S. Dhillon , Antonio J. Monforte, Michel Pitrat, Sudhakar Pandey, Praveen Kumar Singh, Kathleen R. Reitsma, Jordi Garcia-Mas, Abhishek Sharma, and James D. McCreight

I. Introduction II. First Contribution of Indian Melon Germplasm to the U.S. Melon Breeding Programs III. Useful Traits from Indian Melons IV. Genetic Diversity V. Melon Breeding VI. Future Role of Indian Melon Germplasm and Conclusions Acknowledgments Literature Cited

4. Transgenic Vegetable Crops: Progress, Potentials, and Prospects

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88 90 92 120 123 130 133 133

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Jo~ ao Silva Dias and Rodomiro Ortiz I. World Vegetable Production II. Case for Transgenic Vegetables III. Case Studies IV. GM Vegetables and Integrated Pest Management V. Outlook Literature Cited

5. Millets: Genetic and Genomic Resources

153 154 164 218 221 224

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Sangam Dwivedi, Hari Upadhyaya, Senapathy Senthilvel, Charles Hash, Kenji Fukunaga, Xiamin Diao, Dipak Santra, David Baltensperger, and Manoj Prasad I. Introduction II. Nutritional Quality and Food, Feed, Medicinal, and Other Uses III. Domestication, Phylogenetic, and Genomic Relationships

251 269 277

CONTENTS

IV. Assessing Patterns of Diversity in Germplasm Collections V. Identifying Germplasm with Beneficial Traits VI. Genomic Resources VII. Enhancing Use of Germplasm in Cultivar Development VIII. From Trait Genetics to Association Mapping to Cultivar Development Using Genomics IX. Conclusions and Future Prospects Acknowledgments Literature Cited

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284 300 316 321 332 344 347 347

Subject Index

377

Cumulative Subject Index

379

Cumulative Contributor Index

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Contributors

David Baltensperger, Soil and Crop Sciences, Texas A&M University, 2472 TAMU, College Station, Texas 77840, USA S. R. Bhat, National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi 110012, India Narinder P. S. Dhillon, Present address: AVRDC-The World Vegetable Center, East and Southeast Asia, P.O. Box 1010 (Kasetsart), Bangkok 10903, Thailand Xiamin Diao, Lab of Minor Cereal Crops, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, 12 Zhongguancun South Street, Haidian, Beijing 100081, People’s Republic of China Sangam Dwivedi, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru PO, Hyderabad 502324, AP, India Kenji Fukunaga, Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, 562 Nanatsuka, Shobara, Hiroshima 727-0023, Japan Jordi Garcia-Mas, Institut de Recerca i Tecnologia Agroaliment
aries, Centre for Research in Agricultural Genomics (CSIC-IRTA-UAB), Ctra de Cabrils Km 2, E-08348 Cabrils, Spain I. L. Goldman, Department of Horticulture, University of Wisconsin–Madison, 1575 Linden Drive, Madison, Wisconsin 53706, USA Charles Hash, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru PO, Hyderabad 502324, AP, India James D. McCreight, U.S. Department of Agriculture, Agricultural Research Service, U.S. Agricultural Research, 1636 East Alisal St., Salinas, California 93905, USA Antonio J. Monforte, Instituto de Biologıa Molecular y Celular de Plantas (IBMCP), Universidad Politecnica de Valencia–Consejo, Superior de Investigaciones Cientificas, Ciudad Politecnica de la Innovacio´n, Edificio 8E, Ingenierio Fausto Elio s/n, 46022 Valencia, Spain Rodomiro Ortiz, Department of Plant Breeding and Biotechnology, Swedish University of Agricultural Sciences, P.O. Box 101, SE-230 53 Alnarp, Sweden Sudhakar Pandey, Indian Institute of Vegetable Research, P.B. No. 01, PO– Jakhini (Shahanshahpur), Varanasi 221 305, India Michel Pitrat, Institut National de la Recherche Agronomique (INRA), UR1052, Genetique et Amelioration des Fruits et Legumes, BP 94, F-84143 Montfavet Cedex, France ix

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CONTRIBUTORS

Shyam Prakash , National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi 110012, India Manoj Prasad, National Institute of Plant Genome Research, Aruna Asaf Ali Marg, JNU Campus, PO Box 10531, New Delhi 110067, India Kathleen R. Reitsma, U.S. Department of Agriculture, Agricultural Research Service, North Central Regional Plant Introduction Station, Iowa State University, Ames, Iowa 50011-1170, USA Dipak Santra, University of Nebraska–Lincoln, Panhandle Research and Extension Center, 4502 Avenue 1, Scottsbluff, Nebraska 69361, USA Senapathy Senthilvel, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru PO, Hyderabad 502324, AP, India Abhishek Sharma, Department of Vegetable Crops, Punjab Agricultural University, Ludhiana 141 004, India Jo~ ao Silva Dias, Technical University of Lisbon, Instituto Superior de Agronomia, Tapada da Ajuda, 1349-017 Lisboa, Portugal Praveen Kumar Singh, Indian Institute of Vegetable Research, Regional Station, Sargatia, Kushinagar 274 406, UP, India Hari Upadhyaya, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru PO, Hyderabad 502324, AP, India Xiao-Ming Wu, Oil Crops Research Institute of Chinese Academy of Agricultural Sciences, Wuhan 430062, People’s Republic of China



Deceased

Plate 2.1 Phenotypes of different varieties of B. oleracea: (a,b) var. acephala; (c) var. oleracea (wild type collected from Spain); (d) var. capitata; (e) var. botrytis; (f) var. italica; (g) var. caulorapa; (h) var. alboglabra.

Plate 2.2 IllustrationsofcolecropsandturnipfromtheJulianaAniciaCodex(512 CE)basedon Dioscorides: (a) Krambe hemeros ¼ cultivated krambe [Brassica oleracea]; (b) Krambe agria ¼ wild krambe [B. cretica]; (c) Gagguli [B. rapa]. (Source: Der Wiener Dioskurides 1998, 1999).

Plate 2.3 Phenotypes of vegetable and oilseed variants of Chinese B. rapa: (a) var. chinensis; (b) var. parachinensis; (c) var. narinosa; (d) var. purpurea; (e) var. chinensis; tai-tsa; (f) var. oleifera; (g, h) var. pekinensis; (i) var. parachinensis; (j) var. narinosa.

Plate 2.4 Phenotypes of Chinese vegetable and oil variants of B. juncea: (a, b, h, j) leaf mustard var. multiceps; (c, d) stem mustard var. tsatsai; (e, f, k) root mustard var. megarrhiza; (g, i) stalk mustard var. utilis; (l) oil mustard var. oleifera.

Plate 3.1 Representative fruits of nondessert melon landraces of India: (1) var. acidulus, (2) var. flexuosus, (3) var. chate, (4) var. momordica, (5) cv. Wanga (var. chate?), (6) semidomesticated and ‘‘wild’’ melons.

1 Dedication: Molly M. Jahn Plant Breeder and Geneticist I. L. Goldman Department of Horticulture University of Wisconsin—Madison 1575 Linden Drive Madison, Wisconsin 53706, USA I. BIOGRAPHICAL SKETCH II. RESEARCH PROGRAM III. TEACHING IV. ADMINISTRATION V. AWARDS AND RECOGNITION VI. THE WOMAN LITERATURE CITED SELECTED PUBLICATIONS OF MARGARET M. JAHN GERMPLASM RELEASES AND PATENTS

Volume 35 of Plant Breeding Reviews is dedicated to the illustrious career of Molly M. Jahn, Molly is a dynamic leader in plant breeding, and her career is an inspiration to a new generation of students entering this profession. I. BIOGRAPHICAL SKETCH Molly Jahn was born June 4, 1959, and raised near Detroit, Michigan. As a child, she was fascinated by nature and field biology. A serious illness that kept her hospitalized in Ann Arbor, Michigan, for a long period gave her time to think, and when she recovered, she was determined to pursue a career as a biologist.1 Avery bright student, Molly was selected as the Midwest Scholar at Swarthmore College. Her start as a geneticist was, however, a humbling one. After failing her first genetics test, her professor, John B. Jenkins, asked her if she had studied. When Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick. Ó 2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 1

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she replied that she had studied diligently for the exam, he replied that students who did poorly either were not very bright or did not know how to study, hoping it was the latter. He allowed her to come to see him once each week with a list of questions, which she did faithfully. Soon he offered her a job doing lab preparations, and later he served as the mentor who encouraged her to apply for a National Science Foundation fellowship to attend graduate school and to apply to at least one graduate school. Numerous examples in Molly’s academic career show incredibly successful outcomes emerging from simple beginnings, and these are a testament to her drive, determination, and vision. It is rare to find a scientist like Molly Jahn who combines high intellect and a strong sense of purpose with such an intuitive sense of the future and its possibilities. Throughout this chapter, specific events and turning points in Molly Jahn’s career are identified from descriptions she provided in an interview for the book Democracy and Higher Education (Peters et al. 2010). Molly was awarded the NSF fellowship and was admitted to graduate study at the Massachusetts Institute of Technology (MIT), where she set off to pursue her interest in genetics, integrating the avalanche of molecular insights of the time in a system that would have some applied relevance. Several faculty members at MIT were extremely influential in helping her shape her scientific priorities and experimental approaches, notably Phil Sharp and Frank Solomon. But while visiting her parents back in Michigan, she picked up a book about her maternal greatgrandfather Saunders and his four brothers, each of whom had made major contributions in plant breeding and related agricultural sciences under the tutelage of their father, William Saunders. Her great-grandfather had a distinguished career as a physicist at Harvard, and the family still met regularly for large reunions at Hamilton College, where one of the brothers had been a chemist and a successful peony breeder. Another brother, Charles, together with his father bred ‘Marquis’ wheat, a shortseason cultivar that opened the western Canadian plains for settlement. When the Canadian Parliament committed to a federal agricultural research system in Canada, her great-great-grandfather served as the founding director of the experiment station in Ottawa, Canada, for agricultural research where her great-grandfather, the youngest son, was raised. Much as Molly was drawn to the rigor and excitement of molecular genetics at MIT, she was also drawn to the practical relevance of genetics toward crop improvement. In 1983, she made the difficult decision to shift graduate programs, bringing the background she had acquired to agriculture. So it was with a combination of heredity, aptitude, and good luck that Molly found her way to Cornell University in 1983 to begin graduate work in plant breeding.

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After moving to Ithaca, New York, Molly, following the example of one of her mentors at MIT, looked for a system where she could study mutations that conferred resistance to plant viral disease with the idea that these mutations likely would occur in genes of both fundamental and practical interest. She was particularly focused on genes or gene clusters that appeared to control resistance to sets of viruses, and all paths led to the largest family of plant viruses, the Potyviridae. Because of the role that vegetables play in the developing world and because of their genetic and botanical diversity, she was interested in finding an example of this phenomenon in a vegetable species and eventually settled on the I gene in Phaseolus vulgaris. To work on this problem, she became the student of Michael H. Dickson, a noted breeder of Phaseolus, Brassica, and carrots. From her very earliest days at Cornell, Henry Munger was a key mentor, co-chair of her graduate committee. Ultimately it was his position at Cornell that she filled, appointed in the spring of 1987 as an assistant professor in the Department of Plant Breeding. She received her Ph.D. from Cornell in early 1988 and was allowed to defer her faculty appointment to accept a prestigious postdoctoral fellowship, the Life Sciences Research Foundation fellowship, which she took to the laboratories of Drs. T. J. Morris and A. O. Jackson in the Department of Plant Pathology at the University of California—Berkeley and S. H. Howell at the Boyce Thompson in Ithaca, New York, prior to joining the Cornell faculty in 1991. Although Molly’s primary appointment was in the Department of Plant Breeding, eventually she also held a faculty appointment in the Department of Plant Biology. She assumed responsibility for the germplasm that had been developed by Henry Munger and was an outstanding steward of this important legacy in U.S. vegetable breeding, eventually releasing dozens of varieties, parents, and breeding lines with Munger. Molly and her students and staff worked primarily on Cucurbita, Cucumis, and Capsicum, conducting field-oriented plant breeding and basic laboratory research. Her research laboratory grew to include more than 30 scientists, staff, and students and was supported by a wide variety of funding sources, including federal agencies, contracts, and gifts from seed companies, royalties, private foundations, and significant gifts from individual donors with whom she developed close ties. Special among these were Paul H. Todd, a Cornell graduate and gifted chemist who was interested in her work on peppers, and Charles M. Werly. Molly’s research programs were widely recognized for their breadth and depth and were an ideal training ground for a large number of students, many of whom went on to careers in plant breeding in both the public and private sectors. Her work in plant breeding and plant genetics led to pioneering discoveries related to plant disease resistance and

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quality traits. Furthermore, germplasm releases from her program are now grown commercially on six continents under approximately 60 active commercial licenses. ‘Cornell’s Bush Delicata,’ for example, was named an All America Selection. This achievement was especially notable in that this open-pollinated cultivar combined the best characteristics of an heirloom on a compact, disease-tolerant, highly productive squash and was recognized because it outperformed the best hybrids on the market at the time for both yield and quality. More recently, a cucumber cultivar was noted with the MGA Green Thumb award, and Molly’s licenses now generate royalties that help support the breeding program now led by her student, Dr. Michael Mazourek, an assistant professor at Cornell University. Always committed to ensuring that her work benefited agriculture, Molly worked closely with Cooperative Extension where possible and filled this role herself where budget cuts had resulted in gaps. Because of this commitment to ensuring growers and seed companies had the full benefit of her work, she learned early how important detailed communication and strong partnerships were to her success. As she established herself in basic research, she consistently directed major grants in genomics towards outreach and impact. Molly’s long-term partnerships with George Moriarty, a Research Support Specialist in Plant Breeding and Genetics, and Henry Munger, Professor Emeritus, have been key to the development of so much useful germplasm in the Cornell program along with many key long term staff notably Mary Lyons Kreitinger. Under Henry Munger’s influence with strong support from long-time department chair Ronnie Coffman, Molly committed early to international engagement and has had active research relationships in many countries including Afghanistan, Argentina, Austria, Bangladesh, Brazil, Burkina Faso, Chile, China, Costa Rica, Egypt, Ethiopia, France, Ghana, Greece, Honduras, Hungary, India, Indonesia, Israel, Jordan, Kenya, Mali, Mexico, the Netherlands, Pakistan, Portugal, the Philippines, South Korea, Spain, Sweden, Thailand, Taiwan, Tunisia, Turkey, and South Africa. She welcomed international scholars and students and strongly encouraged U.S. students to acquire international experience. Many have continued their commitment to international engagement and agricultural research. These efforts have resulted in the transfer of many important traits from the Cornell program for use in national programs and seed companies all over the world and sparked ongoing interest in underinvested and indigenous types and species. Molly also worked with the McKnight Foundation for a decade as a charter member of the Oversight Committee of Collaborative Crops.

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II. RESEARCH PROGRAM Beginning with her dissertation research, Molly’s focus on genetics of disease resistance in plants resulted in many publications with two pronounced themes. First, she provided key evidence of the importance of the host translation factor, eIF4E, in virus resistance and provided the first example in plants of a bimolecular interaction whose outcome determined infectivity. This work began with the classical identification and revision of known genes for recessive disease resistance in pepper and concluded with isolation of a series of allelic variants at this gene that varied in the range of isolates controlled. This work was based on a murine model, further establishing the relevance of mammalian model systems for crop improvement. A key observation that defines another important first in plant genetics and plant virology was that eIF4E variants driven by a strong promoter could confer dominant negative disease resistance, despite the presence of a wild-type allele in the cell. A second theme was focused on the organization of disease-resistant genes in the genome. In contrast to prevailing ideas that suggested that the evolutionary pressure on disease resistance loci would lead to rapid diversification and scrambling of these regions of plant genomes, Molly’s laboratory showed conservation of these positions across genera in the Solanaceae, culminating in a definitive study published in 2009 that demonstrated that these loci are conserved across wide evolutionary distances while diversification of specificity occurs frequently even within narrowly defined germplasm pools. The significance of her fundamental research into both the structure and the function of plant disease-resistance genes earned her a berth on the Plant Cell Editorial Board in 2004 and service on the executive committee and as chair of the Plant-Microbe Subcommittee. Another area of fundamental inquiry and significant impact has been her efforts to identify the molecular basis for quality traits in Capsicum, notably color and pungency. She and colleagues used a candidate gene approach to efficiently identify genes with both qualitative and quantitative effects on fruit color in Capsicum, resulting in a widely cited publication. More notable, however, is the definitive work from her laboratory over a decade that defined and mapped loci responsible for both qualitative and quantitative variation in pungency including the C or Pun1 locus for presence/absence of pungency. Capsaicinoid biosynthesis in pepper represents an ideal model to study the appearance of unique and evolutionarily significant metabolic capacities in plants with significant implications for the culinary and pharmacological uses of a number of Capsicum spp.

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In addition to research, student training, and teaching, Molly pioneered a number of new models for public-private partnerships at land grant institutions. These models were based in part on her own experience at Cornell with the licensing of plant germplasm to commercial companies. Those companies became fewer and fewer by the late 1990s, as consolidation whittled the vegetable seed industry down to several major players in the global marketplace. Molly and her colleagues created the Public Seed Initiative (PSI), a mechanism for bringing smaller seed companies and growers together with public sector germplasm. The PSI was, in a sense, a traditional model of cooperation among growers and public sector researchers and allowed for both conventional and organic producers to source public seed. Through the efforts of the PSI, greater connections have been made between smallerscale growers and seed companies, facilitating the marketplace for specialized seed. This has been accomplished through farm-based trials of public sector cultivars and enhanced relationships with Extension educators, who then translate the information to growers in new ways. As part of this project, Molly became aware of an important market in the northeastern United States that was almost entirely underserved by the public sector research establishment, namely organic agriculture. She was a public sector pioneer in the area of breeding and selection in and for organically managed production systems. In 2004, she was awarded the largest federal grant of its kind at the time to establish the Organic Seed Partnership, an effort to integrate public and private sector research efforts with large participatory networks for selection in organically managed production environments and trialing. This effort involves hundreds of farmers across the country connected to public and private sector research programs with particular emphasis on smaller companies with limited research capacities. Molly and her colleagues at Cornell were also instrumental in creating and maintaining the Vegetable Breeding Institute (VBI). The VBI works to assure the continued development of improved vegetable breeding lines and varieties to meet future needs of the vegetable industry and the general public. Through the VBI, which includes faculty from Cornell and, more recently, the University of Wisconsin—Madison, vegetable breeding programs train graduate and undergraduate students to become capable vegetable breeders of the future. The VBI currently has more than two dozen member companies that help support these objectives and participate in yearly field days to exchange information with public sector breeders. Molly Jahn has been a strong advocate for funding and support of plant breeding activities in the public sector. While many public plant

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breeders have lamented the lack of funding for their work, Molly always challenged this notion by arguing that if the work is worth doing and can intersect with strong science and the private sector, resources should be available. Her advocacy helped foster support for plant breeding programs at Cornell and later at the University of Wisconsin—Madison as well as nationally through her work at the United States Department of Agriculture. Molly’s influence has also been to encourage plant breeders and other agricultural scientists to think about the societal impacts of their research and to consider the vitality of the rural economy when planning their work.

III. TEACHING Molly’s core teaching was focused around plant genetics, and the class she taught for many years in that subject at Cornell was a mainstay for graduate students in the field. Plant genetics has become a remarkably active field in the last several decades due to an infusion of insights gained from molecular biology and molecular genetics. Molly was able to incorporate these elements into her courses and bring the best of modern plant genetics to her students. Molly is widely known for thinking far ahead for solutions to problems, and she brought this perspective to her teaching. Characteristic of Molly’s approach was the integration of information gained from other fields, such as mammalian biology, physical sciences, and ecology, into her core subjects. This syncretic format had great benefits for her students, who broadened and deepened their learning and gained valuable insight into the pursuit of knowledge. Molly also taught sophomore plant genetics and many other courses in plant biology during her years at Cornell and is widely regarded as a challenging and beloved instructor by graduate students. She also mentored 14 postdoctoral scientists, 13 international visiting scientists, and served as the major advisor to 19 graduate students during her years at Cornell. As testament to her tireless efforts at mentoring, her former students and mentees characterize Molly’s fierce support of their learning and research projects as absolutely transformative in their education.

IV. ADMINISTRATION In 2006, Molly Jahn was recruited to be dean of the College of Agricultural and Life Sciences and director of the Wisconsin Agricultural Experiment Station at the University of Wisconsin—Madison. Her faculty

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affiliations at Wisconsin are with the Department of Genetics and the Department of Agronomy. Her work there has focused on revitalizing the partnership between the research powerhouse in the College of Agricultural and Life Sciences and the highly varied constituency the college serves. She has been incredibly effective at increasing the resource base of the college, presiding over a substantial increase in extramural funding during her deanship. She also was a driving force behind modernizing administrative and departmental structures and introducing new concepts aimed at improving the efficiency of the use of state resources. Molly is also very well known for serving as an advocate for production agriculture, forestry, the life sciences and higher education in the state. She developed new models for bringing rural students to study at Madison and has championed the cause of curricular reform to capitalize on efficiencies and natural alliances among the sciences. Toward this end, new models for biology instruction, a new major in environmental sciences, a simplified and streamlined degree structure, and reaccreditation of all college-accredited degree programs and animal research were secured. New initiatives in global health, internationalization of curriculum and pre-professional advising in health sciences were launched, and 50 new faculty members were hired, many of whom were recruited to fill new faculty roles. During her deanship, major capital commitments to update facilities and expand infrastructure were secured, including major renovation of Babcock Hall, new construction for the Wisconsin Energy Institute, and a plan for a new Meat and Muscle Biology Laboratory. Emphasizing responsiveness and a strong sense of the land grant mission, Molly has established herself as an important voice in the nearly $60 billion agricultural industry of the state of Wisconsin. Molly also played an instrumental role in developing the Great Lakes Bioenergy Research Center and the Wisconsin Bioenergy Initiative, which together represent close to $200 million in federal and state investment in bioenergy research and outreach. These efforts began in 2007 and are already paying large dividends for the state of Wisconsin and the nation as researchers investigate the potential for biomass-derived energy and the potential trade-offs and synergies, should relevant technologies be commercialized and implemented at scale. In late 2009, Molly took a leave of absence from the University of Wisconsin to serve on a formal loan to the federal government to provide interim leadership at U.S. Department of Agriculture in Washington, D.C., in the mission area of Research, Education, and Economics, initially as Deputy Under Secretary and, effective as of the departure of Dr. Rajiv Shah, subsequently as Acting Under Secretary for

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Research, Education, and Economics. Her work in Washington brought together many of her skills and talents to help advance the science agenda for agriculture, forestry, food safety, nutrition, and environmental sciences during the early phase of the Obama administration. Molly returned to the deanship in Madison on June 1, 2010, and continued through the end of December, 2010. In January, 2011, she took on a brandnew challenge as she transitioned from the deanship to Special Advisor to the Chancellor and Provost for Sustainability Sciences. In this role Molly returned to a more substantial focus on the science that will support decision making with respect to land management strategies, the deployment of innovations on landscapes and our food and energy future.

V. AWARDS AND RECOGNITION Molly Jahn has received numerous awards in her career, among them fellowship in the American Association for the Advancement of Science, the Vegetable Breeding Award of Excellence from the American Society for Horticultural Science, the Wisconsin Dairy Communicator of the Year from the Wisconsin Dairy Business Association, the Service to Industry Award from the Wisconsin State Cranberry Association, a major teaching award at Cornell University, the National Garden Bureau Gold Medal for the winter squash cultivar ‘Bush Delicata’, and the MGA Green Thumb award for her cucumber variety Salt and Pepper. She is widely recognized as a leader in the fields of vegetable breeding and sustainability science and is considered one of the country’s most important voices on the continued relevance of the land grant university in today’s world.

VI. THE WOMAN Molly Jahn is widely known as a visionary leader in the areas of plant breeding, sustainable agriculture and sustainability sciences, and international development, and has been a national and international presence in these fields for many years. She exhibits limitless energy, intellectual brilliance, and a vision for the future that set her apart from her peers. She has served as an inspiration to students, visiting scientists, and colleagues in both science and policy, and her opinions are sought by leaders across a wide spectrum of agriculture and agricultural science fields. Her advocacy for plant breeding education, improved quality and disease resistance in vegetable cultivars grown worldwide, advocacy for small-scale vegetable and seed production in the United States and

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abroad, her work in organic agriculture, and her creation of novel models for public-private partnerships place her among the most widely respected voices for the future U.S. agriculture as a diverse, highly productive, balanced system. She has long been an advocate for the role that vegetables in particular, and improved, stabilized yields of crops and livestock in general will play for human welfare around the world. LITERATURE CITED Peters, S.J., T.R. Alter, and N. Schwartzbach. Democracy and higher education: Traditions and stories of civic engagement. Profile of Molly Jahn. 2010. p. 75–98. Michigan State Univ. Press, East Lansing.

SELECTED PUBLICATIONS OF MOLLY M. JAHN Journal Papers Miller, M.D. [Jahn, M.M.], and F. Solomon. 1984. Kinetics and intermediates of marginal band reformation: Evidence for peripheral determinants of microtubule organization. J. Cell Biol. 99:70–75s. Kyle, M.M. [Jahn M.M.] and R. Provvidenti. 1987. Inheritance of resistance to potyviruses in Phaseolus vulgaris L. I. Two independent genes for resistance to watermelon mosaic virus-2. Theor. Appl. Genet. 74:595–600. Kyle, M.M. [Jahn, M.M.], and M.H. Dickson. 1988. Linkage of hypersensitivity to five potyviruses with the B locus for seed coat color in Phaseolus vulgaris L. J. Hered. 79:308–311. Valyasevi, R., M.M. Kyle [Jahn], P. Christie, and K. Steinkrauss. 1990. Plasmids of Bacillus popilliae Dutky. J. Invert. Pathol. 56:286–288. Kyle, M.M. [Jahn, M.M.], and R. Provvidenti. 1993. Inheritance of resistance to potyviruses in Phaseolus vulgaris L. II. Linkage relations and utility of a dominant gene for lethal necrotic response to soybean mosaic virus. Theor. Appl. Genet. 86:189–196. Gilbert, R.Z., M.M. Kyle [Jahn], H.M. Munger, and S.M. Gray. 1994. Inheritance of resistance to watermelon mosaic virus in Cucumis melo. HortScience 29:107–110. Murphy, J.F., and M.M. Kyle [Jahn]. 1994. Isolation of leaf mesophyll protoplasts from Capsicum species and inoculation with three pepper viruses. Plant Cell Rep. 13:397–400. Fisher, M.L., and M.M. Kyle [Jahn]. 1994. Inheritance of resistance to potyviruses in Phaseolus vulgaris L. III. Cosegregation of phenotypically similar dominant resistance to nine potyviruses. Theor. Appl. Genet. 89:818–823. Prince, J.P., V.K. Lackney, C. Angeles, J.R. Blauth, and M.M. Kyle [Jahn]. 1995. Genetic similarity among Capsicum genotypes as measured by restriction fragment length polymorphism and randomly amplified polymorphic DNA markers. Genome 38:224–231. Murphy, J.F., and M.M. Kyle [Jahn]. 1995. Alleviation of restricted systemic movement of pepper mottle potyvirus in Capsicum annuum cv. ‘Avelar’ by coinfection with a cucumovirus. Phytopathology 85:561–566.

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Munger, H.M., Y. Zhang, S.L. Fenton, and M.M. Kyle [Jahn]. 1995. Leaf blower adapted for large scale inoculation of plants with mechanically-transmitted viruses. HortScience 30:1266–1267. Fisher, M.L., and M.M. Kyle [Jahn]. 1996. Inheritance of resistance to potyviruses in Phaseolus vulgaris L. IV. Inheritance, linkage relations, and environmental effects of systemic resistance to four potyviruses. Theor. Appl. Genet. 92:204–208. Hoffmann, M.P., R.W. Robinson, M.M. Kyle [Jahn], and J.J. Kirkwyland. 1996. Defoliation and infestation of Cucurbita pepo genotypes by diabroticite beetles. HortScience 31:439–442. Valkonen, J.P. T., M.M. Kyle [Jahn], and S. Slack. 1996. Comparison of resistance to potyviruses within Solanaceae: infection of potatoes with tobacco etch potyvirus and peppers with potato A and Y potyviruses. Ann. Appl. Biol. 129:25–38. Collmer, C.W., M.F. Marston, S.M. Albert, S. Bajaj, H.A. Maville, S.E. Ruuska, E.J. Vesely, and M.M. Kyle [Jahn]. 1996. The nucleotide sequence of the coat protein gene and 30 untranslated region of azuki mosaic potyvirus, a member of the bean common mosaic subgroup. Mol. Plant-Microbe Int. 9:758–761. Zhang, Y., M.M. Kyle [Jahn], K. Anagnostou, and T.A. Zitter. 1997. Screening melon (Cucumis melo L.) for resistance to gummy stem blight caused by Didymella bryoniae in the greenhouse and field. HortScience 32:117–121. Prince, J.P., Y. Zhang, E.R. Radwanski, and M.M. Kyle [Jahn]. 1997. A high-yielding and versatile DNA extraction protocol for Capsicum. HortScience 32:937–939. Kyle, M.M. [Jahn], and A. Palloix. 1997. Proposed revision of nomenclature for potyvirus resistance genes in Capsicum. Euphytica 97:183–188. Murphy, J.F., J.R. Blauth, K.D. Livingstone, V.K. Lackney, and M.M. Jahn. 1998. Genetic mapping of the pvr1 locus in Capsicum and evidence that distinct potyvirus resistance loci control responses that differ at the cellular and whole plant level. Molec. Plant Microbe Interact. 11:943–951. Silberstein, L., I. Kovalski, R. Huang, K. Anagnostou, M.M. Jahn and R. Perl-Treves. 1999. Molecular variation in melon (Cucumis melo L.) as revealed by RFLP and RAPD markers. Scientia Hort. 79:101–111. Livingstone, K.D., V. Lackney, J.R. Blauth, R. Van Wijk, and M.M. Jahn. 1999. Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152:1183–1202. Zuniga, T., J.P. Jantz, T.A. Zitter, and M.M. Jahn. 1999. Monogenic dominant resistance to gummy stem blight in two melon (Cucumis melo L.) accessions. Plant Dis. 83:1105–1107. Grube, R.C., E.R. Radwanski, and M.M. Jahn. 2000. Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887. Jahn, M.M., I. Paran, K. Hoffmann, E.R. Radwanski, K.D. Livingstone, R.C. Grube, E.Aftergroot,M.Lapidot,andJ.Moyer.2000.GeneticmappingoftheTswlocusforresistance to tomato spotted wilt tospovirus in Capsicum and its relationship to the Sw-5 allele for resistance to the same pathogen in tomato. Molec. Plant-Microbe Interact. 13:673–682. Grube, R.C., J.R. Blauth, M. Arnedo, C. Caranta, and M.M. Jahn. 2000. Identification and comparative mapping of a dominant potyvirus resistance gene cluster in Capsicum. Theor. Appl. Genet. 101:852–859. Grube, R.C., Y. Zhang, J.F. Murphy, F. Loaiza-Figueroa, R. Provvidenti, and M.M. Jahn. 2000. A new source of resistance to Cucumber mosaic virus in Capsicum frutescens. Plant Dis. 84:885–891. Anagnostou, K., M.M. Jahn, and R. Perl-Treves. 2000. Inheritance and linkage analysis of resistance to zucchini yellow mosaic virus, watermelon mosaic virus, papaya ringspot virus and powdery mildew resistance in Cucumis melo L. Euphytica 116:265–270.

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Collmer, C.W., M.F. Marston, and M.M. Jahn. 2000. The I gene of bean: A dosage-dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to Bean common mosaic virus. Molec. Plant-Microbe Interact. 13:1266–1270. Thorup, T.A., B. Tanyolac, K.D. Livingstone, S. Popovsky, I. Paran, and M.M. Jahn. 2000. Candidate gene analysis of organ pigmentation loci in the Solanaceae. Proc. Nat. Acad. Sci. (USA) 97:11192–11197. Livingstone, K.D., G. Churchill, and M.M. Jahn. 2000. Linkage mapping in populations with karyotypic rearrangements. J. Hered. 91:423–428. Ben Chaim, A., R.C. Grube, M. Lapidot, M.M. Jahn, and I. Paran. 2001. QTL mapping of resistance to cucumber mosaic virus in Capsicum annuum cv. Perennial. Theor. Appl. Genet. 102:1213–1220. Ben Chaim, A., I. Paran, R.C. Grube, M.M. Jahn, R. van Wijk, and J. Peleman. 2001. QTL mapping of fruit-related traits in pepper (Capsicum annuum). Theor. Appl. Genet. 102:1016–1028. Porch, T.G., and M.M. Jahn. 2001. Effects of high temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant Cell Environ. 24:723–731. Celebi-Toprak, FR., S.A. Slack, and M.M. Jahn. 2002. Nytbr, a new gene for dominant hypersensitivity to Potato virus Y maps to chromosome IV in potato. Theor. Appl. Genet. 104:669–674. Welsh, R., B. Hubbell, D.E. Erwin, and M.M. Jahn. 2002. GM crops and the pesticide paradigm. Nature Biotechnol. 20:548. Blum, E., K. Liu, M. Mazourek, E.-Y. Yoo, M.M. Jahn, and I. Paran. 2002. Molecular mapping of the C locus for presence of pungency in Capsicum. Genome 45:702–705. Brown, R.N., A. Bolanos, J. Myers, and M.M. Jahn. 2003. Inheritance of resistance to four cucurbit viruses in Cucurbita moschata. Euphytica 129:253–258. Chen, J.-F., X.D. Luo, J.E. Staub, M.M. Jahn, C.-T. Qian, F.-Y. Zhuang, and G. Ren. 2003. An allotriploid derived from an amphidiploid  diploid mating in Cucumis. Euphytica 131:235–241. Lotfi, M., A.R. Alan, M.J. Henning, M.M. Jahn, and E.D. Earle. 2003. Production of haploid and doubled haploid plants of melon (Cucumis melo L.) for use in breeding for multiple virus resistance. Plant Cell Rep. 21:1121–1128. Aluru, M.R., M. Mazourek, L.G. Landry, J. Curry, M.M. Jahn, and M.A. O’Connell. 2003. Capsaicinoid biosynthesis: Characterization of genes for branched-chain fatty acid biosynthesis. J. Expt. Bot 54:1655–1664. Blum, E., M. Mazourek, M.A. O’Connell, J. Curry, T. Thorup, K. Liu, M.M. Jahn, and I. Paran. 2003. Molecular mapping of capsaicinoid biosynthesis genes and QTL analysis for capsaicinoid content in Capsicum. Theor. Appl. Genet. 108:79–86. Rose, J.K.C., S. Bashir, J.J. Giovannoni, M.M. Jahn, and R.S. Saravanan. 2004. Tackling the plant proteome: Practical approaches, hurdles and experimental tools. Plant J. 39:715–733. Porch, T.G., M.H. Dickson, M.C. Long, D.R. Viands, and M.M. Jahn. 2004. General combining ability effects for reproductive heat tolerance in snap bean. J. Agric. Univ. Puerto Rico 88(3–4):161–164. Porch, T.G., M.H. Dickson, M. Long, D.R. Viands, and M.M. Jahn. 2004. General combining ability effects for reproductive heat tolerance in snap bean. J. Agr. Univ. Puerto Rico 88(3–4):161–164. Nelson, R.J., R. Naylor, and M.M. Jahn. 2004. The role of genomics research in the improvement of orphan crops. Crop Sci. 44:1901–1904.

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Griffiths, P. D., M.M. Jahn, and M.H. Dickson. 2004. Cornell 501: A snap bean breeding line (Phaseolus vulgaris L.) tolerant to white mold. HortScience 39:1507–1508. Naylor, R.L., W.P. Falcon, R.M. Goodman, M.M. Jahn, T. Sengooba, H. Tefera, and R.J. Nelson. 2004. Integrating new genetic technologies into the improvement of orphan crops in least developed countries. Food Policy 29:15–44. Frantz, J.D., and M.M. Jahn. 2004. Five independent loci each control monogenic resistance to gummy stem blight in melon (Cucumis melo L.). Theor. Appl. Genet. 108:1033–1038. Frantz, J.D., J. Gardner, M.P. Hoffmann, and M.M. Jahn. 2004. Greenhouse screening of Capsicum accessions for resistance to European corn borer (Ostrinia nubilalis) HortScience 39:1336–1338. Frantz, J.D., J. Gardner, M.P. Hoffmann, and M.M. Jahn. 2004. Greenhouse screening of Capsicum accessions for resistance to green peach aphid (Myzus persicae) HortScience 39(6):1332–1335. Chen, J., X. Luo, C. Qian, M.M. Jahn, J.E. Staub, F. Zhuang, Q. Lou, and G. Ren. 2004. Cucumis monosomic alien addition lines: Morphological, cytological and RAPD analysis. Theor. Appl. Genet. 108:1343–1348. Alba, R., Z. Fei, P. Payton, Y. Liu, S.L. Moore, P. Debbie, J.S. Gordon, J.K.C. Rose, G. Martin, S.D. Tanksley, M. Bouzayen, M.M. Jahn, and J. Giovannoni. 2004. ESTs, cDNA microarrays and gene expression profiling: Tools for dissecting plant physiology and development. Plant J. 39:697–714. Paran, I., J. Rouppe van der Voort, V. Lefebvre, M.M. Jahn, L. Landry, R. van Wijk, H. Verbakel, B. Tanyolac, C. Caranta, A. Ben Chaim, K.D. Livingstone, A. Palloix, and J. Peleman. 2004. An integrated genetic map of pepper. Molec. Breed. 13:251–261. Quirin, E.A., E. Ogundiwin, J.P. Prince, M. Mazourek, M.O. Briggs, T.S. Chlanda, K.-T. Kim, M. Falise, B.C. Kang, and M.M. Jahn. 2005. PCR-based detection of Phyto.5.2, a major QTL controlling resistance to Phytophthora capsici in Capsicum. Theor. Appl. Genet. 110:605–612. Yeam, I., B.C. Kang, J.D. Frantz, and M.M. Jahn. 2005. Allele-specific CAPS markers based on point mutations in resistance alleles at the pvr1 locus encoding eIF4E in Capsicum. Theor. Appl. Genet. 112:178–186. Stewart, C.S., B.C. Kang, K. Liu, M. Mazourek, E.Y. Yoo, S.L. Moore, B.D. Kim, I. Paran, and M.M. Jahn. 2005. The Pun1 gene in pepper encodes a putative acyltransferase. Plant J. 42:675–688. Qian, C.T., M.M. Jahn, J.E. Staub, X.-D. Luo, and J.F. Chen. 2005. Meiotic chromosome behavior in an allotriploid derived from an amphidiploid  diploid mating in Cucumis. Plant Breed. 124:272–276. Liu, K., B.C. Kang, H. Jiang, S.L. Moore, C.B. Watkins, T.L. Setter, and M.M. Jahn. 2005. A GH3-like gene isolated from Capsicum chinense L. pepper fruit is regulated by auxin and ethylene. Plant Mol. Biol. 58(4):447–464. Liu, K., H. Jiang, S.L. Moore, C.B. Watkins, and M.M. Jahn. 2005. Identification of fruitspecific lipid transfer protein in Capsicum chinense. Planta 223:672–683. Kang, B.-C., I. Yeam, and M.M. Jahn. 2005. Genetics of resistance to plant viruses. Annu. Rev. Phytopath. 42:581–621. Kang, B.-C., I. Yeam, J.D. Frantz, J.F. Murphy, and M.M. Jahn. 2005. The pvr1 locus in pepper encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 42:392–405. Henning, M. J, H.M. Munger, and M.M. Jahn. 2005. ‘PMR Delicious 51’: An improved open-pollinated melon with resistance to powdery mildew. HortScience 40(1): 261–262.

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Henning, M.J., H.M. Munger, and M.M. Jahn. 2005. ‘Hannah’s Choice F1’: A new muskmelon hybrid with resistance to powdery mildew, Fusarium race 2 and potyviruses. HortScience 40:492–493. Cadle-Davidson, M.M. and M.M. Jahn. 2005. Resistance conferred against bean common mosaic virus by the incompletely dominant I locus of Phaseolus vulgaris is active at the single cell level. Arch. Virol. 150:2601–2608. Perez, K., I. Yeam, M.M. Jahn, and B.C. Kang. 2006. Megaprimer-mediated domain swapping for construction of chimeric viruses. J. Virol. Methods 135(2):254–262. Luo, X.D., L.F. Dai, S.B. Wang, J.N. Wolukau, M.M. Jahn, and J.F. Chen. 2006. Male gamete development and early tapetal degeneration in cytoplasmic male-sterile pepper investigated by meiotic, anatomical and ultrastructural analyses. Plant Breed. 125:395–399. Lou, Q.F., J.F. Chen, L.Z. Chen, J.N. Wolokau, B.C. Kang, and M.M. Jahn. 2006. Identification of an AFLP marker linked to a locus controlling gynoecy in cucumber and its conversion to a SCAR marker useful in plant breeding. L. Acta Hort. Sinica 31(2):256–261. Liu, K., H. Jiang, S.L. Moore, C.B. Watkins, and M.M. Jahn. 2006. Identification of fruitspecific lipid transfer protein in Capsicum chinense. Planta 223:672–683. Chen, J.F., G. Ren, X.D. Luo, J. Staub, and M.M. Jahn. 2006. Inheritance of aspartate aminotransferase (AAT) in Cucumis species as revealed by interspecific hybridization. Can. J. Bot. 84:1503–1507. Cadle-Davidson, M.M., and M.M. Jahn. 2006. Patterns of accumulation of Bean common mosaic virus in Phaseolus vulgaris genotypes nearly isogenic for the I locus. Ann. Appl Biol. 148:179–185. Cadle-Davidson, M.M., and M.M. Jahn. 2006. Differential gene expression in Phaseolus vulgaris I locus NILs challenged with Bean common mosaic virus. Theor. Appl. Genet. 112:1452–1457. Brown, C.R., T.S. Kim, Z. Ganga, K. Haynes, D. DeJong, M.M. Jahn, I. Paran, and W.P. DeJong. 2006. Segregation of total carotenoid in high level potato germplasm and its relationship to beta-carotene hydroxylase polymorphism. Am. J. Pot. Res. 83:365–372. Ben Chaim, A., Y. Borovsky, M. Falise, M. Mazourek, B.C. Kang, I. Paran, I., and M.M. Jahn. 2006. QTL analysis for capsaicinoid content in Capsicum. Theor. Appl. Genet. 113:1481–1490. Stewart C., M. Mazourek, G. Stellari, M. O’Connell, and M.M. Jahn. 2007. Genetic control of pungency in C. chinense via the Pun1 locus. J. Expt. Bot. 58:979–991. Porch T.G., R. Bernsten, J.C. Rosas, and M.M. Jahn. 2007. Climate change and the potential economic benefits of heat tolerant bean varieties for farmers in Atlantida, Honduras. J. Agr. Univ. Puerto Rico 91(3–4):133–148. Kang, B.C., I. Yeam, H. Li, K.W. Perez, and M.M. Jahn. 2007. Ectopic expression of a recessive resistance gene generates dominant potyvirus resistance in plants. Plant Biotech. J. 5:526–36. Garces-Claver, A., S. Moore Fellman, R. Gil-Ortenga, M.M. Jahn, and M. Arnedo-Andres. 2007. Identification, validation and survey of a single nucleotide polymorphism (SNP) associated with pungency in Capsicum spp. Theor. Appl. Genet. 115:907–916. Cavatorta, J., G. Moriarty, M. Henning, M. Glos, M. Kreitinger, H.M. Munger, and M.M. Jahn. 2007. Marketmore 97: A monoecious slicing cucumber inbred with multiple disease and insect resistances. HortScience 42:707–709. Yeam, I., J.R. Cavatorta, D.R. Ripoll, B.C. Kang, and M.M. Jahn. 2007. Functional dissection of highly conserved amino acid substitutions in the recessive potyvirus resistance genes encoding eIF4E. Plant Cell 19:1–16.

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Cavatorta, J.R., A.E. Savage, I. Yeam, S.M. Gray, and M.M. Jahn. 2008. Positive Darwinian selection at single amino acid sites conferring plant virus resistance. J. Mol. Evol. 67:551–559. Zhuang, Y., J.-F. Chen, and M.M. Jahn. 2008. Expression and sequence variation of the cucumber Por gene in the synthesized allotetraploid Cucumis  hytivus. Mol. Biol. Rep. Online http://www.springerlink.com/content/l44q32385l431471/fulltext.pdf. Wu, F., N.T. Eannetta, Y. Xu, R. Durrett, M. Mazourek, M.M. Jahn, and S.D. Tanksley. 2009. A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the Genus Capsicum. Theor. Appl. Genet. 118:1279–1293. Mazourek, M., G. Moriarty, M. Glos, M. Fink, M. Kreitinger, E. Henderson, G. Palmer, A. Chikering, D. Rumore, D. Kean, J. Myers, J. Murphy, C. Krame, and M.M. Jahn. 2009. Peacework: A cucumber mosaic virus-resistant early red bell pepper for organic systems. HortScience 44:1464–1467. Mazourek, M., E.T. Cirulli, S.M. Collier, L.G. Landry, B.-C. Kang, E.A. Quirin, J.M. Bradeen, P. Moffett, and M. Jahn. 2009. The fractionated orthology of Bs2 and Rx/Gpa2 supports shared synteny of disease resistance in the Solanaceae. Genetics 182:1351–1364. Online www.genetics.org/cgi/rapidpdf/genetics.109.101022v1.pdf. Mazourek, M., A. Pujar, Y. Borovsky, I. Paran, L. Mueller, and M. Jahn. 2009. A dynamic interface for capsaicinoid systems biology. Plant Physiol. 150:1806–1821. Stellari, G.M., M. Mazourek, and M. Jahn. 2010. Contrasting modes for loss of pungency between cultivated and wild species of Capsicum. Heredity 104:460–471. Miller, J.K., E.M. Herman, M.M. Jahn, and K.J. Bradford. 2010. Strategic research, education and policy goals for seed science and crop improvement. Plant Sci. 179:645–652. Cavatorta, J., K.W. Perez, S.M. Gray, J. Van Eck, I. Yeam, and M.M. Jahn. 2011. Engineering resistance to plant viral disease using a modified potato gene. Plant Biotechnology Journal. In press.

Books Kyle, M.M. [Jahn, M.M.], ed. 1993. Resistance to viral diseases of vegetables: Genetics and breeding. Timber Press, Portland, OR. Popp, J., M. Matlock, and M.M. Jahn. 2011. Biotechnology and sustainability. Cambridge University Press, Cambridge, U.K.

Book Chapters Munger, H.M., M.M. Kyle [Jahn], and R.W. Robinson. 1992. Cucurbits. p. 42–56. In: Historical review of traditional crop breeding practices. Group of National Experts on Safety in Biotechnology Working Group. Directorate for Science Technology and Industry/Committee for Scientific and Technological Policy. Organization for Economic Cooperation and Development. Paris. Munger, H.M., M.M. Kyle [Jahn], and R.W. Robinson. 1992. Cucurbits. p. 42–56. In: Historical review of traditional crop breeding practices. Group of National Experts on Safety in Biotechnology Working Group. Directorate for Science Technology and Industry/Committee for Scientific and Technological Policy Organization for Economic Cooperation and Development, Paris:. Munger, H.M., M.M. Kyle [Jahn], and R.W. Robinson. 1992. Cucurbits. p. 42–56. In: Historical review of traditional crop breeding practices. Group of National Experts

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on Safety in Biotechnology Working Group. Directorate for Science Technology and Industry/Committee for Scientific and Technological Policy. Organization for Economic Cooperation and Development, Paris. Superak, T.H., B.T. Scully, M.M. Kyle [Jahn], and H.M. Munger. 1993. Interspecific transfer of viral resistance. p. 217–236. In: Resistance to viral diseases of vegetables: Genetics and breeding. M.M. Kyle [Jahn], ed. Timber Press, Portland OR. McCouch, S.M., P. Ronald, and M.M. Kyle [Jahn]. 1993. Biotechnology and crop improvement for sustainable agricultural systems. p. 157–191. In: M.B. Callaway and F. Forella (eds.), Crop improvement for sustainable agricultural systems. Univ. Nebraska Press, Lincoln, NE. Kyle [Jahn], M.M., and R. Provvidenti. 1993. Genetics of broad spectrum viral resistance in bean and pea. p. 153–166. In: M.M. Kyle [Jahn], (ed.), Resistance to viral diseases of vegetables: Genetics and breeding. Timber Press, Portland OR.

GERMPLASM RELEASES AND PATENTS Plant Variety Protection Certificates Bugle, powdery mildew–resistant butternut squash awarded September 2001. Molly Jahn and George Moriarty Cornell’s Bush Delicata, powdery mildew–resistant winter Cucurbita pepo awarded May 2002. Molly Jahn and George Moriarty

Cornell Open-Pollinated and Hybrid Squash Cultivars Cucurbita pepo Cornell’s Bush Delicata (2002) All America Selection Harlequin F1 (2002) Celebration F1 (2004) Success PM (2004) Romulus PM Zucchini (2005) Sweet REBA winter squash (acorn type) (2005) Three inbred PMR pumpkin parent lines used in three hybrid pumpkin varieties One parent of three commercial hybrid summer squash varieties

Cucurbita moschata Bugle (2002) Parents of two leading commercial hybrids Bright Eyes (NY07-140A) (2009) Little John NY-05-130 (2009) Oro Verde NY07-131C-N (2009) Honeynut (NY07-134A)

Cucumis melo Hannah’s Choice F1 (2005) PMR Delicious 51 (2005) Farmer’s Daughter (2009)

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Cucumis sativus Marketmore 97 with Henry Munger (1997) Poinsett 97 with Henry Munger (1997) Poinsett 2000 with Henry Munger (2000) Greenfinger NY 08-143 (2006) Platinum NY06-873 (2008) Salt and Pepper NY08-7107 (2009) Silver Slicer (2009)

Capsicum annuum Peacework (2007) CU Early NY06-368 (2008) King Crimson (2009)

Patents U.S. Patent Application No. 10/538,434, Pub. No. 2006–0294618 A1 ‘‘Recessive plant viral resistance results from mutations in translation initiation factor eIF4E (allowed Feb. 5, 2010). PCT/US2009/061675. ‘‘Mutated eIF4E sequences from potato which are useful in imparting virus resistance.’’ Publication number WO/2010/048398 (published 29 April 2010).

2 History, Evolution, and Domestication of Brassica Crops Shyam Prakash National Research Centre on Plant Biotechnology Indian Agricultural Research Institute New Delhi 110012, India Xiao-Ming Wu Oil Crops Research Institute of Chinese Academy of Agricultural Sciences Wuhan 430062, People’s Republic of China S. R. Bhat National Research Centre on Plant Biotechnology Indian Agricultural Research Institute New Delhi 110012, India

ABSTRACT Brassica crops are unique as various plant parts have been modified during domestication for use—for example, roots, leaves, stems, and inflorescences in various vegetables and seeds in edible oils and condiments. The genus Brassica comprises six crop species: B. nigra (2n ¼ 16), B. oleracea (2n ¼ 18), B. rapa (2n ¼ 20), B. carinata (2n ¼ 34), B. juncea (2n ¼ 36), and B. napus (2n ¼ 38). Of these, B. oleracea, B. rapa, and B. juncea (2n ¼ 36) are highly polymorphic, displaying a range of morphotypes. Cytogenetic evidence point to an archetype with a basic chromosome number of x ¼ 6. However, molecular markers strongly suggest the involvement of two evolutionary pathways: B. nigra in one direction and B. oleracea/B. rapa together in the other. Comparison of chromosome collinearity and comparative chromosome painting (CCP) suggested the paleopolyploid nature of the three basic genomes, which are composed of three variants of Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick.
2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 19

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an ancestral genome originating through an ancient hexaploid event, now referred to as the triplication theory. The Brassicaceae paleoarchetype had the chromosome constitution 2n ¼ 8; following another cycle of genome duplication it produced a tetraploid genome of 2n ¼ 4x ¼ 16 referred to as the ancestral crucifer karyotype (ACK). Another cycle of genome duplication resulted into a hexaploid (2n ¼ 6x ¼ 24). This hexaploid ancestor gave rise to three diploid basic genomes following reduction in chromosome number. An alternative view proposes that a reduction in chromosome number in ACK resulted into a smaller Brassica genome, known as the ancestral Brasssicaceae karyotpe with 6 haploid chromosomes. This subsequently diverged into nigra and rapa/oleracea lineages 7.3 to 4 million years ago. Brassicas are believed to have originated in the countries surrounding the Mediterranean basin and further extension into southwest and central Asia encompassing mainly Mediterranean, Irano-Turanian, and SaharoSindian phytogeographical regions. It is now believed that B. rapa was the first species to be domesticated followed by B. nigra and B. juncea; B. oleracea entered into cultivation later. The history of the domestication of B. carinata and B. napus is relatively recent. Ancient Indian, Chinese, Greek, and Roman literature is extremely rich in detailing information concerning brassica crops. Based on information from these sources and genetical and molecular evidence, possible domestication centers have been constructed. Brassicas first entered into domestication as vegetables and later as edible oil crop. KEYWORDS: Brassica carinata; Brassica juncea; Brassica napus; Brassica nigra; Brassica oleraceae; Brassica rapa ABBREVIATIONS I. INTRODUCTION A. Crop Species B. Origin of the Word Brassica II. ARCHETYPES AND EVOLUTION OF BASIC GENOMES AND DERIVED ALLOPOLYPLOIDS A. Basic Karyotypes B. Diploid Genomes C. Allopolyploid Genomes III. ETHNOBOTANY, ORIGIN, AND DOMESTICATION A. Origin of Diploid Species B. Brassica nigra C. Brassica oleracea 1. Taxonomy and Origins 2. Cabbage 3. Cauliflower and Broccoli 4. Chinese Kale (B. alboglabra) D. Brassica rapa 1. Taxonomy and Origin 2. European Forms 3. Indian Forms 4. Chinese Forms 5. Turnip

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

21

E. Brassica carinata F. Brassica juncea 1. Taxonomy 2. Origin and Domestication 3. Indian Forms 4. Chinese Forms G. Brassica napus IV. CONCLUDING REMARKS ACKNOWLEDGMENTS LITERATURE CITED

ABBREVIATIONS ACK cp FISH ITS Mya RAPD RFLP rDNA rRNA

Ancestral crucifer karyotype Chloroplast Fluorescence in situ hybridization Internal transcribed spacers of nuclear ribosomal DNA and 5.8S rRNA gene Million years ago Randomly amplified polymorphic DNA Restriction fragment length polymorphism Ribosomal DNA genes Ribosomal RNA

I. INTRODUCTION A. Crop Species The origin and domestication of Brassica crops of the Brassicaceae is a fascinating story. Literatures from several ancient civilizations (Indian, Chinese, Greek, and Roman) have frequent references of these crops. The earliest mention of these can be traced back to a Chinese almanac (ca. 3000 BCE), Assyrian cuneiform documents (ca. 1800 BCE), and Indian Aryan literature (ca. 1500 BCE). Gautama Buddha in India (6th century BCE) told a parable concerning mustard seeds. Ancient Greek and Roman writers make frequent references to Brassica crops. Among the references are Theophrastus (370–285 BCE) in Historia de Plantis (Inquiry into Plants); Marcus Porcius Cato (234–149 BCE) in De Agri Cultura (On Farming); Pedanius Dioscorides (20–70 CE) in Peri Ylis Iatrikis, Latinized

22

S. PRAKASH, X.-M. WU, AND S.R. BHAT

as De Materia Medica (On Medical Matters); Lucius Junius Moderatus Columella (4–70 CE) in De Re Rustica (On Agriculture); and Gaius Plinius Secundus—known to us as Pliny the Elder—(23–79 CE) in Historia Naturalis (Natural History). Plant parts, particularly seeds, have been excavated from several ancient sites (Allchin 1969; Hyams 1971; Ghosh et al. 2006; Wu et al. 2009). In the botanical and agricultural books of the Renaissance, descriptions of various crops along with their usage, often accompanied by illustrations, are found in the herbals of Fuchs (1542), Tragus (1552), Mattioli (1571), Dodonaeus (1578), de Lobel (1581), Durante (1585), Dalechamps (1587), Gerard(e) (1597, 1633), Bauhin (1623), and Bauhin and Cherler (1651). Comprehensive taxonomy, geographical distribution, cytogenetical and biochemical evidence, and, in recent years, use of molecular markers have greatly helped in reconstructing the past events about crops’ origin, evolution and domestication. However, the origin of any crop involves two separate aspects: (1) the evolutionary processes that led to the origin of the wild species prior to its domestication, and (2) the history of domestication and superdomestication resulting from human intervention. The brassicas are important components of the cuisine of many cultures. These represent a valuable source of vitamin C, dietary fiber, and anticancer compounds (Fahey et al. 1997). In the majority of crop plants, domestication usually has enhanced a single plant part for use by humans, such as seeds, fruits, or roots. However, the Brassica crops are unique in that practically every plant part has been selected and elaborated to yield different crop plants.They provide edible oils, condiments (seeds), and vegetables (roots, leaves, stems, and inflorescences). The Brassica crops complex comprises six species (Table 2.1). Brassica oleracea, B. rapa, and B. juncea are highly polymorphic, displaying a range of morphotypes, although B. nigra is cultivated exclusively as condiment mustard. The cultivated B. oleracea forms exhibit enormous morphological variability in leaf, stem, and inflorescence and are collectively referred to as cole crops—a term given in 1901 by L. H. Bailey, the American botanist and horticulturist (Bailey 1922). Various forms of B. oleracea are popular vegetables worldwide. Forms of B. rapa are variously referred to as turnip rape (oilseed forms of Europe and Canada), sarson (oil seed forms of the Indian subcontinent), and leafy vegetables (China and other southeast Asian countries). B. carinata, the Ethiopian mustard, has a range of uses: for example, vegetables, edible and industrial oils, a condiment, and medicinal. Its cultivation is restricted primarily to Ethiopia but also extends to Kenya. Brassica juncea (Indian or brown mustard) is a major source of edible oil on the Indian subcontinent, northern China, and eastern European countries, as root and leaf

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

Table 2.1.

23

Cultivated species of the genus Brassica and their variations.

Botanical name

2n

Common name

Usage

B. nigra B. oleracea var. acephala var. alboglabra var. botrytis var. capitata var. fruticosa var. gemmifera var. gongylodes var. italica var. sabauda B. rapa spp. oleifera var. brown sarson var. toria var. yellow sarson ssp. rapifera ssp. chinensis ssp. pekinensis ssp. nipposinica ssp. parachinensis B. carinata B. juncea B. napus spp. oleifera spp. rapifera

16 18

Black mustard

Condiment (seed)

Kale Chinese kale Cauliflower Cabbage Branchingbush kale Brussels sprouts Kohlrabi Broccoli Savoy cabbage

Vegetable, fodder (leaves) Vegetable (stem, leaves) Vegetable (inflorescence) Vegetable (head) Fodder (leaves) Vegetable (head) Vegetable, fodder (stem) Vegetable (inflorescence) Vegetable (terminal buds)

Turnip rape Brown sarson Toria Yellow sarson Turnip Pak-choi Chinese cabbage Ethiopian mustard Mustard

Oilseed Oilseed Oilseed Oilseed Fodder, vegetable (root) Vegetable (leaves) Vegetable, fodder (head) Vegetable (leaves) Vegetable (leaves) Vegetable, oilseed Oilseed, vegetable

Rapeseed Rutabaga, swede

Oilseed Fodder

20

34 36 38

Source: Prakash et al. 2009.

vegetables in China, and as hot mustard condiment used in mayonnaise, salad dressing, and sauces in Europe, Canada, and America (Skrypetz 2003). Brassica napus is a major edible oilseed crop widely grown in Europe, Canada, China, and Australia. One of its root variants, rutabaga or swede (ssp. rapifera), is grown for fodder, particularly in Scandinavian countries and England. Following the determination of chromosome numbers in the early 1920s, the Japanese scientist Morinaga carried out pioneering cytogenetical investigations involving hybridizations and the study of chromosome pairing behavior. Morinaga (1934) interpreted that crop brassicas comprise six species, of these three are low-chromosome monogenomic diploids—B. nigra (n ¼ 8), B. oleracea (n ¼ 9) and B. rapa (syn. B. campestris, n ¼ 10)—and three are high-chromosome digenomics—B. carinata (n ¼ 17), B. juncea (n ¼ 18), and B. napus

24

S. PRAKASH, X.-M. WU, AND S.R. BHAT

Fig. 2.1. Cytogenetic relationships of crop brassicas (U, 1935). Solid and broken lines in the allopolyploids represent female and male parents, respectively. (Source: U 1935; Prakash et al. 2009).

(n ¼ 19) that have evolved through convergent allopolyploid evolution between any two of the diploid species. Another Japanese scientist U (1935) represented these cytogenetical relationships diagrammatically, now famously referred to as the triangle of U (Fig. 2.1). Various lines of evidence such as cytogenetics, molecular cytogenetics and molecular markers gathered during last several decades have substantiated these relationships (Prakash et al. 2009). A journey into the past through evolutionary events of origin and domestication of these crops makes a fascinating story, which we have attempted to synthesize in this review. Useful information dealing with some of these aspectes are given in recently published books, such as Biology of Brassica Coenospecies (Go´mez-Campo 1999) and Vegetable Brassicas and Related Crucifers (Dixon 2007). B. Origin of the Word Brassica Several views have been proposed concerning the origin of the word Brassica, and its etymology has been discussed since 1727 (see Prakash and Hinata 1980; Dixon 2007; Maggioni et al. 2010). Henslow (1908) quoted Hermann Boerhaave (1727) that the term Brassica originated from the Greek a ´ po´@´ubs´axein [apooibsazein], Lat. vorare (to devour). Hegi (1919) believed that it originated from the Celtic word for cabbage, Bresic or Bresych, and a contraction of praesecare (to cut off early), as the leaves were removed from the stem for cattle fodder according to the Roman scholar Marcus Terentius Varro (116–27 BCE) in his De Lingua

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

25

Latina. Another possible derivation is from the Greek word ßo´a ´ o´sein (crackle), as the leaves produce a crackling noise on being broken off (Gates 1953). The Greek word br´askh (braske) has also been favored for its derivation, which was a local name used by Greeks in southern Italy (Maggioni et al. 2010). A word in the Phoenician dialect of the Punic language Burutzim is also considered a possible progenitor of the word Brassica (Herv
e 2003). The written word Brassica first appeared, in the 3rd-century BCE Latin literature by the playwright Plautus. II. ARCHETYPES AND EVOLUTION OF BASIC GENOMES AND DERIVED ALLOPOLYPLOIDS A. Basic Karyotypes There has been continuing debate and conflicting views on the origin and evolution of basic karyotypes in Brassica. In the initial stages, these views were based on classical cytological studies. During last 25 years, use of DNA markers has unraveled facts for interprating the phylogenetic relationships and origin of basic genomes (Prakash and Hinata 1980; Go´mez-Campo 1999). In the early 1940s, it was widely believed that the three basic genomes originated from one archetype, sharing common ancestry, making them secondary balanced polyploids. Based on several cytological surveys, a scenerio emerged suggesting that this archetype was a smaller genome. However, variable basic chromosome numbers of the archetype ranging from 3 to 9 were proposed. For example, Catcheside (1934, 1937) suggested x ¼ 6 as the basic number, his conclusion based on secondary chromosome associations in B. napus and B. oleracea. He also proposed the primitive haploid number in Brassicaceae as x ¼ 7 and assummed that x ¼ 6 arose from it by fusion of two chromosomes. Alam (1936) and Haga (1938) agreed with Catcheside by observing secondary chromosome pairing in the three basic diploid species. Sikka (1940) carried out detailed cytogenetical analysis in several Brassica and related species and proposed a basic number of x ¼ 5 from observing secondary bivalent associations in three species: B. monensis (syn. Coincya monensis 2n ¼ 24), B. sinapistrium (syn. Sinapis arvensis, 2n ¼ 18), and B. nigra. He suggested that the evolution in Brassica occurred toward tetraploidy, citing in evidence the chromosome series 2n ¼ 30, 60, 90, and 120 in the genus Crambe, all multiples of x ¼ 5. However, pachytene chromosome analysis of the basic genomes (R€ obbelen 1960) provided compelling evidence in support of x ¼ 6 as the constitution of basic archetype and a monophyletic origin of the

26

S. PRAKASH, X.-M. WU, AND S.R. BHAT

diploid species. Meiotic chromosome pairing in the haploids of B. oleracea (2n ¼ 8, 2II þ 4I, Thompson 1956), B. nigra (2n ¼ 8, 2II þ 4I) (Prakash 1974a), and a related species B. tournefortii (2n ¼ 10, 1III þ 2 II þ 3I) (Prakash 1974b) also lent support to that proposal. However, investigations in the last 20 years using molecular markers firmly disprove the theory of monophyletic origin. The first indication came from nuclear DNA restriction fragment length polymorphisms (RFLPs) by Song et al. (1988a), which was further corroborated by investigations from nuclear, chloroplast, and mitochondrial DNA RFLPs. These studies strongly suggested that two evolutionary pathways are involved in the origin of diploid species: B. nigra evolved in one direction and B. rapa/ B. oleracea together in the other. Also these investigations clearly revealed a vertical division of the subtribe Brassicinae into two lineages, referred to as Nigra and Oleracea/Rapa (Warwick and Black 1991; Pradhan et al. 1992). Earlier, cytogenetical investigations predicted this divergence between B. nigra and B. oleracea/B. rapa lineages based on chromosome pairing in hybrids (Mizushima 1950; Prakash and Hinata 1980). Arabidopsis, a member of the Brassicacea, is regarded as a model species in plant molecular and genomic researches. Its genome has completely been sequenced (Arabidopsis Genome Initiative 2000), and this information is widely used for comparative mapping using Arabidopsis-derived probes to understand the architecture and organization of Brassica genomes and deciphering their evolution. Two strategies have been followed to unravel the constitution of ancestral karyotype and reconstruct the evolutionary events leading to the origin of current karyotypes. These are: (1) comparative genetic mapping (i.e., the comparison of chromosome collinearity) and (2) comparative chromosome painting. Availability of virtually repeat-free A. thaliana bacterial artificial chromosome clones has considerably helped in comparative chromosome painting in several Brassicaceae species. Many duplicated regions have been discovered that could not have been identified through classical genetical analysis and provided additional insight into karyotype evolution. Arabidopsis-genome sequence information indicated a large number of duplications, both intra- and interchromosomal, suggesting that this genome is a relic of an ancient whole genome duplication. Comparative RFLP mapping of the three basic genomes and Arabidopsis also confirmed the paleopolyploid nature of the three basic species (B. nigra, B. oleracea and B. rapa), suggested that the existing diploid genomes are paleopolyploids, and, for the first time, indicated that these are composed of three variants of an ancestral genome evolved probably by an ancient hexaploid event (Lagercrantz and Lydiate 1996; Lagercrantz 1998; Babula et al. 2003). This hypothesis

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

27

is now referred to as the triplication theory. It envisages that a common ancestral genome of Arabidopsis and Brassica underwent genome duplication events twice before their split while the third duplication event was a genome triplication after this divergence and was confined to the Brassiceae lineage only. There is evidence that this tribe represents a monophyletic lineage and that all the taxa are derivatives of this hexaploid genome (Lysak et al. 2005). This triplication model finds support from the earlier studies involving classical cytogenetics and ribosomal DNA (rDNA) markers, such as those by Chen and Heneen (1991) and Cheng and Heneen (1995), who observed three pairs of satellited chromosomes with active nucleolus organizer regions in B. nigra and S. arvensis and occurrence of three pairs of chromosomes carrying 25S rDNA gene loci in B. nigra (Fukui et al. 1998), B. oleracea (Maluszynska and Heslop-Harrison 1993; Snowdon et al. 1997a; Armstrong et al. 1998; Ali et al. 2005; Hasterok et al. 2006) and related species S. alba (Schrader et al. 2000) and S. arvensis (Ali et al. 2005). It is inferred that the number of three chromosome pairs carrying the 25S rDNA gene is basic for the Brassicaceae (Ali et al. 2005). The Brassicaceae paleoarchetype had in all probability a genome comprising 8 somatic chromosomes (n ¼ 4) and following another cycle of genome duplication produced a tetraploid genome having 2n ¼ 4x ¼ 16, an event that occurred 24 to 40 million years ago (Mya) (Henry et al. 2006). This ancestral crucifer karyotype (ACK) has been put forward as the common ancestor of family Brassicaceae. It had a genome possessing 8 haploid chromosomes (AK1–AK8) and some 24 conserved genome blocks (Lysak et al. 2006; Schranz et al. 2006). This genome was similar to the present-day A. lyrata and Capsella rubella (2n ¼ 16, 230 Mbp) from which derived the genomes of existing Brassica species and A. thaliana (Schranz et al. 2006). The similar karyotypes of Arabidopsis and Capsella lineages further substantiated that the ancestral Crucifer karyotype had resemblance with Arabidopsis–Capsella karyotypes and possessed 16 somatic chromosomes (Lysak et al. 2006). The evidence in support of this n ¼ 8 ACK karyotype is derived as follows: (1) x ¼ 8 is the most common base number in the Brassicaceae (Warwick and Al-Shehbaz 2006), and (2) 8 chromosomes of A. lyrata and Capsella rubella possess nearly identical linkage groups (Bolvin et al. 2004; Kuittinen et al. 2004; Koch and Kiefer 2005; Lysak et al. 2006, 2007). The ACK gave rise to the Arabidopsis genome (2n ¼ 10) having 157 Mbp of DNA (Johnston et al. 2005; Schranz et al. 2006) around 14.5 to 20.4 Mya (Yang et al. 1999) in one pathway due to chromosomal rearrangements, mainly fusions and gene loss, while members of the tribe Brassiceae originated in the other pathway.

28

S. PRAKASH, X.-M. WU, AND S.R. BHAT

Several investigations based on molecular marker maps (Lagercrantz 1998; O’Neill and Bancroft 2000; Rana et al. 2004; Park et al. 2005; Parkin et al. 2005) and fluorescence in situ hybridization (FISH) maps (Lysak et al. 2005; Ziolkowski et al. 2006) suggested that diploid Brassica genomes evolved from this tetraploid following another cycle of genome duplication. The resulting genome was a hexaploid with chromosome constitution of 2n ¼ 6x ¼ 24. Ziolkowski et al. (2006) also proposed that the final event of genome triplication was allopolyploidization (Fig. 2.2) involving hybridization between an Arabidopsis-like diploid and a tetraploid genome. This allopolyploidization was responsible for, in part, increase in DNA content from 230 Mbp to 529–696 Mbp of diploid Brassica species (Johnston et al. 2005). However, the mechanism of reduction in chromsome numbers from 24 to 16–20 is not properly explained. Mand
akov
a and Lysak (2008) extended chromosome painting investigations to eight species with x ¼ 7 (2n ¼ 14, 28) comprising six X

X

Brassicaceae common ancestor (diploid)

X′

Polyploidization Brassicaceae common XX′ ancestor (allotetraploid?) Chromosomal diploidization

Y

Scenario 2 translocation

Scenario 1 translocation

Y′

Polyploidization

Arabidopsis ancestor (diploid)

ancestor I Y′Y′ Brassica (tetraploid)

Y′′′

Chromosome number reduction

Y′′ Brassica ancestor II (diploid)

A Present-day A thaliana (diploid)

Brassica ancestor I (diploid)

Polyploidization

Y′Y′Y′′ Brassica ancestor III (hexaploid) Chromosomal diploidization

B Present-day B. oleracea (diploid)

Fig. 2.2. Model of diploid Brassica genome evolution via hexaploidization. (Source: Ziolkowski et al. 2006).

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

29

Brassicaceae tribes. They proposed that a karyotype with n ¼ 7 chromosomes, referred to as Proto-Calepineae karyotype (PCK, n ¼ 7), was derived from the ACK due to the loss of one chromosome. They further suggested that this prototype was the progenitor of the tribe Brassiceae prior to undergoing whole-genome triplication and was followed by diploidization. Thus, the original triplication pattern was lost. However, some genome blocks were retained as single or duplicate copies, others in three copies, while a few were increased further due to homologous recombination. These authors did not rule out the possibility of further reduction in chromosome number to n ¼ 6 as originally proposed by cytogenetical research. Although the mapping sequence data suggest triplication of the ancestral genome involving three events of polyploidy, it is not readily accepted as it fails to explain the origin of extant chromosome numbers. This ancestral hexploid genome (2n ¼ 24) would have required extensive chromosome number reduction to yield 2n ¼ 16, 18, and 20 karyotypes and would require genome downsizing, which is not supported by genome size data. A possible model is proposed by Qiu et al. (2009) to resolve this ambiguity. Since the monogenomic diploids have more or less identical or similar chromosome numbers as the putative tetraploid ancestral genome (ACK, 2n ¼ 16), these diploids might have evolved from it after insertion of transposable elements, segmental duplications, and chromosomal rearrangements rather than undergoing another round of genome duplication followed by chromosome number reduction. Thus, x ¼ 8 can be considered the most likely ancestral chromosome number of the family. Qui et al. (2009) emphasized that transposable elements have played a major role in genome evolution of Brassica species, a view also suggested earlier by Lim et al. (2007) and Alix et al. (2008). For example, transposable elements account for 20% (139 Mbp) of the total DNA content (696 Mbp) of B. oleracea. Brassica genomes also have lower gene density than Arabidopsis, which is associated with larger introns and spacers and extensive gene arrangements. Hence, it appears to be a reasonable explanation that reconciles triplication of sequences and chromosome number changes. However, Mun et al. (2009) although agreeing with the triplication theory, believed that large-scale deletion of duplicated genes in the triplicated genome, along with less accumulation of transposons, resulted in smaller-size Brassica genomes. Considering all these different hypotheses on evolution of diploid karyotypes, an alternative view envisages a reduction in chromosome number in ACK (n ¼ 8) or PCK (n ¼ 7) resulted in a smaller genome. It had six haploid chromosomes (ABCDEFG) and can be regarded as the

30

S. PRAKASH, X.-M. WU, AND S.R. BHAT

progenitor of tribe Brassiceae. We refer to it as ancestral Brassiceae karyotype. Several mechanisms—reciprocal translocations, pericentric inversions leading to generation of acrocentric chromosomes, and elimination of unstable minichromosomes at meiosis—are reported to operate for reducing the chromosome number in Brassicaceae (Lysak et al. 2006; Mand
akov
a and Lysak. 2008). This prototype (ancestral Brassiceae karyotype) subsequently diverged into Nigra and Rapa/ Oleracea lineages 7.3 to 4 Mya (Wroblewski et al. 2000) or about 7.9 Mya (Lysak et al. 2005) (Fig. 2.3). Thus, x ¼ 6 is most likely the basic chromosome number of the tribe Brassiceae and the genus Brassica.

Fig. 2.3. Proposed model of the origin of basic and alloploid Brassica species (solid and broken lines in allopolyploids represent female and male parents, respectively).

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

31

Cytogenetical evidence also unequivocally suggests that the Brassicae ancestral karyotype had a constitution of x ¼ 6. R€ obbelen (1960), for the first time, following pachytene analysis, recognized six basic types of chromosomes in each genome based on absolute length, symmetry of arms, and shape of heterochromatic centromeric region, and proposed that selective chromosome duplication in the archetype resulted in the evolution of basic genomes. According to his scheme in B. rapa, two chromosomes, A and D, are duplicated, and one chromosome, F, is triplicated, with the constitution AABCDDEFFF. B. nigra has the constitution ABCDDEFF and is tetrasomic for chromosomes D and F, and B. oleracea is a triple tetrasomic for three chromosome types B, C, and E with the constitution ABBCCDEEF. Truco et al. (1996) also proposed a model of genome evolution based on the conservation of marker arrangement. The model envisages that these basic genomes were derived from six ancestral chromosomes (W1–W6) (Fig. 2.4), which underwent several duplications and rearran-

A10

A5

C5

A4

B6

C1

B3

A1

B5 W3

C4 A6

C7

W5

W4

Cx W6

C6

C3

W1 W2

A6

A7

Bx

C8 B1

A8 C9

B8 B7

B4 B2

A9 C2

A2

Fig. 2.4. Hypothetical ancestral genome of six chromosomes (W1 to W6) originating specific A, B and C genome chromosomes deduced by homoeologous relationships. Bx and Cx are intermediate chromosomes. Broken lines indicate tentative homologies. (Source: Truco et al. 1996).

32

S. PRAKASH, X.-M. WU, AND S.R. BHAT

gements. C genome chromosomes also gave rise to A genome chromosomes. Two intermediate chromosomes, Bx and Cx, originated from W1. Bx produced B1, B2, B4, and B8 chromosomes, and the Cx chromosome gave rise to A7. Chromosomes Bx and C1 were similar in their genetic content. Chromosomes B7 and C9 might have originated from W6 or independently, one from W6 and other from a seventh ancestral chromosome, W7. The two chromosomes B7 and C9 do not share homology with any other group. Panjabi et al. (2008) used intron polymorphism markers selected from Arabidopsis single-copy genes to construct a detailed molecular map of B. juncea. A comparative study of B. juncea, A. thaliana, and three diploid Brassica genome maps revealed a high degree of colinearity. They also proposed the evolutionary events that might have contributed to karyotype variations in the three basic genomes. Significant similarity between the five linkage groups of A and B genomes was observed. Chromosome rearrangements, mostly translocations, were thought to be responsible for karyotype diversification. Ancestral blocks that remained unaltered since their inception were identified based on map information of the B genome. It was observed that three linkage groups of the B genome (B4, B5, and B6) are similar to the A genome. The remaining five chromosomes—B1, B2, B3, B7, and B8—appear to have originated through (1) rearrangements without any loss of chromosome (B1, B2, B3, and B8 consisting of four linkage groups of A/C genomes: A1–C1, A2–C2, A3–C3, and A10, respectively), and (2) rearrangements with variations in chromosome number (chromosome B7 by fusion of two linkage groups A7–C7/A8–C8). Both A and C genomes display a high degree of collinearity and show only minor changes. However, it is difficult to predict whether these changes occurred in one of the lineages after their divergence or independently in both the lineages. No structural changes were observed in the A1–C1, A2–C2, A3–C3, and A7–C7. The major changes in the evolution of A and C genomes involve rearrangements: mainly the translocations in the C4, C5, and C6, which are specific to the C genome and probably occurred after the diversification of A and C genomes; and C8 and C9 have rearranged blocks. C9 was derived by fusion of half of A9 and entire A10 while C8 is constituted of the other half of A9 and the entire A8. B. Diploid Genomes In spite of their origin from two different lineages, these three genomes possess similar genetic information with many duplications (Slocum et al. 1990; Chyi et al. 1992; Jackson et al. 2000; Parkin et al. 2003).

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

33

However, the gene organization and distribution on chromosomes is different (Truco et al. 1996). Following their evolution, these genomes underwent genetic diploidization and regulation of pairing forming a strictly bivalent regime. Chromosome differentiation and repatterning occurred mainly through duplications and translocations (Hosaka et al. 1990; McGrath et al. 1990; Truco and Quiros 1994; Quiros 1999) as well as deletions (Hu and Quiros 1991). Because of their secondary balanced nature, these changes were tolerated and adjusted (Kianian and Quiros 1992a). The B genome is separared from A/C genomes by a large number of rearrangements and also possesses cytoplasm distinct from A/C types of B. rapa/B. oleracea but still retains some homology (Palmer et al. 1983; Yanagino et al. 1987; Warwick and Black 1991; Pradhan et al. 1992). In comparison, A and C genomes are less differentiated (Lagercrantz 1998) and also cytogenetically very close, as expressed in high degree of chromosome pairing in hybrids between them (Mizushima 1950; Olsson 1960b; Wen et al. 2008). Supporting evidence is provided by: (1) FISH mapping of two families of repetitive DNA, which are confined to pericentromeric regions of most chromosomes of A and C genomes but absent in the B genome (Harrison and Heslop-Harrison 1995); (2) structural analysis of rDNA intergenic spacers (Bhatia et al. 1996); (3) collinearity between these two genomes as revealed by comparative analysis (Scheffler et al. 1997; Panjabi et al. 2008); and (4) extent of homologous pairing detected by genomic in situ hybridization (Snowdon et al. 1997a; Ge and Li 2007), FISH, and molecular markers (Nicolas et al. 2007). RFLP analysis also indicated that C genome is more conserved than A or B genomes as detected by microsatellites (Bornet and Blanchard 2004). These basic species are characterized by very small genomes (Table 2.2). Johnston et al. (2005), using internal transcribed spacers of nuclear ribosomal DNA and 5.8S rRNA gene (ITS), attempted to present an evolutionary overview of family genome size and reported an ancestral Table 2.2.

1c nuclear DNA content and genome size in Brassica species.

Species B. carinata B. juncea B. napus B. nigra B. oleracea B. rapa Source: Johnston et al. 2005.

1c nuclear DNA content (pg  SE)

Genome size (1x) (Mbp)

1.308  0.018 1.092  0.001 1.154  0.006 0.647  0.009 0.710  0.002 0.539  0.018

642 534 566 632 696 529

34

S. PRAKASH, X.-M. WU, AND S.R. BHAT

genome size of approximately 0.20 pg. However, a reconstruction by Lysak et al. (2009) from five data sets found a mean value of 0.50 pg. Thus, there is only a slight increase in genome size. It is also estimated that B. rapa and B. oleracea separated from each other 7.3  4 Mya (Wroblewski et al. 2000; Inaba and Nishio 2002) and incorporation of transposons played a major role in their divergence (Alix et al. 2008). C. Allopolyploid Genomes It is now well established that the three high-chromosome species— B. carinata, B. juncea, and B. napus—originated in nature following alloploid evolution involving different combinations of the diploid species, as proposed for the first time by Morinaga (1934) and subsequently confirmed by U (1935). Several sets of evidence, such as taxonomy, artificial syntheses, molecular analysis, and chromosome mapping and painting, have unequivocally established allotetraploid origin of these three species (see Prakash et al. 2009 for references). It is also conclusively established from the information from Fraction-1 protein (Uchimiya and Wildman 1978) and chloroplast and mitochondrial DNA restriction patterns (Erickson et al. 1983; Ichikawa and Hirai 1983; Palmer et al. 1983; Yanagino et al. 1987; Warwick and Black 1991; Pradhan et al. 1992; Cunha et al. 2004) that B. nigra and B. rapa were the cytoplasm donors of B. carinata and B. juncea, respectively. The maternal parent of B. napus is not yet clearly established. Based on RFLP patterns of the plastid genomes, Erickson et al. (1983) suggested B. oleracea as the C genome donor of B. napus. Subsequent study by Song and Osborn (1992) indicated B. montana, a related wild species of B. oleracea, as the most likely C genome donor of B. napus. However, plastid simple sequence repeats analysis did not support B. montana as the maternal parent. On the contrary, it identified B. rapa as the most likely plastid donor (Flannery et al. 2006). Recently, Allender and King (2010) made a detalied investigation involving a lage number of accessions of B. napus, B. montana, B. rapa, B. oleracea, B. carinata, B. nigra, and B. juncea and employed a combination of chloroplast and nuclear genetic markers to resolve this issue. Their study also ruled out the possibility of any B. oleracea or B. montana having participated in the origin of B. napus and supported polyphyletic origin of B. napus. This is in agreement with the earlier study by Palmer et al. (1983), which suggested that chloroplast genomes in B. carinata and B. juncea are highly conserved since their origin while the chloroplast genome of B. napus has gone through evolutionary alteration. Also, both mitochondrial and chloroplast genomes in all the three species have

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35

been coinherited over generations (Palmer 1988). Considerable cytoplasmic influence on the evolution of nuclear genomes of alloploid species is also reported. The alloploid genomes are highly plastic, and allopolyploidy is accompanied by an increase in DNA amount, but eventually some DNA is eliminated due to diploidization (Lukens et al. 2004, 2006). Narayan (1996) reported the amount of DNA in the allopolyploid species of B. napus, B. juncea, and B. carinata to be less than the sum of their putative parent species by 0.095, 0.094, and 0.049 pg less, respectively, an overall reduction of >6% (Table 2.2). Compelling evidence suggest rapid and extensive structural rearrangements of chromosomes in these alloploid species since their evolution (Slocum 1989; Slocum et al. 1990; Kianian and Quiros 1992a,b; Song et al. 1993, 1995; Poulsen et al. 1993; Harrison and Heslop-Harrison 1995). These chromosomal rearrangements arising as a result of homologous recombination also induce morphological variants (Sharpe et al. 1995; Parkin and Lydiate 1997; Osborn et al. 2003; Pires et al. 2004; Udall et al. 2005; Nicolas et al. 2007). In fact, such morphological and physiological variants of nonhomologous origin have been obtained in synthetic B. juncea population (Prakash 1973b). These events are regarded as progressive steps in evolution. However, Song et al. (1995) disputed this view. Their investigations employing RFLP markers in natural and synthetic B. juncea indicated that the nuclear genomes in B. juncea have not undergone drastic changes and have remained largely unchanged since its origin, a view also supported by Axelsson et al. (2000) and Panjabi et al. (2008). In spite of considerable homolology between chromosomes of the partaking genomes, these present-day allopolyploid species exhibit true diploid-like meiosis devoid of any higher-order chromosome associations. Several mechanisms have been proposed for such bivalent-forming regimes. When the two genetically distinct genomes come together, they should adjust in a common nucleus by regulating gene expression and chromosome pairing. It is suggested by several researchers that this diploid-like meiosis is genetically regulated in Brassica and its related genera (Prakash 1974c; Attia and R€ obbelen 1986; Eber et al. 1994; Sharpe et al. 1995; Jenczewski et al. 2003). The other factors are point mutations, gene conversion, and DNA methylation (Szadkowski et al. 2010). The role of ribosomal RNA (rRNA) genes has also been highlighted as a contributing factor. It is observed in a number of allopolyploids that rRNA genes from only one parent are transcribed while the transcription of such genes of the other parent are suppressed, a phenomenon referred to as nucleolar dominance. A hierarchy of nucleolar dominance—namely, B. nigra > B. rapa > B. oleracea—has been

36

S. PRAKASH, X.-M. WU, AND S.R. BHAT

demonstrated in allotetraploids (Chen and Pickard 1997; Pickard 2000; Ge and Li 2007). These results suggest that nucleolar dominance may contribute decisively in preferential stabilization of chromosomes from the parent exerting nucleolar dominance. All these factors lead to stabilization of newly evolved allopolyploids and their successful colonization (Prakash et al. 2009). III. ETHNOBOTANY, ORIGIN, AND DOMESTICATION A. Origin of Diploid Species A hypothetical model for the origin of Brassica has been proposed by Song et al. (1990) and is depicted in Fig. 2.5. According to this scheme, Brassica or related species with n ¼ 7 and n ¼ 8 evolved from a common ancestor through two pathways: one group comprising Hirschfeldia incana (n ¼ 7) or a closely realated species as the primary ancestor of B. nigra, B. fruticulosa, and others in Nigra lineage. Diplotaxis erucoides (n ¼ 7) or a close relative was the primary ancestor for the other group, which gave rise to B. oleracea, B. rapa, and other species in Rapa/Oleracea lineage. In support, D. erucoides has been shown to be very close to B. rapa/ B. oleracea by Harbinder and Laksmikumaran (1990) based on analysis of repeat sequence (satellite DNA) and nucleotide sequences of the S-locus related gene, SLR1 (Inaba and Nishio 2002). This closeness is also reflected in their nuclear DNA (Song et al. 1990) and chloroplast (cp) DNA (Warwick and Black 1991; Pradhan et al. 1992) and high chromosome pairing in their hybrids (Vyas et al. 1995). This ancestral D. erucoides evolved into a common ancestor having n ¼ 9, which in turn gave rise to B. oleracea and B. rapa. Since B. oleracea is considered to be an older species (Prakash and Hinata 1980; Song et al. 1990), it evolved first. Primitive forms of B. rapa were subsequently derived from one of the wild or very primitive cultivated B. oleracea form. Brassicas are believed to have originated in countries surrounding the Mediterranean basin and further extended into southwest and central Asia encompassing mainly the Mediterranean, Irano-Turanian, and Saharo-Sindian phytogeographical regions. This whole region can be regarded as the cradle of development for this group (Fig. 2.6). This area represents the world’s most traveled corridor of prehistoric times with the migrating people carrying a variety of seeds with them, thus making their diffusion possible. Go´mez-Campo and Prakash (1999) believed that, chronologically, B. rapa (turnip rape) was the first diploid species to be domesticated several millenia ago as a multipurpose crop (e.g., roots in turnip, leaves in Chinese vegetable forms, seed in turnip

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37

Common ancestor, n=7

common ancestor -1, n=7

common ancestor -2, n=7

Diplotaxis erucoides or related n=7 species with A/C type cytoplasm

Hirschfeldia incana or related n=7 species with B type cytoplasm

B. fruticulosa, n=8

bridge species, n=8

B. nigra

common ancestor, n =9

Sinapis arvensis, n=9 primitive B. oleracea,n=9

wild B. oleracea and

primitive B. rapa, n=10

turnip, turnip rape

pak-choi

B. alboglabra, both n=9

primitive cultivated B. oleracea-kales

Cabbage group

sarson group

Chinese cabbage and other leafy forms

Broccoli and cauliflower

Fig. 2.5. Hypothetical model for genetic evolution of Brassica diploid species. (Source: Adapted from Song et al. 1990).

rape and sarson) that was widely adopted by all the civilizations in the regions of domestication. Brassica nigra is also an ancient species. B. oleracea entered into cultivation later as its natural area (Atlantic coast) was too far from major centers of its domestication. Although we do not have any precise information about B. carinata, it seems its domestication history is not too old, similar to B. napus, which entered into cultivation only 400 years ago. These three species (B. oleracea, B. rapa, and B. juncea) are highly polymorphic with a range of morphotypes. B. rapa and B. oleracea with close genomic homologies exhibit

38

S. PRAKASH, X.-M. WU, AND S.R. BHAT

B.napus B.oleracea B.rapa B.juncea

B.carinata

Fig. 2.6. Geographic distribution and probable places of origin of different Brassica species. (Source: Dixon 2007).

parallel series of differentiation in Asia and Europe, respectively, while B. rapa and A genome containing B. juncea exhibit such parallelism in Asia (Table 2.3). These represent the classical examples of parallel structural evolution in plants. Parallelism is apparent also in nuclear DNA variations (Song et al. 1988b). One of the striking features of these species is that while in India, B. rapa and B. juncea are grown for reproductive products (i.e., seeds), in East Asian countries they are cultivated for vegetative growth. Another interesting point is that European B. rapa variation resembles broccoli group of B. oleracea, and the variation in East Asian group of B. rapa is similar to cabbage group of B. oleracea. Nishi (1980) pointed out that this might not be due to ecological adaptations of the plants but rather to cooking habits of the regions concerned and their wider geographical distribution. B. Brassica nigra This species was collected from the wild and subsequently cultivated for its medicinal uses since antiquity. Hippocrates (480 BCE) and Pliny

39

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Latin English/local Distribution

Bush

Elongated stem

Heading

Kohlrabi type

Loose head

Savoy

Stalking type

Turnip

Source: Prakash and Hinata 1980.

var. acephala Kale Worldwide

Latin English Distribution

Basic

var. botrytis, B. alboglabra Broccoli, kailaan Worldwide

var. sabauda Savoy cabbage Worldwide

var. acephala Portuguese kale Atlantic islands

var. gongylodes Kohlrabi Worldwide

var. capitata Cabbage Worldwide

var. acephala Marrow stem kale Europe

var. acephala Thousand headed borecole Europe

B. oleracea

B. rapa ssp. rapifera Turnip Worldwide

Central and S. China, Japan

ssp. chinensis

ssp. pekinensis Hakusai Southeast Asia

ssp. pekinensis Chinese cabbage Southeast Asia

ssp. pekinensis Chinese cabbage Southeast Asia

Japan

ssp. japonica

B. rapa Spinach mustard Japan, China

B. rapa

Nomenclature of parallel morphological variations in Brassica oleracea, B. rapa, and B. juncea.

Type

Table 2.3.

Turnip mustard North China

Kigarashi Japan, China

Chirimen takana Japan, China

Katsuo-na Japan, China

Pickling mustard Central China

Heading mustard South China

Tashin-chetsai Taiwan

Shelifong China

B. juncea Leaf mustard Japan, China

B. juncea

40

S. PRAKASH, X.-M. WU, AND S.R. BHAT

referred to its medicinal value. Greeks believed that it had been made known to mankind by Aesculapius, the god of medicine, and Ceres, the goddess of seeds (Hedrick 1919). The New Testament also mentions it (sı´napi, sinapi). Its natural distribution is in Mediterranean area extending into Middle East and central Asia. It probably originated in central and south Europe (Bailey 1922; Zeven and Zhhukovsky 1975) and was available for domestication to Mediterranean civilizations (Mesopotamia, Egyptian, Greek, Roman), where it was an important condiment. Several herbalists mentioned B. nigra under the name Sinapis. We find S. primum in Mattioli (1571) and Dodonaeus (1578), S. sativum Erucae aus Rapifolis in de Lobel (1581), and Sinapi sativum in Gerarde (1597, 1633). ‘‘It has great virtues because it is hot, dilates the passages and destroys the humours’’ wrote de Glanville (1518) in a French book. The word mustard is believed to be a derivative of Latin mustus ardens because of the pungent seeds. Its Middle English/Old French word is mustarde and was originally an occupational name for a person dealing in hot spices. People in Rhodes consume its infloresecence boiled and seasoned with salt, lemon juice, and olive oil. In Sicily, it is cultivated for medicinal uses while in Turkey, it is used as a spice for flavoring sausage. It is called sanafitch in Ethiopia and is grown for seed oil, spice, as a leaf vegetable, and for medicinal use (Tsunoda 1980). RFLP investigations suggest that B. nigra has diverged much less from the wild ancestor since its origin (Song et al. 1988a). It still shows wild or semidomesticated characters (e.g., tall plant stature, enormous vegetative growth, small-size pods with reduced numbers of small seeds). A related wild species S. arvensis has traditionally been considered very close to B. nigra, which is reflected in high levels of chromosome pairing in their hybrids (BSa, 2n ¼ 17, up to 8 II) (Mizushima 1950). Several investigations substantiate the closeness of B. nigra and S. arvensis, including research on seed proteins (Vaughan and Denford 1968), fraction 1 protein (Uchimiya and Wildman 1978), nuclear DNA RFLPs (Song et al. 1988a; Poulsen et al. 1994), cp DNA analysis (Yanagino et al. 1987; Warwick and Black 1991; Pradhan et al. 1992), 5S rDNA spacer (Bhatia et al. 1993; Capesius 1993), repetitive DNA (Gupta et al. 1990, 1992; Kapila et al. 1996), chemotaxonomic markers (Tsukamoto et al. 1993; Simonsen and Heneen 1995), cytology (Cheng and Hennen 1995), karyotypes (Yuan et al. 1995), randomly amplified polymorphic DNA (RAPD) patterns (Wu et al. 1996), nuclear sequence of S-locus related gene SLR1 (Inaba and Nishio 2002), and ITS/trnL sequence data (Warwick and Sauder 2005). A previous concept was that B. nigra evolved from

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41

S. arvensis, but now it is well setteled that B. nigra preceded S. arvensis (Song et al. 1990). Both these species overlap in geographical distribution and still have not developed a strong reproductive isolation barrier. C. Brassica oleracea 1. Taxonomy and Origins. B. oleracea is a highly polymorphic species with extensive variation in leaf, stem, and inflorescence morphology. It represents a classical example of structural evolution in plants (Plate 2.1). The variants provide a range of vegetable forms and are considered important sources of vitamins and fibers (Lorenz and Maynard 1988; Rubatzky and Yamaguchi 1997) and anticarcinogenic compounds (Rosa et al. 1997). Bailey studied many cultivated forms of B. oleracea and applied for the first time the general term ‘‘cole crops’’ in 1901 in his book Principles of Vegetable-Gardening (Bailey 1922). This B. oleracea complex includes at least six well-defined groups designated as varieties. Snogerup (1980) and Dixon (2007) described the major cultivated groups: 1. Kales (var. acephala), which develop a strong main stem bearing edible foliage and include marrow stem kale, collards, and green and dwarf Siberian kales. Landraces of these kales are widely scattered. 2. Cabbages (var. capitata) characterized by formation of heads consisting of tightly packed leaves and include headed cabbages, Brussels sprouts, and savoy cabbage. 3. Kohlrabi (var. gongylodes) grown for its thickened stout edible stem particularly in China and Vietnam. 4. Inflorescence kales (var. botrytis, var. italica), which are cultivated for thickened edible inflorescences and include cauliflower, broccoli, and sprouting broccoli. Almost all cauliflowers are white- or cream-curded but occasionally forms with colored curds also occur. 5. Branching bush kales (var. fruticosa) used to be grown for edible foliage. These are very popular in European supermarkets as ‘‘fresh leaves.’’ 6. Chinese kale (B. alboglabra) widely cultivated in southeast Asian countries where the flower bud, flower stalk, and young leaves are consumed. It has close morphological resemblance with related wild species B. cretica ssp. nivea. Vast information is available about the antiquity of these cole crops. Maggioni et al. (2010) in a recent and informative article documented in

42

S. PRAKASH, X.-M. WU, AND S.R. BHAT

detail the antiquity and domestication of these crops considering the literary, linguistic, and historical sources and presented the terminolgy used by the Greeks and Romans. Kr´ambh (krambe) was the main word for B. oleracea in ancient Greek (before ca. 330 BCE). Theophrastus described several different forms of cole crops and refers to branching bush kales and stem kales, sometimes with curled leaves. Dioscorides also referred to cole crops, but the original manuscript was not illustrated. The first illustration of various brassicas is found in the Dioscoridean recension known as the Juliana Anicia Codex dated 512 (Plate 2.2). The Romans Cato and Pliny mention several forms of coles including stem kales and headed cabbages. Cato devotes a chapter (De brassica) to cole crops in De Agricultura. Based on their description, it appears that quite a large number of forms were cultivated by Romans. Farmers collected their own seeds and as a result of cross-pollinations because of self-incompatible nature, new variations arose that led to the development of local cultivars through selection. Subsequently, stabilization gave rise to modern-day types. Early Greek and Roman authors used the word caulis, which means ‘‘stem,’’ to define the entire cole plant. Names of cole crops in modern European languages are derived from it: Kohl in German; cole, collard,  and kale in English; kal in Scandinavian; cal in Gaelic; cole in Spanish; chou in French; cavolo in Italian; and couve in Portuguese. Medieval information about cole crops can be found in the Capitulare de Villis imperialibus, which describes plants occurring in the garden of Charlemagne (ca. 800 CE). Cauli, probably kale or cabbage, and ravacauli, kohlrabi, are mentioned. Several Ibero-Arabic treatises describe brassicas in detail. The best-known ones, by Ibn-al-Awam (12th century) and Ibn-al-Baithar (13th century), draw heavily from Greek and Roman writings. Kale is described as caules onati in the 14th-century Tacuinum Sanitatis, the illustrated manuscripts based on an 11th-century Arabic manuscript Taqwim al-Sihha bi al-Ashab al-Sitta (Rectifying Health by Six Causes) written by Sa’dun Ibn Butlan of Baghdad (Dauney et al. 2009). Cultivated B. oleracea forms have been well depicted in paintings produced in Flanders and Holland from the 16th to 19th century (Zeven and Brandenburg 1986). Pieter Aertsen (1509–1575), his nephew Joachim Beuckelaer (1535–1575), and Floris Gerritsz van Schooten (1590–1655) painted cauliflower and cabbage. Cauliflowers are of normal size and the curd is well formed. Floris van Dijck (1575–1651) and Frans Snijders (1579–1657), however, painted cauliflower with loose curds. A painting by Adriaen van Utrecht (1599–1652) shows cauliflower with both long and short stems. Cabbages are more

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43

commonly painted than cauliflower. Gerard Dou (1613–1675), Joachim Beuckelaer, and Peter Aertsen frequently depict cabbages in their paintings. Red cabbage is painted by many artists and must have been quite common at that time. Lucas van Valckenburg (1540–1597) illustrates a red cabbage with greenish leaves and reddish ribs. Although kale was common during this period, it is not found in paintings; Brussels sprouts are not found in this period. Almost all the 16th- and 17th-century illustrated herbals have extensive descriptions of cole crops. One of the earliest was by Macer Floridus in De Herbarum viribu (1506), where the plant appears to be wild and is called caulis (Henslow 1908). Dodonaeus (1583) described several forms; one of these, Flourie Coleivort (Brassica Cypria), appears to refer to cauliflower and is described in this way: ‘‘the small stems grow together in the center, thick set and fast throng together’’ (Giles 1941). Gerarde (1597) in The Herball or Generall Historie of Plants devotes an entire chapter to cabbages and gave 15 examples of coleworts or forms of B. oleracea (Fig. 2.7). Brussels sprouts are referred to as Brassica capitata polycephalos in Dalechamps (1587), B. ex.capitibus pluribus Bauhin 1623), and B. polycephalos (de Lobel 1581). Cabbage is referred to as B.quartum genus (Fuchsius 1542), Caulis capitularis (Tragus 1552), B. capitata (Mattioli 1571), B. capitata albida (Dalechamps 1587), B. alba sessilis glomerata, aut capitata Taclucae habitu (de Lobel 1581), B. capitata alba (Bauhin and Cherler 1651), and B. capuccia (Durante 1585). Kohlrabi is named B. caule rapum gerens (Dodonaeus 1583), Rapa Br. peregrine, caule rapum gerens (de Lobel 1581), B. raposa (Durante 1585; Dalechamps 1587), B. gongylodes (Mattioli 1571), Caulorapum rotundum (Gerarde 1597, 1633), and B. caulorapa (Bauhin and Cherler 1651). Precise information about the progenitors of these brassicas is unavailable although several theories have been proposed. It was earlier believed that all the cole crop forms evolved through mutations, human selection, and adaptation from the primitive kales growing wild along the Mediterranean coast from Greece to England, where it might have been cultivated by Celts. Kale traveled to the eastern Mediterranean region between first and second millennia BCE, where it became fully domesticated with explosive diversification giving rise to a range of cultivated forms. However, this concept is disputed at present, and the Mediterranean kales are considered as mere escapes from early cultivation. These species occur in cliffs and in rocky islets, in more or less small isolated places with distinct ecogeographical centers and mainly confined to Mediterranean region (Fig. 2.8). These wild forms are closely related to cultivated forms and might have participated in their origin and domestication. Snogerup (1980) has grouped them in this way:

44

S. PRAKASH, X.-M. WU, AND S.R. BHAT

Fig. 2.7.

Illustrations of various cole crops and mustard. (Source: Gerard 1633).

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

45

Distribution of wild B. oleracea

B. oleracea

B. montana

B. rupestris-Incana complex

B. hilarionsis

B. insularis

B. cretica

©EnchantedLearning.com

Fig. 2.8. Distribution of wild species of Brassica oleracea complex. (Source: Snogerup 1980).

B. cretica grows in the Aegean area, southen Greece, and southwestern Turkey. It is a woody and much-branched perennial plant. Ssp. nivea occurs in Paloponnesos and Kriti while ssp. cretica grows in maritime cliffs. B. rupestris-incana complex. A number of regional variants in this complex occur in Sicily and south-central Italy. The different variants include B. incana, B. villosa, B. rupestris, and B. drapenensis. However, their ranks are uncertain. These are characterized by tall main stem and large petiolated leaves. B. insularis occurs in Corsica, Sardinia, and Tunisia. It is characterized by stiff, fleshy, glabrous leaves and large fragrant flowers. B. macrocarpa is endemic in west Sicily with very thick fruits containing seeds in two rows in each locule. B. montana occurs in northeastern coastal area of Spain, southern France, and northern Italy. It is a shrubby perennial plant. B. oleracea occurs on coasts of northern Spain, western France, and southwestern Britain. It is a stout perennial plant with a strong vegetative stock.

46

S. PRAKASH, X.-M. WU, AND S.R. BHAT

B. hilarionis with a very narrow endemism in the Kyrenia Mountains of Cyprus, very much resembles B. macrocarpa except for large pink flowers. These wild species, all 2n ¼ 18, are easily crossable with oleracea forms and produce fertile or semifertile hybrids (Kianian and Quiros 1992c; Go´mez-Campo 1999). Harberd (1972) assigned them to the same cytodeme or crossing group in a cytotaxonomical investigation while Gladis and Hammer (1992) suggested subspecies status to them. Bailey (1922, 1930) described a number of cultivated forms, created some new species, and suggested wild B. oleracea as the possible progenitor. Neutrofal (1927) and Snogerup (1980) believed B. montana to be the progenitor of cabbage and kales and B. rupestris of kohlrabi, while Schiemann (1932) suggested different Mediterranean wild species as the progenitors. Schulz (1936) specifically mentions the role of B. cretica in the origin of cauliflower and broccoli. Helm (1963) in a detailed scheme of evolution of different forms (Fig. 2.9), proposed three different pathways for the origin of different forms from wild B. oleracea but did not specify precisely any species. Accordingly, in one direction, the oldest form var. ramosa (thousand-headed kale) gave rise to var. gemmifera probably in Belgium from which developed monstrosities such as var. dalechampi. In another direction, the wild cabbage was the progenitor of var. costata (Portuguese kale), which originated in the Iberian peninsula. Cabbage (var. capitata) and savoy cabbage (var. sabauda) both derived from it in Italy. The kales and collards (vars. acephala, sabellica, selensia, and palmifolia) gradually developed from one stock that also gave rise to the forage crop marrow stem kale (var. medullosa), which also gave rise kohlrabi (var. gongylodes). Sprouting broccoli (var. italica), which initially developed from wild var. sylvestris, gave rise to cauliflower, with both the forms originating in the eastern Mediterranean. However, in recent years, these concepts have changed; these Mediterranean kales are regarded as mere escapes from early cultivation. At present, a polyphyletic origin is proposed from several wild Mediterranean B. oleracea (Gustafsson 1979; Snogerup 1980; Mithen et al. 1987). Several wild species are mentioned in this context, although the molecular investigations did not support this concept (Hosaka et al. 1990; Song et al. 1990). The low chloroplast diversity does not indicate multiple domestication events (Allender et al. 2007). Gates (1953), following a study of different wild species and cultivated forms, came to the conclusion that cabbages, Brussels sprouts, and kale originated from B. oleracea var. sylvestris in western Europe, cauliflower and broccoli in the eastern Mediterranean, and kohlrabi in the middle

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

47

Fig. 2.9. Schematic representation of the origin of various Brassica oleracea cultivars. (Source: Adapted from Helm 1963).

Mediterranean. In recent years, the theory of origins again reverted to the old concept of implicating wild Atlantic B. oleracea as the progenitor with subtantial introgressions from different wild species, which had been responsible for increasing the varaibility and adaptability of cultivated forms. Song et al. (1988b, 1990) carried out studies on cultivated and wild forms within B.oleracea group using nuclear DNA RFLPs, divided them into three groups (kales, cabbages and broccoli), and suggested a monophyletic origin. Louarn et al. (2007), based on microsatellite marker investigations, agreed with this grouping. Song et al. (1988b) believed that ancient wild progenitor was similar to wild B. oleracea and B. alboglabra, which must be the closest ancestors of cultivated forms. The earliest cultivated form was probably a leafy kale from

48

S. PRAKASH, X.-M. WU, AND S.R. BHAT

which originated a variety of kales due to natural hybridization, gene introgression, and selection along the Mediterranean coast and north Atlantic from Greece to Wales. However, the linguistic, literary, and historical sources favor the origin of B. oleracea in the north-central and northeastern Mediterranean extending from southern Italy to Greece and the west coast of Turkey (Maggioni et al. 2010). This whole region also overlaps with the distribution of related wild species of B. oleracea. Many studies in recent years have been carried out to investigate the evolutionary relationships between these wild taxa and between them and crop types to assess their possible role in the evolution of crop forms using both nuclear and organelle-based molecular markers (L
azaro and Aguinagalde 1996, 1998a,b; Lann
er 1998; Panda et al. 2003; Allender et al. 2007; Louarn et al. 2007; Mei et al. 2010). Although the results from nuclear and cp genomes are not consistent, these sudies broadly suggested the possibility of co-ancestry and gene flow between wild and crop types. There is a close association of cultivated types and B. incana, B. montana, B.cretica, and B. hilarionis (Mei et al. 2010). At the same time, the relative lack of cp diversity in these species (Panda et al. 2003; Allender et al. 2007) indicates a single rather than multiple centers of domestication of cole crops. 2. Cabbage. Neolithic farmers collected cabbage for food before it entered into cultivation. The word cabbage is a derivative of Latin caboche or caputium, meaning ‘‘head.’’ It was an important ingredient of Greek and Roman cuisine. However, the early forms did not form a compact head as found in modern cultivars. De Candolle (1824) believed that it was independently domesticated by the Basques and also at different places in Europe. In evidence, he cited several names for cabbage: kap or kab, caul or kohl in Latin, German, and Celtic. However, the idea of domestication by Celts in western and northwestern Europe is not very convincing since all the Celtic names are derived either from Greek (krambai and kaulos) or Latin (brassica, caput, olus and caulis). Most likely, the invading Celts in 6–8th-century BCE found it already domesticated by the native Ligurians and Iberians and adopted it along with its name. Another point of contention is how a wild plant from the Atlantic coast reached Egypt and Mesopotamia. Go´mez-Campo and Gustaffson (1991) believed that cabbages migrated along the sea tin route linking the British ‘‘Casiteride’’ Islands with the eastern Mediterranean. The Tartessians from southwest Spain were exploring the tin mines of Cornualles and traded tin with the seafaring Phoenicians. The Greek word krambe for ‘‘cabbage’’ is most likely of Phoenician origin. A word shaw’t in Papyrus Harris, a document written in 1166 BCE on the death of

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Ramses III comprising a list of offerings to the god Amon, has been interpreted as ‘‘cabbage.’’ However, its authencity is questionable (Aufrere 1987; Nunn 2002) as the Egyptians used the word gramb for cole crops, which is a possible derivative of Greek krambe. The Greek Theophrastus and the Romans Cato and Pliny mentioned stem cabbage kales and headed cabbages. Theophrastus mentions three and Dioscorides mentions six types of cabbage, indicating a diversity of forms at that time. Ch evre et al. (1998) describe the myriad uses of cabbage in 16thcentury French books. According to Mizauld (1578): ‘‘The ancient Egyptians, who dearly loved wine, used to eat cooked cabbage at their meals before eating anything else; and at their banquets and feasts the first dish used to be cabbage so that the wine should not harm them. The juice of raw cabbage sipped with wine serves as a remedy against vipers’ bites; and as a plaster with fenugreek flour is a sovereign remedy against gout and other diseases of the joints.’’ Brussels sprouts are supposed to have been developed in 14th century near Brussels in Belgium. Gerarde (1597, 1633) described a similar form of kale with finely dissected leaves and numerous buds as ‘Parseley cabbage’ (Henslow 1908). It is reported that these sprouts were served at the royal wedding feast of Alcande de Bredrode in 1481 at Brussels (Hyams 1971). 3. Cauliflower and Broccoli. Cauliflower and broccoli produce large dense structures made up of modified infloresences. In cauliflower, the undifferentiated mass of inflorescence meristems form a structure called curd. About 10% to 15% of the meristems develop into normal flowers with the rest aborting. The word cauliflower is dervied from Latin caulis (stem) and floris (flower) or Greek kaylo´z. It is believed that both these forms evolved in eastern Mediterranean (Hyams 1971; Snogerup 1980). Although early Greeks and Romans mentioned sprouting forms of cabbage, probably a distinction was not apparent between broccoli and cauliflower. Possibly both were considered as variants of the same form. Yahya ibn Muhammad Ibn-al-Awam, a Moor living in Spain in the 12th century, was the first to make a clear distinction between heading and sprouting forms. He compiled a Spanish-Arabic treatise Kitab-al-Felahah (Book of Agriculture, ca. 1140) wherein he devoted a full chapter to cauliflower, described three types, and called it Syrian or Mosul cabbage or quarnabit, the current Arabic word for ‘‘cauliflower.’’ Ibn-al-Baithar, in the 13th century, also mentioned it. Hyams (1971) is of the opinion, based on Ibn-Al-Awam’s observations, that cauliflower was, noticed, selected, and propagated in Syria. Dodonaeus (1583), while describing various forms of cole group, referred to it as B. cypria, indicating its possible origin in Cyprus. It is now generally regarded that cauliflower originated from

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broccoli (Giles 1944; Crisp 1982; Gray 1982). This is also supported by Smith and King (2000), based on the distribution of alleles for curd development in B. oleracea. In fact, this close relationship between these two forms is further substantiated by the presence of a nonsense mutation in a floral gene (Purugganan et al. 2000). Crisp (1982) hybridized cauliflower and broccoli, which led him to conclude that a single major gene mutation in broccoli produced cauliflower. In recent years, use of various molecular markers has unraveled the molecular genetic basis of domestication in several crops including cauliflower. Several floral homeotic genes controlling flower traits have been identified in Arabidopsis thaliana. Mutations in these genes cause floral deformities. These genes belong to MADS-box regulatory gene family (Yanofsky 1995; Riechman and Meyerowtz 1997) and include APETALA 1 (AP1) responsible for floral meristem identity and correct specification of sepals and petal organs (Mandel et al. 1992; Gustafson et al. 1994). The other gene CAULIFLOWER (CAL) also specifies the floral meristem identity (Kempin et al. 1995). Mutations in both these genes arrest the development at the inflorescence meristem stage and result in a dense mass of inflorescence meristems as in cauliflower (Kempin et al. 1995). These results suggest the involvement of B. oleracea orthologues referred to as BoCAL (Kempin et al. 1995) and BoAPL (Anthony et al. 1993, 1996; Carr and Irish 1997) in curd formation. Further studies by Lowman and Purugganan (1999) revealed that BoAPL is present in two copies in B. oleracea genomes and are referred to as BoAPL-A and BoAPL-B. Mutant genes have a reduced ability to specify floral meristem identity. BoAPL-B is transcriptionally silenced in both cauliflower and broccoli and appears to be a pseudogene. Genetic studies by Crisp and Tapsell (1993) suggested the involvement of several loci in curd formation with at least one major and several modifier genes. Lowman and Purugganan (1999) believed that variation in at least two loci is responsible for curd formation: a nonsense mutation in BoCAL and a 9 bp insertion in exon 4 at BoAPL-B. Brassica oleracea ssp. botrytis still possesses a functional BoAPL-A gene as the flowers that are produced from the curd are normal. Smith and King (2000) reconstructed the possible events leading to domestication of cauliflower based on genetic, phenotypic, and molecular information, together with ecogeographic distribution of alleles, and proposed a two-step process. They considered Sicilian Purple types as a primitive curding type that was selected following introduction of a mutant BoCAL-a or BoAP1-a allele into the gene pool of basic heading plants. Follwing the introduction of a mutant copy of the second locus, either BoCAL-a or BoAP1-a, present-day cauliflower with fully developed curd evolved. This specific

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genetic architecture with curd formation to develop normal flowers and capability to produce seeds was selected by farmers so that the mutant could be preserved (Purugganan et al. 2000). Broccoli includes several heading forms with a single large terminal inflorescence made up of a mass of fully differentiated flower buds of which only few abort before flowering. A related form is sprouting broccoli, where the inflorescence is branched. The word broccoli is derived from the Italian brocco and the Latin brachium, which means ‘‘arm’’ or ‘‘branch’’ (Bosewell 1949). Cultivation of broccoli dates back to an earler period than cauliflower (Vilmorin 1885). It is believed that the raw forms were introduced to Italy from the eastern Mediterranean during the fourth to sixth century BCE, where diversification took place and many forms similar to modern types, including heading and sprouting forms, originated (Schery 1972). Ancient Romans referred to broccoli as cyma. The first documented description of it was given by herbalist Dalechamps (1587) in Historia Generalis Plantarum; it is called ‘‘sprout cauliflower’’ or ‘‘Italian asparagus’’ in Miller’s Gardeners’ Dictionary of 1724 (Hedrick 1919). 4. Chinese Kale (B. alboglabra). Although originated and cultivated in initial stages in Mediterranean, Chinese kale was domesticated in southern China (Guangdong Province). It represents an ancient domesticate without any history of wild progenitors, although possible similarities to B. cretica ssp. nivea are apparent (Dixon 2007). It does not require vernalization and it flowers early. Su shi (1037–1101), a famous poet and gastronomist in the Song dynasty, praised it as delicious as mushroom in a poem. A number of more primitive varieties of B. oleracea that were once under cultivation have either disappeared or are grown only in a very limited area. These include branching or thousand-headed kales and true kales and collards (var. ramosa and var. viridis) and palm cabbage—var. palmifolia, which had a wider distribution in Italy (Hamelt 1998; Farnham et al. 2008). Nonheading forms of cabbage became popular in the British Isles, Portugal, and Spain and were known as coleworts by the English, a term that became ‘‘collards’’ in the Americas during the 1700s (Zohary and Hopf 1993). Collards are considered the oldest forms of cultivated B. oleracea. D. Brassica rapa 1. Taxonomy and Origin. The cultivated forms of Brassica rapa, a highly polyomorphic species, exhibit distinct infraspecific types and comprise three different groups:

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1. Oleiferous. Grown in Canada, Australia, and Europe, where it is known as turnip rape. The forms cultivated in the Indian subcontinent are called sarson. 2. Leafy forms. Extensively cultivated in southeast Asian countries as vegetables. These are also used as oilseeds in central and southern China. 3. Turnip or root-forming type. The root-forming types are grown for vegetable and fodder with a wide global distribution. The antiquity of oilseed B. rapa is not well documented, although references to oleiferous forms are found in ancient Indian Aryan literature (ca. 1500 BCE). B. rapa seeds were found in the stomach of Tollund man (a mummified corpse of the fourth-century BCE found in Scandinavia) (Renfrew 1973). Wild forms of B. rapa grow from the western Mediterranean region through Europe to central Asia and the Near East (Sinskaia 1928; Vavilov 1949; Mizushima and Tsunoda 1967; Zeven and Zhukovsky 1975; Tsunoda 1980). The Fertile Cresent region comprising present-day Iran-Iraq-Turkey is most likely the place of its origin. It probably was first domesticated at some of these places perhaps several millennia ago. B. rapa in one way or other has been widely used by all the civilizations in this region. Burkill (1930) suggested Europe as the place of its origin and also believed that it was originally biennial but, through selection and domestication, annual forms were developed. Sinskaia (1928) and Vavilov (1949) strongly considered central Asia, Afghanistan, and the adjoining northwest part of the Indian subcontinent as one of the independent centers of its origin. Based on comparative morphology, Sun (1946) proposed the existence of two races, the Western race comprising oilseed forms and turnip, and the Eastern race comprising vegetable forms. Protein analysis (Denford 1975), isozyme distribution patterns (Denford and Vaughan 1977), nuclear RFLP (Song et al. 1988b), RAPD (Chen et al. 2000; He et al. 2003) and Amplified fragment length polymorphism (AFLP) studies (Guo et al. 2002; Zhao et al. 2005; Takuno et al. 2007) substantiate the existence of two races. The most likely explanation is that these groups represent two independent centers of origin with Europe being the primary center for oleiferous forms. Turnip later traveled further eastward through the Middle East. Once the primitive or semidifferentiated types entered India and China, they developed toward oilseed forms in India and toward leafy forms in China, primarilysouth China. China is also the center of origin of a unique form of ssp. oleifera (oilseed form) (Li 1981). 2. European Forms. European and North American oleiferous forms are quite distinct from Indian forms. It is believed that Europe took to its

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cultivation in the early Middle Ages. The first commercial plantings of B. rapa occurred in the Netherlands in the 16th century; its oil was first used for lamps and as lubricants in steam engines. Since World War II, its cultivation was taken up on a large scale in Europe and Canada, where at present ‘‘double-low’’ cultivars dominate. European and Canadian oilseed forms, spring-type cool-season crops, possess better cold tolerance. For this reason, they have become the predominant crop in the more northern regions of Europe and in some parts of Scandinavia. In Canada, it is often referred to as Polish rape or summer turnip rape. 3. Indian Forms. The Indian forms comprise three ecotypes: brown sarson, yellow sarson, and toria. Brown sarson is believed to be the oldest, and has been identified with the Sanskrit word sarshap. The modern Hindi word sarson appears to be a derivative of sarshap. Two views exist regarding its origin: (1) it evolved independently from the original stock in the northwest of India in the foothills of Himalayas, or (2) it reached nortwestern India in a subdifferentiated state through Iran. Hinata and Prakash (1984) are of the view that only primitive forms entered India with migrating people and from these the brown sarson was the first to evolve in northwestern India and later spread eastward. Two forms of brown sarson are cultivated in India, the self-incompatible lotni and the self-compatible tora. Since all the cultivated and wild forms of B. rapa are self-incompatible, it is assumed that lotni is older and tora is a derivative form. The tora form is very similar to yellow sarson in inflorescence shape, flower morphology, introse anthers, and growth rate. The only difference is in the brown seed color. In view of these similarities and its cultivation in the traditional yellow sarson area, Hinata and Prakash (1984) proposed that the tora form arose through hybridization with yellow sarson while lotni brown sarson arose somewhere in eastern India. In fact, these tora forms can be produced easily through such hybridization. Cultivation of yellow sarson is confined to a very limited area in eastern parts of India. In all probability it evolved from brown sarson as a mutant. Yellow sarson is characterized by yellow seeds and self-compatibility. Another important feature is the occurrence of 2-, 3-, and 4-valved siliquae. Yellow sarson has flowers of higher growth rate after the initiation than self-incompatible brown sarson. Its self-compatibility trait is controlled by a modifying gene (m) that is independently inherited from the S alleles. This recessive epistatic gene m suppresses the action of S allele on the stigma side but not on the pollen side. It was selected by farmers because of its attractive yellow seed color and a deceptive bold seed size. It was mentioned as siddhartha in Sanskrit literature of 1000 BCE. Hinata and Prakash (1984)

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suggested the tentative dates and place for its origin as ca. 1200 BCE in northwestern India. Toria perhaps evolved as a mutant form of the brown sarson population, differing in being dwarf with a shorter life cycle. Lotni brown sarson, being self-incompatible, is allogamous and hence can allow perpetuation of mutant alleles in its population. Most of the variability in toria is met within types from submountainous tracts of the Himalayas where toria-like plants were selected from brown sarson populations and thrived in relatively warmer climates. In spite of numerous references to brassicas in Sanskrit literature, the descriptions are not precise enough to identify the species. Several names referring to these crops are mentioned, such as rajika, swesarshapa, and siddartha. Hinata and Prakash (1984) proposed that sarshap connotes only brown sarson and siddhartha yellow sarson. 4. Chinese Forms. The vegetable forms of B. rapa (Plate 2.3) are extensively cultivated in China, Korea, Malaysia, Vietnam, Taiwan, Indonesia, and Japan. These are eaten fresh as salad, boiled, or salt-pickled. Because of foliar diversity, much confusion arose in naming various forms. Linnaeus (1753) described B. chinensis, for the first time, using plants raised from the seeds collected in China by Osbeck in 1751. Subsequently, many investigators described them under various names (Prakash and Hinata 1980). Bailey (1922, 1930) assigned species ranks to these varieties as B. parachinensis, B. pekinensis, B. narinosa, B. chinensis, and B. nipposinica. At present, these have been designated as subspecies by most researchers and include: ssp. chinensis Pak choi with large thick leaves and broad thick white petioles and does not form a head ssp. narinosa Resembles ssp. chinensis but differs from typical pak choi types by its flat appearance and many dark green leaves ssp. japonica Pot herb mustard. Forms a large stump with many narrow thin leaves ssp. pekinensis Chinese cabbage. Cabbage-like heads of different shapes formed by tightly overlapping light green large leaves with a wrinkled surface that have large white midribs It is now widely accepted that these forms originated from oilseed forms after B. rapa it was introduced into China, probably in the first century CE, through western Asia or Mongolia (Burkill 1930; Nishi 1980). There is supporting evidence in the Yun T’ai in Ch’i-min-yao-shu, a Chinese agriculture treatise of the fifth or sixth century (Li 1969). Li (1982) has discussed the origin of various forms as represented in Fig. 2.10.

2. HISTORY, EVOLUTION, AND DOMESTICATION OF BRASSICA CROPS

Fig. 2.10.

55

Origin of various leafy forms of Brassica rapa. (Source: Adapted from Li 1982).

Pak-choi (ssp. chinensis) with a narrow or wide green-white petiole was the first to evolve in central China and is most closely related to the primitive European forms (Song et al. 1988b). Its antiquity is suggested by a vast range of morphological varations (Li 1982) and high level of DNA polymorphism (Figdore et al. 1988; Song et al. 1988b). Among the East Asian forms, this is the most primitive type from which originated ssp. parachinensis in central China. The Chinese cabbage (ssp. pekinensis) has a well-documented history and origin (Li 1982). It first appeared as a loose-leaved form as a result of hybridization between pakchoi and turnip in the 10th century in the city of Young-Chow. A book Ben-Cao-Tou-Jing (The Classics of Illustrated Medical Herbs) by Su Song has recorded this information. Its hybrid origin is also supported by nuclear RFLPs (Song et al. 1988b). This primitive form is still grown in southern China. The appearence of a heading form with thick petioles is documented in the 12th century for the first time. Semi-heading and solid compact head forms subsequently evolved. These two forms are

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mentioned in the 14th-century treatice, Shua-Pu-Tsa-Su (Miscellanea of Gardening). Selection by farmers for better types resulted in heads with fluffy tops or fully solid heads, which were described in ShuinTian-Fu-Tse (Local Records of Shuin Tian Fu), a compiliation of the 17th century. These vegetable forms are also extensively grown in Japan and are believed to have entered through China or Siberia in the Meji era in the 19th century (Aoba 2000). During cultivation, a unique vegetable form, ssp. japonica, was selected by farmers. It possesses many basal branches and leaves. Because of its close similarities to B. juncea, it is suggested that natural hybridization with B. juncea might have played a role in its evolution (Nishi 1980). There are two prominent forms: Mizuna with deeply dissected bipinnate leaves and Mibuna with slender entire leaves. 5. Turnip. Turnip is of European origin, and its seeds have been excavated from Neolithic sites in Switzerland, 8000 BCE (Hyams 1971). The domestication history is ancient, as is evident from the Assyrian word laptu, ca. 1800 BCE (Oppenheim et al. 1973; Vogl et al. 2007). Turnip is mentioned during the period of Ashur-Nasir-Apli in the ninth century BCE (Leach 1982). The earliest record of its cultivation is found in a list of plants grown in the garden of Merodachbaladan (722–711 BCE) in Babylonia (Zohary and Hopf 1993). It is also referred to in the Jewish Mishna composed in the first century. De Candolle (1886) proposed its cultivation in Europe around 2500–2000 BCE and its spread to Asia after 1000 BCE. Many Semitic, Greek, and Slavic words, such as meip, erifinen, rapa, and rippa, indicate the antiquity of its domestication (Reiner et al. 1995). Turnip formed an important component of the cuisine of ancient Greek and Roman civilizations. There are charred remains from the ancient site of Sparta in Greece (Hather et al. 1992). It appears that biennial forms of turnip were selected for food value of the swollen hypocotyl. A Chinese book Shih Ching (Chinese Book of Poetry) comprising poems that were composed between 1000–500 BCE and said to have been edited by Confucius (551–479 BCE) refers to turnip as feng (Keng 1974). Theophrastus mentioned it as gongylis, and this name is used in the Juliana Anicia Codex of Dioscorides from 512 CE that contains an image of turnip (Plate 2.2). Both Columella and Pliny described different types of turnip. Pliny used the word napus and mentioned five types: Cornithian, Cleonaceum, Liothasium, Boeoticum, and Green. Columella provides significant information about turnips and described Long Roman, Round from Spain, the Syrian, the White, and the Egyptian. During the

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Middle Ages, turnip was an important food plant in Europe. It is referred to as napi in Capitulare de Villis of Charlemagne (ca. 800); as ruba by Hildegard von Bingen (1098–1179), and as napo and rapa by Albertus Magnus (1193–1280) (Vogl et al. 2007). It is also mentioned and illustrated in the late 14th-century handbook Tacuinum Sanitatis (Daunay et al. 2009). The word turnip is derived from the Middle English word nep from napus, which together with turn (made round) became turnip (Bosewell 1949), but this word appeared only after 1400. In the early 16th century, rape and turnep were still in use to indicate this plant. Many herbalists frequently mentioned turnip of two types, the common flat and the long ones. Hedrick (1919) lists the many names used by herbalists: Rapum (Mattioli 1571), Rapum vulgare (Dodonaeus 1578), and Rapum majus (Gerarde 1597, 1633) for the flat turnips; Rapum tereti, rotunda oblangaque radici (de Lobel 1581), Rapum oblongius (Dodonaeus 1578), Rapum rediceoblonga (Gerarde 1597, 1633) and Rapum sativum rotundum et onlongum (Bauhin and Cherler 1651) for the long ones. It is a very well known vegetable in the entire Middle East (Arab: lift, Persian: salgham). It probably arrived with the invading armies and from there spread eastward to India, where it also is known by the Persian word salgham. Turnip now has a bad image as a poor man’s crop. E. Brassica carinata Ethiopian mustard is cultivated on the East African Plateau, particularly in Ethiopia and in parts of the east and west coasts of the African continent. No information is available regarding its origin. It is considered to have evolved in the highlands of Ethiopia and adjoining portion of East Africa and the Mediterranean coast (Go´mez-Campo and Prakash 1999). Brassica nigra, which grows wild in this region, and a kale-like form that has been in cultivation since ancient times are the possible ancestors (Mizushima and Tsunoda 1967), and which underwent natural hybridization in the remote past (Prakash and Hinata 1980; Song et al. 1988a), a point demonstrated by observing wide genetic diversity based on RAPDs (Teklewold and Becker 2006). In Ethiopia, resource-poor small-holder farmers produce the crop for several uses. Young tender leaves and stem tips are eaten raw in salads while older leaves and stouter stem portions are cooked and eaten like collards. Flowering stalks may be cooked and eaten like broccoli. The seeds are used for a mustard preparation and as a source of edible oil. Ethiopian mustard has also been reported as a useful fodder crop. Because of its better drought tolerance and resistance to fungal

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pathogens, it is gaining area in semiarid areas of southern Europe, western Canada, Australia, and India (Malik 1990; Rakow and Getinet 1998; Cardonea et al. 2003). F. Brassica juncea 1. Taxonomy. The history of mustard utilization and domestication dates back to 6000–7000 years ago. Carbonized mustard seeds have been excavated from Banpo in China (ca. 4800 BCE), which contains the remains of several well-organized Neolithic settlements (Institute of Archaeology Report, 1963) as well as from a site in the Indus Valley (ca. 2500 BCE) in the northwest part of the Indian subcontinent (Allchin 1969). There are references in ancient Indian and Chinese literature as early as 2500 BCE (Prakash and Hinata 1980; Hinata and Prakash 1984; Go´mez-Campo and Prakash 1999; Manohar et al. 2009). The earliest Chinese literature record of brassicas being used as a vegetable appeared in Xiaxiaozhen (Ancient Almanac) in the Xia dynasty (about 3000 BCE) and Shijin-Gufeng (A Collection of Poems) in the Zhou dynasty (1122–247 BCE). The species entered Europe during the Middle Ages as a medicinal crop and was later grown as a vegetable, condiment, and oil crop (Hemingway 1976). Because of its highly polymorphic nature and importance for human nutrition, B. juncea has long attracted the attention of botanists, taxonomists, and plant breeders. In ancient times, Greeks used the word aı´n while Romans referred to it as sinapi. Pliny described it as thlaspi. Herbalists mentioned its use for medicinal purposes and described it as Sinapi alterum (Mattioli 1571) and S. sativum alterum (Dodonaeus 1583; Gerarde 1597, 1633). Since the 17th century, many expeditions were carried out to collect different accessions of B. juncea in several countries; they resulted in a vast accumulation of synonmy, which was described either under Sinapis or Brassica (Prakash and Hinata 1980). The botanists Cosson of France (1859) and Czernjaew of Russia (1859) finally transferred it to Brassica with the species name juncea. Hooker and Thomson (1861), for the first time, reported polymorphism in B. juncea particularly the large variations in leaf shape. Chiefly due to this character, it was accorded the rank of subspecies and occasionally species. Bailey (1922), in a comprehensive investigation on various forms of B. juncea primarily collected from China and Japan but also from India and Europe, confined his observations mainly to variations in leaf form. He created several botanical varieties: crispifolia, having large crisped curled and fringed leaves; japonica with pinnatifid basal leaves; and multisecta with multifid leaves.

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Vaughan et al. (1963), who reviewed the taxonomy and vast synonymy of B. juncea in detail, considered morphological variations, volatile oils, and seed protein characters to place all the variations into four well-defined groups: B. juncea var. sareptana with lyrate lobed basal leaves and includes S. ramosa Roxb., B. juncea Hook. Fil. & Thomson (Prain), B. besseriana Andrz., B. juncea Coss. (Bailey), and B. juncea var. sareptana Sinsk. B. juncea var. integrifolia with entire or small lobed basal leaves, including B. rugosa var. cuneifolia Prain, S. patens Roxb., B. juncea var. foliosa Bailey, B. integrifolia Rupr., B. juncea var. subintegrifolia Sinsk., and B. juncea var. integrifolia Sinsk. B. juncea var. japonica with dissected basal leaves, including B. juncea var. longidens Bailey, B. juncea var. japonica Bailey, and B. juncea var. multisecta Bailey. B. juncea var. crispifolia with dissected and crisped lower leaves including B. juncea var. crispifolia Bailey, B. juncea var. subcrispifolia Sinsk, and B. juncea var. crispifolia Sinsk. In a recent publication, Dixon (2007) distinguished seven groups: 1. Hakarishina (B. juncea). Oilseed form of Indian subcontinent, central Asia and Europe 2. Nekarashina (var. napiformis) with enlarged roots 3. Hsueh li hung (var. foliosa) and Nagan sz kaai (var. japonica) with dissected leaves 4. Azanina (var. crispifolia) with dissected leaves and a general appearance of curly kale used for salads and as ornamentals in the United States 5. var. integrifolia with entire succulent leaves 6. var. rugosa, a large-size plant with leaves having flat entire midribs 7. Ta hsin tsai (var. bulbifolia) with plants having succulent stems Chinese researchers (Fu et al. 2006; Qi et al. 2007, 2008; Wu et al. 2009) describe variants following Gladis and Hammer (1992): leaf mustard (B. juncea var. multiceps), stem mustard (B. juncea var. tsatsai), root mustard (B. juncea var. megarrhiza), oilseed mustard (B. juncea var. juncea), and seed stalk mustard (B. juncea var. utilis) are the major representatives of this diversified crop (Plate 2.4). These forms are widely grown in most Southeast Asian countries; China is the leading country in terms of crop area. These forms are consumed as pickled

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leaves, stem and root, seed oil, and seed mustard. At present, oil forms are simply referred to as B. juncea Czern. while the Chinese variations are given the varietal rank as mentioned. 2. Origin and Domestication. Prain (1898), for the first time, proposed that B. juncea evolved in China and subsequently spread to India through a northeastern route. He substantiated his views by observing that a wild form of B. juncea, which he referred to as Sinapis patens, is common along this route. This view proved to be incorrect as S. patens is now identified as Nasturtium indicum (Hooker and Anderson 1872; Schulz 1919). Prain was later supported by Sinskaia (1928). She believed that East European B. juncea is also of Chinese origin from where it migrated naturally from the Kirgiz steppes, where it grows wild. She further speculated that most primitive forms have lyrate-pinnatisect leaves from which evolution occurred in three directions: (1) the East Asian forms with bipinnate leaves dissected into threadlike segments, (2) the Chinese forms with crisp leaves, and (3) nondivided leaves comprising the central Asian and Indian forms. Burkill (1930) and Sun (1970) did not agree with a Chinese origin for B. juncea; both suggested the Middle East as the place of origin. Sun (1970) argued that since parent species do not occur naturally in China, B. juncea had to be introduced from outside. Russian botanist Vavilov (1949) proposed Afghanistan and adjoining regions as its primary center of origin and central and western China, eastern India, and Asia Minor through Iran as the secondary centers. Cytogenetical, biochemical, and in recent years molecular evidence has suggested the polyphyletic origin at many places with a sympatric distribution of parental species (Olsson 1960a; Prakash 1973a; Vaughan 1977; Prakash and Hinata 1980; Song et al. 1988a) The region of Middle East (Fig. 2.6) has been favored strongly as the place of its origin by many researchers as both parental species grow wild in this region (Olsson 1960a; Mizushima and Tsunoda 1967). Wild forms of B. juncea can still be seen in the plateau of Asia Minor and adjoining southern Iran (Tsunoda and Nishi 1968; Tsunoda 1980). Regions of northwest India and southwest China constitute two important secondary centers for the domestication of B. juncea as they exhibit enormous variation. Sun et al. (2004), while studying variations in B. juncea, also suggested central China, mainly the Gansu and adjoining region, as the major center of diversity. Biochemical evidence for the existence of two different races was provided by studies of Vaughan et al. (1963) and Vaughan and Gordon (1973). The seeds of Chinese forms have a marked mucilagenous epidermis and produce allyl isothiocynate, while the

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Indian forms produce 3-butenyl isothiocynate. RFLP studies (Song et al. 1988a) provide support to this concept of two main centers of origin: the Middle East Indian region where mainly oil forms evolved and China where leafy types developed. 3. Indian Forms. The earliest record of B. juncea from India is the excavated seeds from the ancient sites of the Indus Valley civilization (ca. 2300–1500 BCE) in the present-day Sindh and Punjab states of Pakistan. Its inhabitants were mostly meat eaters who used mustard oil for cooking, food preservation, and body massage (Prakash 1961). When migrating Aryans came to northwest India around 1800 BCE, they learned to use B. juncea oil from the original inhabitants. Ancient Sanskrit literature of Aryans is replete with references of Brassica species. Rigveda, Atharvaveda, Chandogya Upanishad, and Brahmanas used several names, such as siddhartha, rajika, baja, sarshap, and svet sharshap (Hinata and Prakash 1984; Watt 1989). However, the use of oil was not very popular with the Aryans (Atharvaveda). In the period around 800–300 BCE, mustard seeds were used for food seasoning and mustard stalks were consumed as vegetables, as mentioned often in early Buddhist and Jain works, such as Jataka and Acharanga Sutra. In the same period, the Buddhist texts Bodhyan Grhya Sutra, Sankhyan Grhya Sutra, and Sankhyan Sautra Sutra mentioned the use of mustard oil for cooking. It is also mentioned in Buddhist canonical literature Dhammapada, Suttanipita, and Samyutta Nikaya. During 300 BCE to 75 CE, known as the Maurya and Sunga period, Kautilya (ca. 300 BCE), the author of famous Arthashastra, mentioned three types of mustard. Mustard seeds were used to add pungency (Kashyap Samhita, ca. 200 BCE). The medical treatise Charak Samhita (3rd century CE) mentioned the use of mustard oil in food preparation and also of mustard stalks as vegetables. The period from 300 to 750 was an era of great prosperity in India. During this time three famous Chinese travelers, Fahi-an, HuenTsang, and Itsing, came to India and provided an excellent record of Indian food habits. Mustard oil was in common use as a frying medium (Itsing in India 671–689; Huen Tsang in India 632–643). Itsing also mentioned two types of mustard—white and black— which were produced in large quantities, and their oil was used for cooking (Takakusu 1896). A Sanskrit book Sukraniti (1100) referred to mustard oil as a common medium for frying and cooking and mustard stalks as winter vegetables. It is evident that in a period of over 3,500 years, mustard came to occupy an important place in the Indian diet. The only seed remains of Brassica species excavated are of B. juncea. In spite of numerous references to brassicas in Sanskrit literature, the

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descriptions are not precise enough to identify the species. Watt (1889) interpreted rajika, Siddhartha, and svet sarshapa as referring to blackand brown-seeded B. juncea and white-seeded Sinapis alba, respectively. Similarly sarshap was used both for brown sarson and B. nigra (Watt 1889). Hinata and Prakash (1984) are of the view that sarshap denoted only brown sarson and siddhartha unmistakably indicated yellow sarson. The present-day Hindi word sarson is clearly a derivative from sarshap. Vedic Aryans used rajika for B. juncea and were unaware of B. nigra and Sinapis alba. All the available evidence indicates that B. juncea was under cultivation in the Indus Valley around 3000 BCE. The art of extracting oil was known to this civilization, with the oil being used for massage. Seeds of B. juncea have been excavated from Chanhu-daro, a site of this civilization (Allchin 1969). With the arrival of Aryans in northwest India around 1500 BCE, its oil was adopted first as a preservative and later for cooking and massage purposes. Subsequently around 1000 BCE, it spread eastward with the stream of migrating people. Its carbonized seeds have been recovered from Damoder River valley site in eastern India, ca. 1000 BCE (Ghosh et al. 2006) and, by ca. 700 CE, it became firmly established as an oil crop in the Indo-Gangetic plain of north India, as evident from the reports of Chinese travelers Huen Tsang (ca. 640) and Itsing (ca. 690). Conflicting views have been expressed regarding the route of its entry into India. Hinata and Prakash (1984) strongly believe that it entered into northwest India from the Middle East, the place of its origin, through Afghanistan between 4500–2300 BCE but not before that date. This is supported by the fact that an ancient Neolithic site of agriculture at Mehrgarh (7000–4700 BCE), in the area of Indus Valley civilization and on a historical route connecting it to west Asia through the Iranian Plateau, did not yield seeds of any Brassica species (Jarrige and Meadow 1980). Natural hybridizations between the parental species with a sympatric distribution in Aghanistan and adjoining region also originated new genetic stocks. However, Indian forms exclusively developed in the direction of oilseed types with lyrate pinnatisect leaves. Several factors, such as introgressive hybridization leading to incorporation of adaptive gene complexes, played vital roles in the further adaptation of Brassica species. A leafy form of B. juncea with large leaves and thick white fleshy stalks is cultivated as a vegetable in the foothills of the Himalayas from Kashmir in the west to Assam and Sikkim in the east. Roxburgh (1832) referred to it as Sinapis rugosa and S. cuneifolia. It is very similar to the Chinese leafy form and might have been brought by Buddhist monks who since ancient times frequently traveled the Himalayas and subsequently established this species in cooler climates.

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4. Chinese Forms. China has a long history of B. juncea cultivation (Wen 1980; Chen 1982). The southwest region exhibits enormous polymorphism in vegetable forms, as described earlier. The history of mustard utilization and domestication dates back 6000–7000 years (Liu 1996). Carbonized mustard seeds stored in a gallipot were excavated from the Banpo site in China in 1963, and carbon dating indicated that the seeds belonged to the New Stone Age, ca. 4800 BCE (Institute of Archaeology Report 1963). The earliest Chinese literature record of brassicas being used as vegetable appeared in Xiaxiaozhen (Ancient Almanac) in the Xia dynasty (ca. 3000 BCE) and Shijin-Gufeng (A Collection of Poems) in the Zhou dynasty literature (1122–247 BCE) (Wu et al. 2009). During the West Han dynasty (206 BCE–24 CE), its use had been recorded as a flavoring agent. Dai in his work Liji (The Book of Rites) referred to a ‘‘sliced jam of fish with mustard.’’ It was a popular crop in the first century CE, as frequent references are available in Tu-Bin-Jin-Cao (Illustated Book of Medicinal Herbs) by Su (10–61 CE). Chia-Ssu-hsieh’s book Ch’i-min-yao-shu of the late 5th or early 6th century described various uses of leaves and seeds (Li 1969). Wang (1576–1588) mentioned a root form in his work Gua Guo Shi (Explanations of Cucurbits and Vegetable Crops). During the Ming dynasty, a famous work by Li (1578) described many forms for their leaves and shoots. Wen (1980) presented a fascinating account of the origin of variations (Fig. 2.11). Based on ancient literature from the fifth century, he proposed that the primitive type was an annual plant with poor leaf growth and was cultivated for its pungent seeds. Subsequently, variants in leaf shape and heading forms were evolved and selected due to human intervention. During the Tang dynasty (607–907), broad-leaved forms were developed and used as greens in temperate and humid south China. A form with deeply dissected leaves adapted to arid regions was developed in northern China. It subsequently produced tillering forms that were more productive, branched early during vegetative growth, and were used for pickles. The Qing dynasty (1644–1911) witnessed the origin of types having leaves with broad, thick midribs and petioles. Later, headed forms with leaves with fleshy midribs and petioles evolved simultaneouly with forms having swollen stems. Fleshy root forms evolved independently from broad-leaved forms, most probably after the 12th century. In a recent study on these vegetable forms comprising accessions of all the diverse variations, Fu et al. (2006) employing RAPDs observed that these various accessions are not a homogenous group. Further, using sequence variations of ITS1, 5.8s rRNA, and ITS2, Qi et al. (2007) proposed their division into two clades, one having accessions close to Nigra lineage and other accessions closer to Rapa/Oleracea lineage.

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Fig. 2.11. Evolution of Chinese mustard crops: (a and b) primitive types; (c) var. oleifera; (d) var. rugosa; (e) var. napiformis; (f and g) var. crispifolia; (h and i) var. capitata, K1 and K2 var. tsa-tsai. (Source: Wen 1982).

These observations are in disagreement with earlier observations from cp, mitochondria, and nuclear DNA RFLPs (Wu et al. 2009). Another observation is that morphological and molecular classifications are incongruent as forms with similar phenotypes do not necessarily have closer relationships. These authors (Fu et al. 2006; Qi et al. 2007, 2008; Wu et al. 2009) also inferred that Chinese forms evolved separately from Indian forms, consistent with the earlier views of the existence of two races. Once some seed stocks were established, introgression from parental species B. nigra and B. rapa further differentiated these types mediated by human selection. There may be two possibilities for the origin of these variations: (1) different B. rapa leafy morphotypes hybridized with B. nigra, as amply demonstrated by obtaining B. juncea forms closely resembling the natural ones following artificial synthesis using various Chinese B. rapa parents (Prakash 1973a), and (2) mutations

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and/or nonhomologous recombination between A and B genome chromosomes. Such morphological variants closely resembling the natural forms were produced following the selfing of F1 interspecific hybrids B. rapa  B. nigra (Prakash 1973b). G. Brassica napus This crop came into cultivation only in the 15th century. Two forms are now in cultivation: (1) oilseed rape, widely grown for its edible oil in Canada, Europe, China and Australia, and (2) root-forming swede or rutabaga for food and fodder. Theophrastus and Dioscorides mentioned a root form as bounias, which was wrongly identified as swede in the 16th century (Henslow 1908). Zwinger (1696) described a form steckruebenkohl, which in all probability represents an early form of rutabaga. The rutabagas include two forms, one with white flesh and the other with yellow. The first description of the white one is by Bauhin in Prodromus (1620), and it is named again in his Pinax (1623), where it is called napobrassica. Tournefort (1700) mentioned it as Brassica radice napiformi, or chou-navet, in France while De Candolle (1821) described it as navet jaune, navet de Suede, chou de Laponie, and chou de Suede. Its earliest reference in Germany as Kohlrabi unter der Erden appeared in 1748. Subsequently until the early 20th century, it was recognized in several languages as the underground form of B. oleracea var. gongyloides. The Linnean concept of B. napus was a turnip with an elongated root. Usage of Brassica napus, originally named as Brassica napus rapifera Metzger (Metzger 1833), for rutabaga created enormous confusion and also an erroneous idea that it is an ancient species (Ahokas 2007). It became popular as fodder in Scandinavia and later in the 18th century spread to England (McNaughton and Thow 1972). An important staple food plant earlier, particularly during World War I, it is now mostly grown for forage. It must have originated as a consequece of hybridization between turnip and some forms of B. oleracea in farmers’ fields. Such root-forming morphotypes were obtained from crosses between turnips and different B. oleracea forms (Olsson et al. 1955; Kato et al. 1968). The first reference of oil forms occurs in the Cruydt Boek of Dodonaeus (1554), where slooren is mentioned as being grown for seed oil (Toxopeus 1979). It was most likely to be an early form of winter rape and came into cultivation in the early 17th century (Baur 1944). Its oil, known as raepolie, was first used for illumination and later as an edible oil and for soap making. Spring forms were developed in the late 17th or early 18th century as a selection from winter forms suitable for locales

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where winter is not too severe. At present, in some European countries and in China, winter forms are cultivated. In Canada, northern Europe, and Australia, only spring forms are grown. The oil form of B. napus does not occur in the wild. Sinskaia (1928) and Schiemann (1932) proposed the southwest Mediterranean region as the place of origin where the constituent parents overlap in natural distribution. However, this overlapping probably did not exist (Tsunoda 1980). As Go´mez-Campo and Prakash (1999) observed, wild B. rapa is very poorly represented in Spain. Thus, it is difficult to envisage its arrival at Atlantic maritime cliffs where B. oleracea grows wild. These authors believed that it originated outside the Mediterranean region. Several researchers suggested its multiple origins in an agricultural environment (Olsson 1960b; Prakash and Hinata 1980). This has been substantiated by investigations based on organelle and nuclear RFLP analyses (Song and Osborn 1992). A study by Song et al. (1988a) identified B. rapa ‘‘spring broccoli raab’’ as the closest extant relative of maternal genome of B. napus.However, as stated earlier, the maternal donor of B. napus has not been unequivocably established. The plastid genome of B. napus shows considerable variability, suggesting its polyphyletic origin (Allender and King 2010). An introgression of genetic information from B. rapa, one of its constituent parents, has also played a major role in developing an array of cultivars (Aru´s et al. 1987; Aguinagalde 1988). Large-scale natural hybridizations between both the constituent parents have been recorded in fields; such hybridizations have contributed to the increase in B. napus variability (Bing et al. 1996). One of the most striking aspects of oilseed B. napus is that in a brief span of 400 years since its origin, its distribution, cultivation and production has far exceeded other oilseed brassicas. This change started in early 1980s. Busch et al. (1994) have documented an account of its introduction into Canada and development of canola-quality rapeseed. Spring forms of B. napus were introduced before World War II; the oil was first used as a marine lubricant during the war. Later in the 1950s, attention was paid to use it for human consumption. However, the presence of erucic acid (cis-13-docosenoic acid, 22:1, n-9) in oil and glucosinolates in meal prevented its adoption. Low–erucic acid cultivars were soon developed by Downey and Harvey (1963), followed by the world’s first zero-erucic and low-glucosinolate cultivar ‘Tower’ (Bell 1982). During the last 25 years, many high-yielding canola-quality conventional and hybrid cultivars have been bred and released in Canada, Australia, Europe, and China. The term canola is a special one and was coined and defined as seed, oil, and meal that contain <1% of the total fatty acid as erucic acid and <18 m mol of aliphatic glucosinolates

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per gram of oil-free meal (Consumer and Corporate Affairs, 1986). Although first used in Canada, this term is now internationally accepted. Herbicide-resistant cultivars, both transgenic and conventional, are widely grown. Yellow-seeded forms with higher oil and lower fiber are also under development, and cultivars producing low-linolenic and high-oleic canola oil now make up about 15% of the Canadian sown crop area. Rapeseed/canola oil is not only a nutrionally desirable edible oil but also has impotant industrial applications as a lubricant, a slip agent in plastics manufacture, bioplastic production, tensides for detergents and soap production, biodegradable plastic, and biofuel. Brassica napus entered into China around 1940. Available records show that Professor Jin-Rang Yu of Zhejiang University introduced it from Korea in the early of 1930s. In 1941, his colleague, Professor Feng-Ji Sun, introduced European accessions from Britain. An introduced Japanese cultivar ‘Sheng Li You Cai’ became very popoular between 1955 and 1979 in the Yangtze Valley. Subsequently, efforts to breed new cultivars with high yield and short duration have been carried out in many breeding organizations, resulting in the release of several new ones, including ‘Zhongyou 821’, which exhibits high yields with strong Sclerotinia rot resistance, abiotic stress resistance, and wide adaptability in the main rapeseed production area (Yangtze Valley).With the discovery of Polima cytoplasmic male sterility (CMS) in 1972 by Fu Ting Dong in Huzhong Agricultural University, sound foundations were laid to develop 3-line hybrids. At present, the major emphasis is on developing hybrids with canola. Attempts were made to cultivate B. napus in India around 1975 by S. Prakash through the introduction of exotic accessions from Canada and Europe. However, due to very late flowering and extremely poor seed set, the attempts were unsuccessful. Artificial synthetics were also obtained using very diverse constituent parents (Prakash and Raut 1983). At present, its cultivation is confined to a very limited area primarily due pod shattering and poor adaptability to dry conditions.

IV. CONCLUDING REMARKS Brassica is a unique genus that gave rise to crops that provide edible oil, vegetables, and condiments. Displaying high polymorphism in three species, B. rapa, B. oleracea, and B. juncea, the brassicas represent a classic example of structural evolution. In this review, we have collated information from various sources to unravel the constitution of ancestral karyotypes of the Brassicaceae and subsequently the evolution of derived diploid genomes. Also, we have attempted to shed light on the

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possible domestication events and centers. Often, the views expressed in the past were hypothetical and conjectural, requiring further evidence to corroborate them. During the last 25 years, significant advances have been made in understanding genome organization and evolution using an array of molecular markers. Genome sequencing in the model Crucifer species Arabidopsis has greatly helped in such researches. Several investigations, based on comparative mapping, provided compelling evidence that Brassica genomes have evolved through whole-genome triplication from an ancestral karyotype with n ¼ 4 chromosomes leading to a hexaplod genome with 2n ¼ 6x ¼ 24. Further, the three basic genomes of Brassica are considered to have originated from this hexaploid following reduction in chromosome number. However, there is no consensus on this view. Alternatively, it is suggested that two duplication events resulted in a tetraploid genome (2n ¼ 4x ¼ 16) from whence the diploid genomes evolved after the insertion of transposable elements, segmental duplications, and chromosome rearrangements. The classic cytogenetical view is that the Brassica ancestral genome had 6 chromosomes and through selective chromosome duplication originated the 3 diploid genomes. However, all these hypotheses are not firmly established and need further evidence to identify the precise mechanisms involved in the Brassiceae karyotype evolution. It is hoped that a correct secenerio will emerge in the near future. Ancient Indian, Chinese, Greek, and Roman literature is extremely rich in testifying the antiquity of brassica crops. Possible domestication centers have been identified based on linguistic, literary, historical, genetic, and molecular evidence. It appears that Brassica first entered into domestication as a vegetable, and its use as an edible oilseed crop was a later development. The illustrated herbals of the Renaissance are valuable sources of information on the presumed medicinal properties of the brassicas, extracted from the knowledge contained in the ancient writings of Greek, Roman, Byzantine, and Arab scientists. Such herbals were among the first to be printed after the introduction of printing in Europe around 1450. The illustrations were made by wood engravings and in some case are hand tinted. However, information from ancient Asian sources, particularly China and India, has been generally ignored in the West. With the expansion of Asian science, this deficiency is being corrected. Identifying the wild progenitors is an important requirement to understand the process of domestication. Despite rapid advancements in cytology, we do not know precisely what wild species were the ancestors of these crops. Molecular information can be of considerable help in tracing the ancestry, phylogeny, and relationships with wild

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species. It often provides critical support to findings based on morphology and cytology as well as linguistic and historic studies. A combination of these sources can pinpoint the place of initial domestication and subsequent radiation. In recent years, specific domestication genes associated with evolution of new characters have been identified. For example, the BoCAL gene is involved in developing unusual inflorescence morphology in cauliflower and broccoli. Similarly, FRUITFUL controls pod-shattering trait. It appears that such transcriptional regulators played a crucial role in domestication. Superdomestication, the term used by Vaughan et al. (2007), refers to improving the present forms or developing new forms with substantial yield increases and incorporation of traits conferring agronomic advantages through the use of modern genetics and biotechnology. These new approaches include genome manipulation, chromosome engineering, and transgenic technology. During last 30 years, progress in tissue culture and somatic cell hybridization techniques has helped to overcome cross-incompatibility barriers, thus facilitating introgression of desirable cytoplasmic and nuclear genes from related wild species even across tribes.Thus, changing crops to C3–C4 intermediate photosynthesis (Ueno et al. 2007), alteration in oil and meal quality (Scarth and Tang 2006), and incorporation of resistance to silique shattering (Østergaard 2006) are examples of superdomestication. Similarly, exploitation of heterosis either through hybrid technology or through increased allelic diversity, following genome manipulations (Prakash et al. 2009), constitutes superdomestication. With all the tools available, modern plant breeding has the potential to further modify these crops in order to realize higher yields and better nutritional quality. One of the amazing features of the brassicas is that crop evolution is still under way, providing insight into the process of domestication in action. During the last 40 years, new oilseeds called low-erucic acid B. napus and B. rapa cultivars were developed and are now known as canola (Canadian oil). Canola has become important in Canada, China, Australia, and the United States with world production reaching 48.5 million tonnes. Canola is now the world’s third largest source of vegetable oil (13%), after soybean (32%) and palm oil (28%). One of the spectacular achievements in Brassica research concerns the genetic improvement in nutritional quality of oil and meal, primarily in B. napus, and subsequently in other species, a classic example of plant breeding. The development of canola as a crop can be credited to the pioneering activity of Canadian Brassica breeders R. K. Downey (Rakow 2000) and B. R. Stefansson (Bell 1982). Japanese researchers in

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the last 50 years have synthesized several new fodder and vegetable types of B. napus using leafy and root-forming types of B. rapa (ssp. chinensis, pekinensis, narinosa, nipposinica, and rapa). Among these are a fodder rape ‘CO’, which has vigorous growth and winter hardiness (Hosoda 1950). A novel, synthetic head-forming vegetable form, designated as ‘Hakuran’, was obtained from the cross B. oleracea var. capitata  B. rapa ssp. pekinensis. It is very popular because it is less fibrous and has soft leaves and high degree of resistance to soft rot (Shinohara and Kanno 1961; Takeda 1986). A similar type has also been produced using the same parents through protoplast fusion (Taguchi and Kameya 1986). New vegetable types of cauliflower with green (broccoflower) and purple heads are now in the market, along with Romanesco broccoli, characterized by striking and unusul fractal patterns. The Chinese brassicas, such as pak-choi, are increasingly produced in the West. We can expect many more permutations of the brassica genome to produce new and improved crops through the wonders of plant breeding and genetic manipulation. Collaborative research integrating genetics, molecular biology, archaeology, geography as well as literary and historical sources hold promise to decipher and reconstuct the precise domestication events of Brassica crops.

ACKNOWLEDGMENTS This manuscript is dedicated the memory of Dr. Shyman Prakash (born October 15, 1941), distinguished cytogeneticist, colleague, and friend who died August 14, 2010, just after completing the final manuscript of this chapter. He will be missed. Before he passed away, he dedicated the review to the memory of the late Professor C
esar Gomez-Campo, Universidad Politecnica de Madrid, Ciudad Universitaria, Madrid, Spain, who made significant contributions to taxonomy and phylogenetics of Brassicaceae. We are grateful to Professor Jules Janick, Purdue University, USA, for providing valuable literature and critical review of the text. We express our sincere gratitude to R. K. Downey, G. E. Dixon, K. Hinata, W. K. Heneen, and M. W. Farnham for their valuable comments on this chapter. We thank Lorenzo Maggioni, Bioversity International, Rome, Italy; A. Ahokas, MTT-Agrifood Res. Finland for providing articles; Yongju Huang, Rothamsted Research Station, Fang-chin Chen, AVRDC, and Li Xixiang, Institute for Vegetable and Flowers, CAAS, for providing pictures. Shyam Prakash acknowledges the Indian National Science Academy for financial support in the form of a senior scientist position.

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3 Melon Landraces of India: Contributions and Importance Narinder P. S. Dhillon
Department of Vegetable Crops Punjab Agricultural University Ludhiana 141 004, India Antonio J. Monforte Instituto de Biolog
ıa Molecular y Celular de Plantas (IBMCP) Universidad Politecnica de Valencia–Consejo Superior de Investigaciones Cientificas Ciudad Polit
ecnica de la Innovacio´n Edificio 8E, Ingenierio Fausto Elio s/n. 46022 Valencia, Spain Michel Pitrat Institut National de la Recherche Agronomique (INRA), UR1052 G
en
etique et Am
elioration des Fruits et L
egumes, BP 94 F-84143 Montfavet Cedex, France Sudhakar Pandey Indian Institute of Vegetable Research P.B. No. 01, PO—Jakhini (Shahanshahpur) Varanasi 221 305, India Praveen Kumar Singh Indian Institute of Vegetable Research Regional Station, Sargatia Kushinagar 274 406, UP, India
Current address: AVRDC-The World Vegetable Center, East and Southeast Asia, PO Box 1010 (Kasetsart), Bangkok 10903, Thailand

Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick.
2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 85

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Kathleen R. Reitsma U.S. Department of Agriculture Agricultural Research Service North Central Regional Plant Introduction Station Iowa State University Ames, Iowa 50011-1170 USA Jordi Garcia-Mas Institut de Recerca i Tecnologia Agroalimentaries Centre for Research in Agricultural Genomics Ctra de Cabrils Km 2 E-08348 Cabrils, Spain Abhishek Sharma Department of Vegetable Crops Punjab Agricultural University Ludhiana 141 004, India James D. McCreight U.S. Department of Agriculture Agricultural Research Service U.S. Agricultural Research Station 1636 East Alisal Street Salinas, California 93905, USA

ABSTRACT Indian melon (Cucumis melo L.) landraces comprise a wealth of genetic diversity that has been exploited over the millennia by farmers and over the last century by scientifically trained plant scientists in the public and private sectors. Melons in India may be feral or cultivated, have netted or smooth rinds, be sweet and eaten as a dessert fruit or not sweet and consumed as a vegetable fresh, cooked, or dried. The fruit may be processed for sweet juice and confectionary flavoring, and the seeds are a source of high-quality cooking oil and high-protein seed meal. This chapter reviews genetic variation for resistance to fungal, bacterial, and viral diseases and to nematodes and insects; and tolerance to soil salinity, drought, flooding, and high temperatures with a focus on melon accessions of Indian origins. Some of these resistances have knowing or unknowingly been transferred through scientifically based breeding programs into open-pollinated and hybrid sweet melon cultivars grown in Africa, Asia, Australia, Europe, and the Americas for domestic and export markets. Indian melons include unique sources of high acidity and sugar:acid ratio that enable breeding for new

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combinations of sweet and sour flavors for fresh and processed melon products. Genetic variation in carotenoids (b-carotene), ascorbic acid, and micronutrient (Fe and Zn) contents in Indian germplasm promise more nutritious melons. High percentages of unique alleles are present in southern (24.2%) and eastern (30.4%) Indian landraces and in ‘‘wild’’ accessions from northern India (34.5%). Extensive collection, preservation, and evaluation of Indian melon landraces is vital to prevent further genetic erosion in this primary center of melon diversity, to increase genetic variability for melon breeding, and to introduce new traits into modern melon cultivars. International collaborations are developing genomics tools for melon that will facilitate allele mining within Indian germplasm and introduce new genetic variability. We are on the verge of an exciting era of melon genetic improvement as whole-plant breeding and genomics technologies combine to preserve and fully characterize the complete array of genetic variability in melon and exploit that germplasm and information for the further improvement of salad and dessert melons for diverse markets worldwide. KEYWORDS: breeding; Cucumis melo; flavor; genetics; host plant resistance; molecular markers; phytonutrient I. INTRODUCTION II. FIRST CONTRIBUTION OF INDIAN MELON GERMPLASM TO THE U.S. MELON BREEDING PROGRAMS III. USEFUL TRAITS FROM INDIAN MELONS A. Fungal Disease Resistance B. Virus Resistance C. Root-knot Nematode and Insect Resistance D. Resistance to Insect Transmission of Viruses E. Flavor Improvement F. Vitamin and Mineral Content G. Seedling, Vegetative, Flower, and Fruit Traits and Isozymes IV. GENETIC DIVERSITY V. MELON BREEDING A. Development of Improved Salad Melons B. Melons with Stable Yield and Consistent Sweetness C. Tailoring of ‘‘Climate-Ready’’ Melons D. Molecular Markers VI. FUTURE ROLE OF INDIAN MELON GERMPLASM AND CONCLUSIONS ACKNOWLEDGMENTS LITERATURE CITED

We are not really much interested in conserving the old varieties as varieties; it is the genes we are concerned about. The older landraces can be considered as populations of genes and genetic variability is absolutely essential for further improvement. In fact, variability is absolutely essential to even hold onto what we already have. Harlan (1972)

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I. INTRODUCTION Melon (Cucumis melo L.; 2n ¼ 2x ¼ 24) is a tropical Old World species, and its exact geographical origin is still in dispute. Most taxonomists have suggested Africa as the region of domestication of melon (Whitaker and Davis 1962; Kirkbride 1993). This idea was supported by the fact that wild African Cucumis spp. had the same, or multiple, chromosome number as C. melo whereas C. sativus, with a clear Asian origin, has a chromosome number of 2n ¼ 14. Moreover, the South African wild species C. sagittatus has been proposed as the phylogenetically closest relative of melon (Ghebretinsae et al. 2007). Recent research, however, strongly supports an Asian origin (Renner et al. 2007; Schaefer et al. 2009; Sebastian et al. 2010), and the closest wild species, C. picrocarpus, has been found in Australia (Sebastian et al. 2010). Domestication of melon is also disputed. Melon may have been first domesticated as a food source in Egypt and Iran during the second and third millennia BCE, respectively (Keimer 1924; Stol 1987; Janick et al. 2007), although some researchers suggest that India is the center of domestication, with the earliest remains date to between 2300 and 1600 BCE at the Indus Valley site of Harappa (Vishnu-Mittre 1974). EsquinasAlcazar and Gulick (1983) suggested that domestication of melon may have occurred independently in Southeast Asia, India, and East Asia and identified a broad primary center of diversity in southwest and central Asia that included north and central India as well as Turkey, Syria, Iran, Transcaucasia, Afghanistan, Turkmenistan, Tadjikistan, and Uzebekistan. In their view China, Korea and the Iberian Peninsula are secondary centers of melon diversity. Melon was cultivated in the Roman Empire (Janick et al. 2007). In China, melon is mentioned several times in a book written before 500 BCE (Keng 1974). Melons were brought to the New World by Columbus (Robinson and Decker-Walters 1997). The world production of melons in 2008 was estimated at 27.7 million t from 1.3 million ha of land and is a 60% increase in production from 36% more land in 1998 (FAO 2010). China is the dominant producer of melons with nearly 45% of the production from 51.8% of the area harvested (Table 3.1). Nineteen countries accounted for 87.2% of the total production and 90% of the area harvested; another 70 countries accounted for 12.8% of the world total production and 9.9% of the area harvested. None of the other countries exceeded 10% of the total world melon production or area harvested. Yield (t per ha) range from 6.32 in Panama to 33.44 in Morocco. Melons in India may be feral or cultivated, have netted or smooth rinds, be sweet and eaten as a dessert fruit or not sweet and consumed as

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Table 3.1. Melon production, area and yield per hectare in 2008 of countries that produce 1% of the world’s total melon production. Area harvested Country Bangladesh Brazil China Egypt France Guatemala India Iran Iraq Italy Kazakhstan Mexico Morocco Pakistan Panama Spain Turkey Ukraine U.S.A. World

Production z

(ha)

(%)

12,545 15,746 570,874 31,255 14,747 18,900 31,500 80,000 21,000 28,199 15,600 24,011 23,432 18,626 17,500 33,388 105,000 19,400 35,990 1,281,318

1.0 1.2 44.6 2.4 1.2 1.5 2.5 6.2 1.6 2.2 1.2 1.9 1.8 1.5 1.4 2.6 8.2 1.5 2.8 –

(t)

(%)z

Mean yield (t/ha)

204,593 340,464 14,322,480 757,677 265,576 445,035 645,000 1,230,000 205,852 653,309 215,750 582,288 736,800 274,664 110,586 1,021,800 1,749,935 97,000 1,042,530 27,637,248

0.7 1.2 51.8 2.7 1.0 1.6 2.3 4.4 0.7 2.4 0.8 2.1 2.7 1.0 0.4 3.7 6.3 0.4 3.8 –

16.31 21.62 25.09 24.24 18.01 23.55 20.48 15.38 9.80 23.17 13.83 24.25 31.44 14.75 6.32 30.60 16.67 5.00 28.97 21.57

z

Percent of total world production or area harvested. Source: FAO 2010.

a vegetable fresh, cooked, or dried. The fruit may be processed for sweet juice and confectionary flavoring, and the seeds are a source of highquality cooking oil and high protein seed meal. India’s mean yield per hectare is nearly equal with the world mean (Table 3.1). This is remarkable because in many areas, such as Rajasthan, melons are grown with no inputs (supplemental irrigation, fertilizer, pesticides). It may be due in part to the widespread popularity of nondessert (nonsweet) or vegetable melons where a larger proportion of the potential fruit yield is harvested than is the case with dessert (sweet) melons, which in addition to sweetness must have acceptable external appearance (e.g., shape, rind color, pattern, and netting), interior (e.g., cavity size, mesocarp thickness), and flesh (e.g., texture, flavor, aroma, and color) characteristics, and in many cases long shelf life for distance transport. Discussions with knowledgeable persons in the Indian vegetable industry suggest, based on 2009 seed sales of hybrid and open-pollinated varieties of melons, that India grows melons on

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125,000 ha and yields range from 20 to 25 t per ha (N. P. S. Dhillon, pers. commun.). Melon subspecies classification has been confusing and controversial. This may be due in part to the classification by various scientists of incomplete collections of germplasm and in part to philosophical differences among them (Jeffrey 1990). This morphologically diverse species was divided on the basis of ovary pubescence by Jeffrey (1980) and Kirkbride (1993) into two subspecies: C. melo subsp. agrestis (with appressed hairs on the youngest fruits) and C. melo subsp. melo (with spreading hairs on the youngest fruits). According to the International Code of Nomenclature for Cultivated Plants (Brickell et al. 2009), the term Group (for cultivar group) should be used under the subspecies level. In this chapter we use the term varietas (var.) (Spooner et al. 2003), reserving the word cultigroup for a lower taxonomic rank: for instance, within the var. inodorus, the Piel de Sapo, Tendral, and Yuva cultigroups can be defined. Munger and Robinson (1991) proposed six varietas encompassing cultivated and ‘‘wild’’ types that simplified the scheme described by Whitaker and Davis (1962), which was a condensation of previous classifications. The Munger and Robinson scheme came into use by many following publication of a monograph by Robinson and Decker-Walters (1997). From a thorough review of the literature and live plant materials, Pitrat et al. (2000) proposed a scheme consisting of two subspecies with 16 varietas. Recently Pitrat (2008) refined the previous proposal and reduced this number to 15, 5 in subspecies agrestis and 10 in subspecies melo. In this chapter, we describe the importance of diversity present in nonsweet (nondessert) melons of Indian origin (Plate. 3.1) with emphasis on subsp. agrestis var. momordica (snapmelon) and acidulus, but also mention subsp. melo var. flexuosus (see Stepansky et al. 1999a and Burger et al. 2010 for additional examples of fruit of the melon groups).

II. FIRST CONTRIBUTION OF INDIAN MELON GERMPLASM TO THE U.S. MELON BREEDING PROGRAMS Powdery mildew appeared on epidemic scale in the melon fields of the arid valleys of southwest California in 1925 and caused enormous losses to melon growers for several years. In February 1929, Professor J. T. Rosa of the University of California, Davis, received a shipment of melon seed collected from the Kathiawar region of Gujarat (Fig. 3.1), India, from one of his former students, Mr. D. N. Mahta, Second Economic Botanist, Nagpur, Central Provinces of India (Whitaker 1979; Swarup 2000.

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Fig. 3.1. Heterogeneous Indian melon landrace with snapmelon components evidenced by the longitudinal cracks in three of the middle fruits. Two fruits of ‘Hale’s Best’ cantaloupe on the left for comparison. (Source: Pryor et al. 1946.)

From this germplasm, Rosa and Ivan C. Jagger, U.S. Department of Agriculture, Agricultural Research Service (USDA, ARS) (working in Chula Vista and Brawley, California) found one snapmelon accession designated California 525 (Pryor et al. 1946) with field resistance to powdery mildew in the Imperial Valley that was conditioned by a single, dominant gene, Pm-1 (Jagger et al. 1938). California 525 was crossed with ‘Hale’s Best’. Backcrossing resistant F2 plants to ‘Hale’s Best’ followed by selfing and selection for resistance in the field for two generations led to the development of the first powdery mildew–resistant line ‘PMR 50’ in 1932 (Whitaker and Jagger 1937; Pryor et al. 1946). Four additional generations of selfing and selection resulted in the famous ‘PMR 45’, which was more uniform and of superior fruit quality (Jagger and Scott 1937). Besides possessing field resistance to the race 1 of powdery mildew, ‘PMR 45’ was adapted to the relatively saline soils and high temperatures of the inland valleys of southwest California. Evidently, Calif. 525, the donor parent for powdery mildew resistance, had the genes for salinity and high-temperature tolerance, as it originated from the coastal, arid zone of Gujarat Province in west India. The release of ‘PMR 45’ rejuvenated the melon industry of California. It was a major relief to the growers and consumers, and the crop was grown commercially for about 50 years after its release. The present-day melon cultivars resistant to Podosphaera xanthii (Castagne) Braun & Shishkoff (formerly

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Sphaerotheca fuliginea) race 1 owe their origin to this genetic stock (McCreight 2004). Unfortunately, this historic landrace, Calif. 525, is not currently available in the U.S. Department of Agriculture National Plant Germplasm System (USNPGS). Obviously, Indian snapmelon germplasm with all sorts of undesirable fruit traits was responsible for the reemergence of a stable and genetically improved melon industry in the United States. In 1938, a new P. xanthii race, race 2, became widespread in Imperial Valley (Jagger et al. 1938). Resistance to this new race was found in the snapmelon cv. Piria brought from India to the United States in 1929 and designated PI 79376 (Pryor et al. 1946). This resistance was combined with resistance to P. xanthii race 1 in ‘PMR 5’ and ‘PMR 6’, released in 1942, and ‘Campo’ and ‘Jacumba’, released in 1964 in the United States (Bohn et al. 1965). Indian powdery mildew–resistant snapmelons PI 124111 and PI 124112 were also resistant to downy mildew incited by Pseudoperonospora cubensis (Berk. & Curtis) Rosteoyzey and were exploited to develop mildew-resistant cultivars in the United States: ‘Georgia 47’ (Anon. 1954), ‘Home Garden’ (Ivanoff 1957), ‘Gulf Stream’ and ‘Planter’s Jumbo’ (Nugent 1994), ‘Mainstream’ (Nugent et al. 1979), and, recently, ‘Chujuc’ (Crosby et al. 2008). PI 164343, collected in Maharashtra, India (local name phoot in Hindi and phut in Punjabi) also contributed to the pedigree of ‘Mainstream’, which is resistant to powdery mildew, downy mildew and cucumber beetles [Acalymma trivittatum (Mannerheim), Diabrotica undecimpunctata undecimpunctata (Mannerheim)] and Diabrotica balteata LeConte (Nugent et al. 1979; USDA, ARS 2010b). Evidently, all the successful commercial diseaseand pest-resistant muskmelon cultivars grown today in the United States have Indian melon germplasm in their pedigrees.

III. USEFUL TRAITS FROM INDIAN MELONS Three main types of nonsweet melons are cultivated in India and belong to the flexuosus, acidulus, and momordica varietas. The var. flexuosus is cultivated from the Mediterranean basin to the Middle East, Afghanistan, and India, while the var. acidulus and momordica are endemic to India. The var. flexuosus group is characterized by long to very long fruits, up to 1.8 m. Fruit skin can be light or dark green, or striped, dark and light green as well, and the fruit surface can be wrinkled, furrowed and lobed, or smooth with ribs. In India, these fruits are usually light green with a wrinkled surface and are known as kakri or tar. The var. acidulus, which is cultivated mainly in south India and known as velleri,

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has oval (elliptic) fruits with very firm, crisp, white, slightly acidic flesh and a smooth epidermis with bright (yellow, orange, green) stripes or spots. Fruit of var. momordica melons, named phut, have a very thin epidermis, mealy flesh, and crack at maturity. A fourth group is formed by ‘‘wild’’ or semidomesticated melons known in India as Chibber or Ra Chibber or Kachri. Their mature fruits are cooked with various vegetable preparations and used for chutneys, pickles, and salad, and dehydrated fruits are sold in the market. The four varietas are usually monoecious. Indian melon landraces extend across numerous ecological niches, including arid to humid tropical environments. Indian melon landraces known to be resistant to various diseases, insects, nematodes, and abiotic stresses (Table 3.2), have been collected in many parts of the country but most notably in the arid northwest (Fig. 3.2). Traditional melon production systems in India may be generally characterized by no or low inputs (e.g., fertilizer, pesticides, and supplemental irrigation). Indian melons possess a wide array of adaptive traits, or genes and gene combinations, some of which may be missing in current open-pollinated and F1 hybrid melon cultivars, which have been selected for high yield, and specific and uniform fruit qualities in intensive production systems where specific inputs (high quality seed, irrigation, fertilizer, and pesticides) are optimized for maximum profits. Plant breeders agree that a huge amount of untapped genetic diversity within crop species exists in landraces and wild species as a result of domestication (Tanksley and McCouch 1997; Zamir 2001; McCouch 2004). These plant genetic resources are potential source of novel alleles that can be exploited for the improvement of tolerance to biotic and abiotic stresses, yield, and other quantitative traits. For example, Gur and Zamir (2004) introduced three quantitative trait loci (QTLs) from the wild species Solanum pennellii into a tomato cultivar obtaining a tomato yield more than 50% higher than that of a control market leader. Following are some examples of valuable Indian melon landraces and chibber accessions. Table 3.2 presents a more complete listing of Indian melon germplasm resistant to various diseases/pests and abiotic stresses. A. Fungal Disease Resistance Powdery mildew is a serious foliar disease of melon worldwide (Sitterly 1978). The two main causal organisms of the disease commonly reported are Golovinomyces cichoracearum (DC) V.P. Heluta (formerly Erysiphe cichoracearum) and P. xanthii (Braun et al. 2002). Evidence has shown that P. xanthii is predominant in most countries (Vakalounakis et al. 1994; Mohamed et al. 1995) and G. cichoracearum is able to cause

94

Monosporascus cannonballus Powdery mildew

Fusarium wilt

PI 414723 ‘‘wild’’ melonz Calif. 525, PI 79374, PI 79376, PI 115908, PI 115935 PI 134192, PI 134197, PI 134198, PI 134199, PI 134200 ‘Arka Rajhans’

5-4-2-1 55-1, 55-2, 77, 113,114 IC 267353, IC 274029, KP-7, B-159 PI 124111F, MR-1

PI 180280 PI 414723

PI 124112

MR-1 Annamali, Buduma Type-1, Buduma Type-2, Buduma Type-3, Ex-2, Phoontee, Goomuk, Nakkddosa, PPD-MR4 (= PPDMR-4 below?), LC-8, LR-1 (‘‘wild’’ melon) PPDMR-4 (= PPD-MR4 above?), PPDMR-35, W1, W3, W4, W5, W6 (= W1, W3, W4, W5, and W6 developed by Thomas and Webb 1981?) PI 124111, MR-1, PI 124111F

Accession

Nath and Dutta 1969

Cohen et al. 1985 Cohen and Eyal 1987 Epinat and Pitrat 1989 Kenigsbuch and Cohen 1992 Thomas et al. 1998 More 2002 Perchepied et al. 2005 Sitterly 1972 1973 Cohen and Eyal 1987 Epinat and Pitrat 1989 Thomas et al. 1998 More 2002 Perchepied et al. 2005 Palti and Cohen 1980 Epinat and Pitrat 1989 Perchepied et al. 2005 Angelov and Krastera 2000 More 2002 Dhillon et al. 2007 Pandey et al. 2008 Cohen and Eyal 1987 Zink and Thomas 1990 Brotman et al. 2005 Dhillon unpublished Pryor et al. 1946

Jhooty and Bains 1983 Bains and Parkash. 1985

Thomas et al. 1990 Sambandam et al. 1979

Reference

Sources of resistance to fungal and viral diseases and abiotic stresses, and fruit quality traits in nondessert-type Indian melons.

Fungal disease resistance Alternaria cucumerina Downy mildew

Trait

Table 3.2.

95

Zucchini yellow mosaic virus

AM 87 IC 274007, IC 274014

PI 414723

Squash mosaic virus Watermelon chlorotic stunt virus Watermelon mosaic virus

PI 180280 PI 124112

PI 371795 (= PI 414723) PI 313970 WMR 29 (PI 180280) 50 landraces lines from two states in southern India: Kerala and Tamil Nadu PI 180283

IC 274014, SM 67, SM 72, SM 73, SM 82 AM 25, AM 82 Phoot, Kachri, FM-1 and FM-5 (resistant); Harela and Chittidar (medium resistant VRM 5-10 (DVRM-1), VRM 29-1, VRM 31-1-2 (DVRM-2), VRM 42-4 and VRM 43-6 PI 124112, PI 124440, PI 414723, 90625 (= PI 313970), ‘Faizabadi Phoont’ PI 124111, PI 124112, PI 17990, PI 313970, PI 414723 Ames 20203, PI 313970, PI 614185, PI 614213

IC 267360, IC 267363, IC 267374, IC 267384, IC 274006 IC 274007, IC 274010, IC 274011, IC 274013 AM 4, AM 25, AM 27, AM 70, AM 78, AM 100 AM 7, AM 29, AM 48 PI 124112, PI 414723, 90625 (= PI 313970) PI 371795, PI 414723, PI 182938

Papaya ringspot virus

Kyuri green mottle mosaic virus Lettuce infectious yellows virus Moroccan watermelon mosaic virus

Cucurbit leaf crumple virus Cucurbit yellow stunting disorder virus

Cucurbit aphid borne yellow virus

Cucumber green mottle mosaic virus

Viral disease resistance Cucumber mosaic virus

PI 164343 PI 371795, PI 414723

PI 124111, MR-1, PI 124112, PI 179901 PI 313970, 90625 (= PI 313970)

Fergany et al. 2010 Fergany et al. 2010 Yousif et al. 2007 Munger 1991 Gilbert et al. 1994 Pitrat and Lecoq 1984 Danin-Poleg et al. 1997 Fergany et al. 2010 Dhillon et al. 2007 (continued)

Kaan 1973 Pitrat and Lecoq 1983 Webb 1979 McCreight and Fashing-Burdette 1996 Dhillon et al. 2007

McCreight et al. 2008 McCreight and Wintermantel 2008 Daryono et al. 2005 McCreight 2000 Lecoq et al. 1998 Fergany et al. 2010

Dogimont et al. 1997

More et al. 1993

Dhillon et al. 2009 Fergany et al. 2010 Rajamony et al. 1990

Pitrat et al. 1998 McCreight 2003, 2006 Pitrat and Besombes 2008 USDA 2010b McCreight 2006

96

z

formerly Cucumis callosus

High ascorbic acid High Fe and Zn content of fruit flesh High P and K content of fruit flesh

High carotenoids

Fruit quality High acidity of fruit flesh

Abiotic stress tolerance Drought Salt and high temperature

Tetranychus cinnaharinus Tetranychus urticae

Meloidogyne incognita

Daucus cucurbitae Bemisia tabaci Diaphania hyalinata Liriomyza sativae

Aulacophora foveicollis

Aphis gossypii

Insect and nematode resistance Cucumber beetle

Trait

Table 3.2 (Continued)

SM 43, SM 45 AM 79 WM 62 SP 3 AM 67, AM 4. AM 71, AM 39

IND-35

Dhillon et al. 2007 Fergany et al. 2010 Dhillon unpublished Casanueva et al. 2010 Garcia-Mas personal comm. Dhillon et al. 2009 Fergany 2010 A. Roy unpublished Dhillon et al. 2007 Fergany et al. 2010 Fergany et al. 2010

Shannon et al. 1984

PI 182964, PI 313970, PI 371795, 91161, 91168 IC 274021, IC 267360 AM 8, AM 51, WM 14, WM 19, WM 22, WM 35

Dhillon unpublished data Whitaker 1979

Nugent et al. 1979, 1984 Kishaba et al. 1998 Bohn et al. 1973 Dhillon et al. 2007 Boissot et al. 2008 Vashistha and Choudhury 1971 Vashistha and Choudhury 1974 Srinivasan and Pal 1998 Sambandam and Chelliah 1972 Boissot et al. 2003 Boissot et al. 2000 Kennedy et al. 1978 Fergany et al. 2010 Dhillon et al. 2007 Dhillon et al. 2008 Mansour et al. 1987 East et al. 1992

Reference

AHK 119, AHK 200, RSM 35, RSM 50, RSMDO 6, ‘Arya’ Calif. 525

PI 164343, PI 183311? PI 414723 PI 414723 IC 267353, IC 267384, IC 274010 PI 164320, PI 164323, PI 164723, 90625 (= PI 313970) JC 20-A and ‘Casaba’ ‘‘wild’’ melonz LED 1-9-1-15-2, MM 102-1, ‘Kharda’ ‘‘wild’’ melonz PI 164723, PI 414723, 90625 (= PI 313970) 90625 (= PI 313970) PI 282448, PI 313970, AM 25, AM 39, AM 41, AM 55, and AM 85 IC 274023 WM 8, WM 16 BUS and CHI PI 124101, PI 124431, PI 164343, PI 179895

Accession

97

Fig. 3.2. Geographical distribution of 69 unique Indian melon accessions from 43 locations with specific plant or fruit traits of interest. Number of accessions and traits from a specific location ranged from 1 to 7 and 1 to 10, respectively. The most notable accession is PI 371795 (indicated by
) with 10 traits from Mussoorie in the foothills of the Himalaya Mountains. Not all of the accessions described in the text are represented, either because the location was unknown or they represented a selection of one of the 69 accessions represented above.

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disease in temperate regions (Nagy 1976; Lebeda 1983). More than 28 races of P. xanthii and nine races of G. cichoracearum have been identified on melon (Kr
ıstkov
a et al. 2004; Lebeda and Sedl
akov
a 2004; McCreight 2006; Pitrat and Besombes 2008). Indian snapmelon landraces provide distinct sources of powdery mildew resistance. The two first and important contributors to powdery mildew resistance were collected in western India: California 525 (P. xanthii race 1), as described earlier from the state of Gujarat, and PI 79376 (P. xanthii race 2 and possibly race 1), from the state of Madhya Pradesh (Pryor et al. 1946). PI 124111 and PI 124112, two snapmelons from the eastern state of Bihar, are resistant to 14 and 17 races of P. xanthii, respectively (McCreight 2006). PI 124112 is susceptible to two races of P. xanthii (McCreight 2006). Both accessions are resistant to races 0 and 1 of G. cichoracearum (Pitrat et al. 1998), but MR-1, which was selected from PI 124111 (Thomas 1986), was susceptible to a Czech Republic isolate (Kr
ıstkov
a et al. 2004). Snapmelon PI 414723 was selected for uniform reaction to melon aphid from PI 371795, a contaminant of cucumber (Cucumis sativus L.) PI 175111 purchased as a roaster’s mix in Mussoorie, a city in the state of Uttar Pradesh, and is resistant to 14 and susceptible to eight races of P. xanthii (McCreight et al. 1992; McCreight 2006). The var. acidulus accession PI 313970 is resistant to P. xanthii races 1 (two variants), 2, 2U.S., 3, 4.5, 5, and S (McCreight 2003; McCreight and Coffey 2007; Pitrat and Besombes 2008) and is susceptible to P. xanthii race F and G. cichoracearum race S (Sedl
arov
a et al. 2009). Seeds of PI 313970 (duplicated as PI 315410) were received into the USNPGS in 1966 from the N. I. Vavilov Research Institute of Plant Industry (VIR), St. Petersburg, Russian Federation, where it was entered in the VIR catalog in 1961 as a collection from an unspecified location in India (USDA, ARS 2009ab). It is likely that this accession was collected in southern India, as acidulus melons are found mainly in the south of India (Pitrat 2008). Five snakemelon (var. flexuosus) accessions were heterogeneous for resistance to P. xanthii race 2 (Pryor et al. 1946), but there are no reports of their use for in the development of powdery mildew–resistant, desserttype melons: PI 115935 (local name kakri) collected in Agra, United Provinces (Anon. 1941). PI 134197 (local name tar Lucknow), PI 134198 (local name tar desi), PI 134199 (local name tar Lahori) collected from Lahore, Punjab, now part of Pakistan), and PI 134200 (local name ‘‘Tar Ferozpuri’’) collected in Ferozepur, Punjab, India (Anon. 1950). PI 134199 and PI 134200 are currently available from NPGS; the other three likely will never be available.

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Two other heterogeneous sources of resistance to P. xanthii race 2 are worthy of note because they represent one or two groups of subsp melo: PI 115908 and PI 134192 (Pryor et al. 1946). PI 115908 was obtained in Pune (formerly Poona), Maharashtra. It had elongated (38 cm  20 cm) yellow fruit that were ‘‘more or less netted’’ and had a ‘‘more or less conspicuous navel,’’salmon-colored, firm and juicy flesh with little flavor (Anon. 1941); possibly they were subsp. melo var. adana (Pitrat 2008). PI 134192 collected in Mumbai (formerly Bombay) and known as kharbuza had elongated (30  15 cm) fruit, smooth and unribbed, with a golden brown rind and pale blotches, and firm, orange flesh, and was reported to be an ‘‘excellent keeper’’ (Anon. 1950), possibly subsp. melo var. inodorus (Pitrat 2008). Neither of these two melons will ever be available from NPGS. The genetics of resistance to powdery mildew in melon is becoming increasingly complex as more accessions are studied and more races are described. ‘PMR 45’ (Calif. 525) is at this time the exception; it has been demonstrated to carry only one dominant gene (Jagger and Scott 1937; Epinat et al. 1993). In contrast, most powdery mildew–resistant Indian melon accessions are resistant to more than one race of P. xanthii and have been demonstrated to possess several distinct genes that may act in an independent, monogenic (dominant, recessive, or codominant) or digenic manner, and may involve epistasis (McCreight et al. 1987; Pitrat et al. 1998; McCreight 2003; Pitrat 2005–2006; McCreight and Coffey 2007; Pitrat and Besombes 2008). Four snapmelons (PI 124111, PI 124112, PI 179901, and PI 414723) and one acidulus melon (PI 313970) have been found to possess as many as 14 resistance genes against many of the reported races of P. xanthii and G. cichoracearum (McCreight et al. 1987; Pitrat et al. 1998; McCreight 2003; Pitrat 2005–2006; Pitrat and Besombes 2008). Additional, possibly unique, genes have been described in the acidulus melon PI 313970. McCreight (2003) reported three putatively new genes (two recessive and one semidominant conditioning resistance to P. xanthii races 1 and 2 U.S. in PI 313970 that appeared to be linked). Pitrat and Besombes (2008) found five genes in progeny 90625 a controlled self-pollination of PI 313970) that conferred resistance to strains representing six races of P. xanthii. This study presented a complicated picture of genetic resistance to cucurbit powdery mildew in melon. Two isolates of race 1 were differentiated where resistance to one strain was conditioned by two recessive genes and resistance to the other was conditioned by a single, semidominant gene designated A. Gene B, a second semidominant gene, conditioned resistance to P. xanthii race 2. These two semidominant genes affected expression of genes that conferred resistance to five other strains: Gene A was epistatic to the two recessive genes that conferred

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resistance to race 1 where AA or Aa enabled them to confer resistance to race 3 and one strain of race 5. Gene B acted similarly on the expression of a third recessive gene where BB or Bb enable this gene to confer resistance to a strain of race 4.5 and two different strains of race 5. The allelic relationship of these genes in PI 313970 with previously discussed melon powdery mildew resistance genes in other Indian accessions remains to be fully resolved. PI 313970 is resistant to P. xanthii race S, which first appeared in the desert areas of Arizona (Yuma Valley) and California (Imperial Valley) in 2003 (McCreight et al. 2005). Inheritance data indicate resistance to race S is controlled by a single recessive gene (McCreight and Coffey 2007). PI 313970 exhibited resistant blisters in response to P. xanthii races 1, 2 U.S., and S in greenhouse and field tests, which suggested nonrace-specific resistance to P. xanthii. Resistant blisters appear on otherwise resistant plants of PI 313970 when susceptible germplasm is heavily infected (McCreight2003).IndianaccessionsPI124111andPI124112alsoexhibited resistant blisters in response to P. xanthii race 2 U.S. (McCreight 2003). Two recessive genes in PI 313970 appeared to control expression of resistant blisters in response to P. xanthii race S (McCreight and Coffey 2007). ‘PMR 5’ (Calif. 525 and PI 79376; Whitaker and Jagger 1937; Pryor et al. 1946), ‘Dulce’ (Calif. 525 and PI 79376; Anon. 1968), ‘Gulfstream’ (Calif. 525; http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1111777), and ‘Jacumba’ (Calif. 525, PI 79376 and PI 124111; Harwood and Markarian 1968), all bred in the United States, were resistant to a race-undefined population of Indian powdery mildew in a controlled inoculation test (Waraitch et al. 1977). Interestingly, ‘Seminole’ (PI 124112; Harwood and Markarian1968),selectedforpowderymildewresistanceintheUnitedStates, was susceptible in this test (Waraitch et al. 1977). Arka Rajhans was the sole melon Indian cultivar resistant to powdery mildew in northern and southern Indian field conditions (Nath and Dutta 1969). The reactions of these cultivars to current Indian populations/races of powdery mildew are unknown. Downy mildew caused by the oomycete Pseudoperonospora cubensis (Berk. & Curtis) Rostov. is an important foliar disease of melons in humid production areas worldwide. Six pathotypes of the pathogen have been identified: 1 and 2 in Japan, 3 and 6 in Israel, and 4 and 5 in the United States (Cohen et al. 2003). These pathotypes are incompatible with Luffa ssp. (Thomas et al. 1987). No evidence for race differences exists between North America and Europe (Horejsi et al. 2000). The Chinese and Indian isolates of downy mildew are able to colonize Luffa ssp. and thus are considered as distinct pathotypes. Shetty et al. (2002) also demonstrated that race of P. cubensis in India was distinct when compared to other locations in the United States and Europe.

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Sambandam et al. (1979) reported immune resistance to downy mildew in eight melons including one muskmelon, ‘Annamali’ (Table 3.2). Palti and Cohen (1980) reported PI 180280 resistant to downy mildew (Table 3.2). Jhooty and Bains (1983) reported muskmelons PPD-MR4 and LC-8 and LR-1, a ‘‘wild’’ melon, collected from Punjab resistant to downy mildew in field and laboratory tests (Table 3.2). PPDMR-4 (¼ PPD-MR4?), W1, W3, W4, W5, and W6 were highly resistant to downy mildew races L1 and L2 (Bains and Parkash 1985). PDMR-35 was resistant to race L1 and highly susceptible to race L2 (Bains and Parkash 1985). Presumably, the W lines are the same as W1, W3, W4, W5, and W6 developed by Thomas and Webb (1981) for multidisease resistance to downy mildew, powdery mildew, Alternaria leaf blight (see below) and Papaya ringspot virus (see below). Five partially dominant resistance genes have been found in four Indian snapmelon accessions: PI 124111 (Pc-1, Pc-2), PI 414723 (Pc-3), PI 124112 (Pc-4), and 5-4-2-1 (Pc-5) (Pitrat 2005–2006). Epinat and Pitrat (1994a,b) have reported oligogenic and incompletely dominant resistance in MR-1, selected from PI 124111 for uniform reaction to downy mildew (Thomas 1986), and PI 124112, with five and four genetic factors, respectively. Taler et al. (2004) reported resistance of PI 124111F to P. cubensis pathotypes 3 and 6 in Israel controlled by two eR genes, At1 and At2, which encode photorespiratory enzymes that could correspond to genes Pc-1 and Pc-2. Partial resistance to downy mildew in 120 RIL from a cross of V
edrantais  PI 124112 was controlled by nine QTL, seven of which originated in the partially resistant PI 124112 (Perchepied et al. 2005a). One QTL from PI 124112 explained 12% to 38% of the phenotypic variation for resistance to P. cubensis pathotype 3 in controlled tests and undetermined stains in field tests; together the nine QTL explained from 14% to 50% of the phenotypic variation for resistance to P. cubensis (Perchepied et al. 2005a). Indian snapmelon accession PI 124111F, resistant to all six reported pathotypes of P. cubensis, is susceptible to the Indian isolate of P. cubensis (More 2002), but four snapmelon accessions (IC 267353, IC 274029, KP 7, and B-159) were observed to be resistant to this Indian pathotype (Dhillon et al. 2007; Pandey et al. 2008). We await data on the reactions of these three snapmelons to the six pathotypes of P. cubensis prevailing in the other parts of the world. Fusarium wilt causes severe damage to melon around the world. This soilborne disease caused by Fusarium oxysporum Schlechtend. f. sp. melonis Sny. & Hans. is specific to C. melo. The pathogen enters through the roots and then spreads in the vascular elements leading to the wilting and death of the plant. Four pathogenic races are known: 0, 1, 2, and 1.2,

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as determined by their ability to colonize a known set of differential melon genotypes (Risser et al. 1976). Race 1.2 is further separated into race 1.2 y, which brings yellowing symptoms before the death of the plants, and 1.2 w, which causes wilting and death without the yellowing symptoms. Two dominant genes for resistance to Fusarium wilt have been identified in melon line: Fom-1 in ‘Doublon’ and Fom-2 in CM 17187 (Pitrat 2005–2006), and both genes have been identified in Indian snapmelon germplasm. PI 124111F and its derivative MR-1 have Fom-1 and Fom-2 (Cohen and Eyal 1987; Zink and Thomas 1990). PI 414723 has Fom-2 (Brotman et al. 2005). The Fom-1 gene confers resistance to races 0 and 2 (Risser 1973), and several molecular markers linked to the resistance have been developed (Brotman et al. 2005; Oumouloud et al. 2008). The Fom-2 gene imparts resistance to races 0 and 1 (Risser 1973). This gene, which has been isolated, encodes a protein that contained leucine-rich repeat (LRR) and nucleotide binding site (NBS), being part of the family of resistance genes characterized by the presence of NBS-LRR domains (Joobeur et al. 2004). Race 1.2 overcomes the genes Fom-1 and Fom-2. Partial resistance to race 1.2 reported in some Far East melon accessions (e.g., ‘Ogon 9’) is under polygenic, recessive control (Perchepied and Pitrat 2004). The genetic complexity of partial resistance is an impediment to breeding; up to nine QTL including one major QTL were found in ‘Isabelle’ (Perchepied et al. 2005b), a breeding line with partial resistance derived from ‘Ogon 9’ (Perchepied and Pitrat 2004). BIZ, a breeding line developed in Israel, exhibited near-complete resistance to race 1.2, at an inoculum level as high as 106 spores per ml with root wounding, which indicates that this resistance is stronger than that in ‘Isabelle’ (Herman and Perl-Treves 2007). Fusariumwilt,whichoccurred everyyearfrom2002 through2009, isthe most devastating fungal disease of melons in India. All the melon cultivars grown by Indian farmers (NS 7455, Punjab Sunehri, Punjab Hybrid 1) are susceptible to this disease. Existing global sources of resistance have been found susceptible in Indian field conditions (N. P. S. Dhillon, unpubl. data), indicating the urgent need to find new sources of resistance to this disease among nondessert melon landraces in India. Sudden wilt disease of melon is caused by Monosporascus cannonballus Pollack & Uecker, and it is common in hot, semiarid melongrowing regions of India, southern Spain, southwestern regions of the United States, Saudi Arabia, Central America, Japan, Taiwan, and Tunisia (Cohen et al. 2000). High resistance to M. cannonballus has been reported in the Asiatic accession C. melo subsp. agrestis Pat 81 (Iglesias et al. 1999). A resistant and vigorous rootstock is essential for

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overcoming sudden wilt caused by M. cannonballus (Cohen et al. 2007). The partially dominant resistance found in Pat 81 is attributed to the high regeneration capacity of the root system (Dias et al. 2004; Fita et al. 2008a). This accession has been observed to be a good rootstock for the grafting of melons to resist M. cannonballus. QTL linked to genes for melon root structure have been identified recently (Fita et al. 2008b), opening new opportunities to develop resistant cultivars by manipulation of root architecture. High-level tolerance/resistance to sudden wilt has also been reported in P6a, a breeding line that originated somewhere in Southeast Asia, and the Taiwan cv. ‘Black Skin’ (Cohen et al. 2000). Cultivation of melons grafted onto Cucurbita rootstocks to combat soilborne diseases is a common practice in the Mediterranean basin and Southeast Asia (Lee 1994), but recently it has been discovered that melon/melon grafting combinations perform better than melon/Cucurbita combinations for disease control and fruit size and quality (Cohen et al. 2002). During melon collection expeditions in the arid and semiarid areas of Rajasthan and southwestern Punjab in India, the senior author observed significantly less incidence of Fusarium wilt or Monosporascus sudden wilt among snapmelon and ‘‘wild’’ melon germplasm compared with muskmelon (var. reticulatus) landraces and cultivars (N. P. S. Dhillon, unpubl. data). The senior author has a large (500 þ accessions) collection of snapmelon and ‘‘wild’’ melons in his gene bank that may have resistance to M. cannonballus based in part on root system vigor and architecture. Alternaria leaf blight is incited by Alternaria cucumerina (Ellis & Everh.) and affects most cucurbits and may be prevalent in areas with high temperatures and frequent rainfall (e.g., southern India and the southeastern United States) (Thomas 1996). Resistance to A. cucumerina is controlled by the single, dominant gene Ac in snapmelon MR-1, which was derived from PI 124111 (Thomas 1986). The resistance reaction is characterized by small necrotic lesions that remain restricted in size and do not support abundant sporulation. B. Virus Resistance Melons are adversely affected by a large number of viruses worldwide (Provvidenti 1993; Lecoq et al. 1998). Symptoms fall into three broad categories: mosaics on leaves that may be accompanied by leaf and fruit deformations, general yellowing of the older leaves, and necrosis as either necrotic leaf spots or generalized necrosis that leads to plant death (Lecoq et al. 1998). The virus situation in cucurbits is dynamic (for a discussion, see Nameth et al. 1986; Lecoq et al. 1998).

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Cucumber mosaic virus (CMV) causes severe damage worldwide in some of the most economically important vegetable crops, including melons. Resistance to CMV was first observed in three var. conomon accessions from east Asia, Freeman Cucumber, White Melon, and Ginmakuwa, and appeared to be dominant (Enzie 1943), but later resistance in Freeman Cucumber was shown to be controlled by three recessive genes (Karchi et al. 1975). The same genes were identified in the Korean accession PI 161375 (Risser et al. 1977). Dogimont et al. (2000) mapped several QTL involved in the resistance of the Korean accession PI 161375 to CMV; the QTL detected varied with the isolate. More recently, Essafi et al. (2008) described the recessive gene cmv-1 in the Korean accession PI 161375 that confers total resistance to some CMV strains but is ineffective against other strains. A genetically dominant source of resistance to a broad array of CMV isolates will facilitate breeding of CMV-resistant cultivars. Indian snapmelon accessions AM 25, AM 82, IC 274014, SM 67, SM 72, SM 73, and SM 82 were highly resistant to CMV and remain possible sources of genetically dominant resistance to a broad array of CMV isolates (Dhillon et al. 2007, 2009; Fergany et al. 2011). Zucchini yellow mosaic virus (ZYMV) is a devastating virus of cucurbits worldwide (Lecoq et al. 1998). Three complementary, dominant genes in PI 414723 (Zym-1, Zym-2, Zym-3) condition resistance to ZYMV (Pitrat and Lecoq 1984; Danin-Poleg et al. 1997). Potentially unique sources of resistance to ZYMV were identified in Indian snapmelon accessions IC 274007 and IC 274014 (Dhillon et al. 2007). The var. acidulus accession AM 87 is a potential source of resistance to ZYMV (Fergany et al. 2011). It may be profitable to determine the genetic relationships among these four sources of resistance to ZYMV. Papaya ring spot virus (PRSV), formerly Watermelon mosaic virus 1, is also widespread (Lecoq et al. 1980). Two alleles, Prv1 and Prv2, for resistance to PRSV have been reported in snapmelon accessions PI 180280 and PI 180283 from India (Kaan 1973; Webb 1979; Pitrat and Lecoq 1983). The gene Prv-2 was reported in the snapmelon PI 124112 (McCreight and Fashing-Burdette 1996); its allelic relationships with Prv1 and Prv2 are unknown. Nine more accessions from northern India were heterogeneous for resistance to PRSV: IC 267360, IC 267363, IC 267374, IC 267384, IC 274006, IC 274007, IC 274010, IC 274011, and IC 274013 (Dhillon et al. 2007). Accessions AM 4, AM 25, AM 27, AM 70, AM 78, and AM 100 exhibited necrosis in response to inoculation (Fergany et al. 2011). The genetic relationships between Prv1 and Prv2 and the genes in these 15 accessions remain to be determined. Resistance to PRSV in the western U.S. shipping type, orange flesh muskmelon

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breeding lines WMR 29, W1, W3, W4, W5, and W6, and ‘Cinco’ were derived from PI 180280 (Bohn et al. 1980; Thomas and Webb 1981, 1982). Moroccan watermelon mosaic virus (MWMV), also known as Watermelon mosaic virus-Morocco (WMV-M), is a potyvirus distinct from PRSV-W, WMV, and ZYMV (McKern et al. 1993). Breeding line WMR 29 was reported resistant to MWMV (Lecoq et al. 1998); it is likely that the resistance was derived from PI 180280, the source of PRSV resistance in WMR 29. Fifty landraces lines from two states in southern India, Kerala and Tamil Nadu, exhibited necrotic reactions in response to artificial inoculation with MWMV (Fergany et al. 2011). Watermelon mosaic virus (WMV), formerly Watermelon mosaic virus 2, is widespread (Lecoq et al. 1980). Munger (1991) reported resistance to WMV in four varietas: conomon, ‘Freeman Cucumber’; momordica, PI 371795 from India, PI 414723 derived therefrom, and PI 414723-4 selected for resistance to ZYMV; subsp. agrestis, PI 182938 from India, a small hard melon with no edible flesh; and var. dudaim, a monoecious melon collected in Louisiana, the United States (Wall 1967). Resistance to WMV in PI 414723 is controlled by a single dominant gene, Wmr (Gilbert et al. 1994). Another source of resistance to WMV has been identified more recently in the accession TGR-1551 from Zimbabwe and is under recessive genetic control (D
ıaz-Pendo´n et al. 2005). Cucurbit aphid-borne yellows virus (CABYV), first observed in France (Lecoq et al. 1992), is transmitted by aphids and has been reported to occur worldwide (Lecoq et al. 1998). Symptoms of CABYV on melon are similar to those induced by whitefly-transmitted yellowing viruses, Lettuce infectious yellows and Cucurbit yellowing stunting disorder virus, both discussed elsewhere in this chapter. Resistance to CABYV was identified in seven melons: PI 255478 from Korea and PI 282448 from South Africa; and five melons from India: ‘Faizabadi Phoont’, 90625 (¼ PI 313970), PI 124112, PI 124440, and PI 414723 (Dogimont et al. 1997). Two complementary, recessive genes, cab-1 and cab-2, control resistance to CABYV in the snapmelon accession PI 124112 (Dogimont et al. 1997). Squash mosaic virus (SqMV) is a seedborne virus that also can be transmitted by various types of beetles (Lecoq et al. 1998). Losses to SqMV can be minimized by use of SqMv-free seed. Resistance to SqMV has been reported in two Cucurbita sp. accessions but not in any of the other cucurbit species, including melon (Lecoq et al. 1998). Indian snapmelons AM 7, AM 29, and AM 48 exhibited light symptoms in response to artificial inoculation with SqMV but had positive in enzyme linked immunosorbent assay (ELISA) tests, which indicated virus multiplication (Fergany et al. 2011). It remains to be to determined whether

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the levels of resistance in these lines prevents fruit yield and quality losses to SqMV or reduces the frequency of seed transmission of SqMV. The Indian acidulus melon accession PI 313970 has resistance to three sweetpotato whitefly (Bemisia tabaci Gennadius; SPWF)–transmitted viruses. Lettuce infectious yellows virus (LIYV), which is transmitted by SPWF biotype A, was limited to the lower desert areas of California (Palo Verde, Coachella and Imperial valleys) and Yuma, Arizona (Wisler et al. 1998), in the United States. Resistance to LIYV is controlled by the dominant gene Liy (McCreight 2002). The single recessive gene culcrv in PI 313970 confers resistance to Cucurbit leaf crumple virus (CuLCV), which is transmitted by SPWF biotype B (McCreight et al. 2008). Resistance to CuLCrV was also observed in four other accessions of Indian origin: PI 124111, PI 124112, PI 179901, and PI 414723 (McCreight et al. 2008). Cucurbit yellow stunting disorder virus (CYSDV) was first observed in the United Arab Emirates in 1982 (Hassan and Duffus 1991). It spread throughout numerous Mediterranean countries and the Middle East (Celix et al. 1996; Wisler et al. 1998; Abou-Jawdah et al. 2000; Desbiez et al. 2000; Louro et al. 2000; Yakoubi et al. 2007). CYSDV first appeared in the Americas in 1999 in the lower Rio Grande River Valley of Texas (Kao et al. 2000). It emerged in 2006 as a serious new pathogen of melon in the Sonoran desert production areas encompassing California and Arizona in the United States and Sonora, Mexico (Brown et al. 2007; Kuo et al. 2007). CYSDV subsequently was found in the southeastern United States (Florida) in 2007 (Polston et al. 2008). Resistance to CYSDV was first reported in TGR-1551 (¼ PI 482420), a salad-type melon from Zimbabwe in southern Africa, but its inheritance is unclear. In Spain, where SPWF biotype Q is the vector (Berdiales et al. 1999), resistance in TGR-1551 was reported to be controlled by a single dominant gene designated Cys (Lo´pez-Ses
e and Go´mez-Guillamo´n 2000). In Texas, where SPWF biotype B is prevalent (Sinclair and Crosby 2002), resistance to CYSDV in TGR-1551 appeared to be quantitatively inherited (Park et al. 2007). PI 313970 appeared to be homogeneous for resistance and three other India accessions (Ames 20203, PI 614185, PI 614213) were found to have some putative resistant plants in naturally infected field tests in Imperial Valley, California (McCreight and Wintermantel 2008). Watermelon chlorotic stunt virus (WmCSV) is economically significant in Yemen, Sudan, and Iran (Yousif et al. 2007). Complete resistance to WmCSV has been confirmed in Indian accessions 90625 (¼ PI 313970), PI 124112, and PI 414723 through graft inoculation and multiple field trials in Sudan (Yousif et al. 2007).

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Cucumber green mottle mosaic virus (CGMMV) is one of a few viruses of melon for which there is no known biological vector; it is easily transmitted mechanically and through growing media (Lecoq et al. 1998). The virus has been reported in Europe and Asia, and although regarded as more of a problem in greenhouse production (Hollings et al. 1975), it affected 70% to 80% of plants in cucurbit fields around Delhi, India (Raychaudhury and Varma 1978). Foliar symptoms of CGMMV infection range from mild mottling to bright yellow mosaic; fruit are reduced in size and deformed (Provvidenti 1993). Eleven sources of resistance to CGMMV have been reported in melon (Table 3.2). Two of these lines, FM-1 and FM-5, are Cornell University breeding lines 83-273-6R and 83-275-6L, respectively (Rajamony et al. 1990). These two closely related lines were derived from crosses of Freeman Cucumber with eastern United States types of muskmelons and are also resistant to CMV (pedigree records of H. M. Munger, M. Mazourek, pers. commun.). Resistance in Phoot, Kachri, FM-1, and FM5, and medium resistance in Harela and Chittidar is a polygenic recessive trait with medium resistance dominant to resistance (Rajamony et al. 1990). The cross Kachri (‘‘wild’’ melon)  Phoot (var. momordica) exhibited heterosis in the F1 and transgressive segregation in the F2 for resistance to CGMMV (Rajamony et al. 1990). CGMMV resistance in Phoot and FM 1 was transferred through a program of controlled inoculation and self-pollination that led to the development of five melon lines (VRM 5-10, VRM 29-1, VRM 31-1-2, VRM 42-4, and VRM 43-6) that have high-level resistance to CGMMVand high yield and total soluble solids (More et al. 1993). Kyuri green mottle mosaic virus (KGMMV) is a mechanically transmitted, seedborne virus in Japan, Korea, and Indonesia (Daryono et al. 2005). KGMMV was initially described as the cucumber strain of CGMMV (Tan et al. 2000). KGMMV causes significant losses in Japan and Korea (Tan et al. 2000; Yoon et al. 2001). The isolate of KGMMV in Indonesia was designated KGMMV-YM (Daryono et al. 2005). Four sources of high-level (asymptomatic, no detectable virus) resistance were identified: ‘Kohimeuri’ and ‘Mawatauri’ from Japan, PI 161375 from Korea, and the Indian melon snapmelon PI 371795 (¼ PI 414723) (Daryono et al. 2005). CMV, CGMMV, SqMV, PRSV, and ZYMV are prominent in the spring (dry season) crop of cucurbits in the trans-Gangetic Plains of India (Punjab), whereas whitefly-transmitted begomoviruses predominate in the rainy season but cause less damage than the Spring virus complex (Sharma et al. 2007). Indian snapmelon landrace IC 274014 is an asymptomatic host of CMV that showed field resistance to an unidentified

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begomovirus and tolerance to a viruslike yellowing disease of undetermined origin (Sharma and Kang 2009). C. Root-knot Nematode and Insect Resistance Melon is subject to attack by several species of nematodes and a wide array insect species worldwide. The species varies to some extent among production areas of the world; some, such as byzaw, Gryllotalpa gryllotalpa (Orthoptera, Gryllotalpidae), in Turkmenistan (McCreight et al. 2010), may be unique to one area or region, while others, such as melon aphid (Aphis gossypii) and SPWF, are present in similar environments worldwide. Few insect-resistant melons have been released (Webb 1998), and there are no nematode-resistant cultivars. This is due to a number of factors (for a discussion, see Webb 1998). The minor crop status of melons along with the relatively low cost and ready availability of chemical insecticides over the past 60-plus years has, in general, minimized the necessity to search for sources of host plant resistance in melon to nematodes and insects. There is at present, however, a desire or an awareness of the need worldwide to change the manner in which chemical pesticides are used on crops in order to reduce adverse environmental and human health effects and to reduce production inputs (costs). Host plant resistance to insects is complex, and successful deployment of resistance to a particular insect in horticulturally acceptable cultivars may simplify or complicate pest management of a crop (Kennedy et al. 1967; Smith 1989). Root-knot nematode (RKN), Meloidogyne spp., reduces melon yield to varying degrees worldwide and has been of particular interest in the southeastern United States, where the sandy, coastal soils and moderate climate are favorable. Cucumis metulliferus (USDA, ARS 2010a) has been of great interest for its disease and insect resistance traits (for a discussion, see Chen and Adelberg 2000). Some accessions of this wild species from Africa possess high level of resistance to RKN, Meloidogyne spp. (Fassuliotis 1967, 1970), but three documented attempts to cross C. metulliferus and melon have not advanced beyond a fertile F1 (Chen and Adelberg 2000). High-level resistance to M. incognita was, however, identified in Indian snapmelon landrace IC 274023 (Dhillon et al. 2007) and ‘‘wild’’ melon accessions WM 8 and WM 16 (Dhillon et al. 2008; Roy et al. 2011). The resistance in this germplasm should be exploitable through conventional breeding. More sources of insect resistance have been described in Indian snapmelon and ‘‘wild’’ melon accessions than in melon germplasm from any other region of the world.

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Melon aphid, sometimes known as cotton-melon aphid (CMA), Aphis gossypii Glover, can adversely affect melon fruit yield and quality in all production areas of the world through feeding (Metcalf et al. 1962) and as a vector of viruses (Smith 1972). CMA is a polyphagus feeder that can be genetically differentiated into plant family-specific genotypes that can be further divided into clones or biotypes (Fuller et al. 1999; Charaabi et al. 2008). Numerous sources of host plant resistance to CMA have been identified in melon germplasm from the West Indies (Ivanoff 1944), India (Kishaba et al. 1972), Korea (Bohn et al. 1973; Lecoq et al. 1980), Spain (Pitrat et al. 1988), Africa (Garzo et al. 2002), and Japan (Boissot et al. 2008). Host plant resistance to CMA was first observed in south Texas on four melon varieties from the West Indies (Ivanoff 1944). Two derivatives of the West Indian melons were susceptible to CMA biotype D, which was collected in Imperial Valley, California (Kishaba et al. 1971). The snapmelon PI 414723, selected from PI 371795 for uniform resistance to CMA biotype D (McCreight et al. 1992), expressed three different mechanisms of resistance to CMA: antibiosis, antixenosis, and tolerance (Bohn et al. 1972), and was used to develop orange flesh muskmelon breeding lines AR Topmark, AR 5, and AR Hale’s Best Jumbo (McCreight et al. 1984). The CMA-resistant Charentais type melon ‘Margot’ was developed from a complex backcross breeding program that used CMA-resistant Korean germplasm PI 161375, Ginsen makuwa, and Kanro makuwa crossed with ‘Vedrantais’ and various Charentais-type recurrent parents (M. Pitrat, unpubl.). The Vat gene, first described in PI 161375, appears to be the major gene responsible for antibiotic and antixenotic mechanisms of resistance in melon to CMA (for a discussion, see Boissot et al. 2008). Vat also confers resistance to transmission of some viruses by CMA (Pitrat and Lecoq 1980; see below for further discussion of resistance to virus transmission in melon to CMA-borne viruses). Tolerance to CMA is independent of antibiosis and antixenosis conferred by Vat. Tolerance to CMA expressed as freedom from curling of leaves following CMA infestation is conditioned by the single dominant gene Ag (Bohn et al. 1973). Tolerance to CMA expressed as vigorous plant growth is partly independent of the leaf curl response in PI 414723 and is not present in PI 161375 (Bohn et al. 1973). PI 255478, which is also from Korea, exhibited high tolerance to CMA expressed as freedom from leaf curl and stunting of plant growth but expressed a lower level of antibiosis than PI 414723 and PI 161375 (Bohn et al. 1973). Tolerance expressed as freedom from leaf curl to CMA in TGR-1551, which was collected in Zimbabwe, is allelic to the dominant

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N. P. S. DHILLON ET AL.

gene Ag in PI 414723 (Sarria et al. 2008). A survey of melon germplasm for tolerance to CMA revealed that many were homogeneous for freedom for leaf curl but susceptible or heterogeneous for stunting (Bohn et al. 1996). CMA biotypes/clones must be considered in choosing a source of CMA resistance for breeding or a CMA-resistant cultivar commercial production. The south Texas and D (California) biotypes differentiated melons from the West Indies and India (Kishaba et al. 1971). Likewise, Soria et al. (2000) showed PI 161375 susceptible (antibiosis was not expressed) to infestation by a CMA biotype obtained, presumably, in the south of Spain. The complexity of biotype differences was further revealed by recent research by Boissot et al. (2008) on the interactions of 21 melon accessions, including three new sources of CMA resistance from India (PI 164320, PI 164323, PI 164723) with four clones of CMA that represented two genotypes. In summary, they hypothesized multiple alleles at the Vat locus that confer resistance to NM1 clones and susceptibility to C9 clones. ‘Miel Blanc’, PI 164323, PI 282448, and ‘Escrito 8429’ were exceptional in that resistance to CMA and virus transmission were independent (Boissot et al. 2008). PI 164323, which was collected from Tamil Nadu, India, behaved like PI 161375 in Spain: susceptible to infestation but resistant to virus transmission. It should also be noted that progeny 90625 (¼ PI 313970) was highly resistant to two clones of one genotype and susceptible to two clones of the second genotype used in the Boissot et al. (2008) study. Cucumber beetles (CB) attack melon seedlings and fruit (Kishaba et al. 1998). Resistance has been reported in melon to three species of CB: western spotted [Acalymma trivittatum (Mannerheim)] and western striped [Diabrotica undecimpunctata undecimpunctata (Mannerheim)], and banded [Diabrotica balteata (Le Conte)]. Western spotted and western striped CB caused extensive damage in California in the early 1950s (Michelbacher et al. 1953), and they have reemerged in recent years as economically damaging pests in that state. Resistance to CB in seedlings and leaves was attributed to two genes, bi (Lee and Janick 1978) and cb (Nugent et al. 1984; Pitrat 2005–2006). PI 164343 was the likely source of the cb gene (Nugent et al. 1979, 1984), although it could have originated in PI 183311, a landrace from Gujarat, India (USDA, ARS 2010d). High susceptibility to feeding damage by CB observed in the central Asian casaba (var. inodorus) melon ‘Deserta Naja’ was dominant to low-level susceptibility in other melon cultivars, and ‘Deserta Naja’ was preferred by CB in choice tests (Coudriet et al. 1980). The Indian snapmelon PI 414723 expressed two levels of resistance to western striped and spotted CB: low level by seedlings and

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high level by fruit rinds (Kishaba et al. 1998). The basis for seedling and fruit resistances in PI 414723 remains to be determined. Melon fruit fly, Bactrocera (Dacus) cucurbitae (Coquillett), is widely distributed in temperate, subtropical, and tropical areas of the world. There is concerted effort worldwide to manage this pest through local area management including male-sterile releases, bagging of fruit, field sanitation, monitoring and control parapheronome lures/cue-lure traps, baits, and biological control (Dhillon et al. 2005). Of the eight species of infesting cucurbits in India, B. cucurbitae is the most common fruit fly on melon (Kapoor 1970). Myiopardalis pardalina (Diptera, Trypetidae) also occurs in India and is an important pest of melon in Turkmenistan, where it is known as melon fly (McCreight et al. 2010). High-level, genetic resistance to B. cucurbitae in ‘‘wild’’ melon is controlled by two complementary recessive genes, dc-1 and dc-2 (Chelliah 1970; Sambandam and Chelliah 1972). High levels of cucurbitacins in fruit of ‘‘wild’’ melon were correlated with resistance to D. cucurbitae (Chelliah and Sambandam 1974). The agromyzid leafminer (ALM), Liriomyza sativae Blanchard (¼ munda Frick), is distributed worldwide on many crop species (Anon. 2010b). Natural and insecticide-induced outbreaks of ALM commonly damage melons (UC IPM Online 2010). Two sources of high-level resistance to ALM were identified in tests at three locations in the United States (Kennedy et al. 1978). Three F1 hybrids of PI 282448 with different susceptible melons suggested the possibility of two or more recessive genes for resistance, evaluated as mean number of mines per leaf, in this bitter, wild melon from South Africa (Kennedy et al. 1978; USDA, ARS 2010c). Resistance to ALM expressed as mean number of mines per leaf and as percent mortality of larvae in the Indian snapmelon PI 313970 was lower but not significantly different from PI 282448 at Beltsville, Maryland, but was significantly lower for number of mines at Irvine, California (Kennedy et al. 1978). Mean number of mines per leaf were essentially equal in these two accessions and their F1 hybrid in a test at Clinton, North Carolina (Kennedy et al. 1978). Resistance to ALM in PI 313970 in an F1 hybrid with ‘Top Mark’ was partially dominant at Clinton (Kennedy et al. 1978). Liriomyza trifolii (Burgess), another species of leafminer, is a serious economic pest in India. Field resistance to this pest has been observed in melon accession 04-02 (var. tibish) from Sudan (Pandey et al. 2010). An F1 hybrid developed using this tibish line and Indian landrace of var. flexuosus (Punjab Long melon 1) exhibited field resistance to leafminer and heterosis for marketable yield, earliness, and carotenoid content (Pandey et al. 2010; see also Section V of this chapter).

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Melonworm, Diaphania hyalinata L., is widely distributed in the Americas (Valles and Carpinera 1992). The insect feeds during the night initially on leaves; as the population increases, it feeds on all plant organs including the flowers and fruit (Valles and Carpinera 1992; Boissot et al. 2000). Resistance to melonworm in 90625 (¼ PI 313970) was likely due to antixenosis as the melonworm life cycle duration and larval and adult mortalities were similar on ‘V
edrantais’ and 90625 (Boissot et al. 2000). Red pumpkin beetle, Aulacophora foveicollis Lucas, is the most destructive and widespread beetle pest in India (Srinivasan and Pal 1998). Six sources of resistance to red pumpkin beetle have been reported in melon: JC 20-A and ‘Casaba’ (Vashistha and Choudhury 1971); ‘‘wild’’ melon (Vashistha and Choudhury 1974); and LED 1-9-1-15-2, MM 102-1, and ‘Kharda’ (Srinivasan and Pal 1998). ‘Casaba’ has a single dominant gene, Af, for resistance to red pumpkin beetle (Vashistha and Choudhury 1974). SPWF is a subtropical insect species that has an extremely broad host range, and several biotypes of this pest are known (Anon. 2010a). Biotypes A (SPWF-A) and B (SPWF-B) were differentiated from one another in the early 1990s when the B biotype displaced the A biotype in the desert southwestern United States. SPWF-B was initially regarded as a distinct species, Bemisia argentifolii Bellows & Perring (Bellows et al. 1994), but was later regarded as a variant of B. tabaci (for a discussion, see Wisler et al. 1998). The Q biotype occurs along with the SPWF-B biotype in Spain and Portugal, where they displaced the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Guirao et al. 1997). Prior to introduction of SPWF-B to the desert southwestern United States, SPWF-A caused yield losses in melon production primarily through its role as a vector of LIYV (Wisler et al. 1998) and secondarily through excretion of honeydew on foliage and subsequent growth of sooty mold that reduced photosynthesis and fruit quality. SPWF-B is a vector of CYSDV and CuLCrV in the desert southwestern United States and perhaps just as important its higher feeding and reproductive rates relative to SPWF-A stunt and kill plants unless very aggressive control measures are implemented (Isaacs et al. 1998). SPWF populations have increased worldwide (Cohen et al. 1992; Brown 1994); in Imperial Valley, California, it increased 1,600-fold from the 1970s (SPWF-A) to the 1990s (SPWF-B), with a sixfold increase from 1981 (SPWF-A) to 1991 (SPWF-B; for a discussion, see Wisler et al. 1998). There were nearly 300-fold and 1,200-fold higher numbers of nymphs and eggs, respectively, on the third true leaves of melon plants in Imperial Valley

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than in Charleston, South Carolina, Leesburg, Florida, and Weslaco, Texas (McCreight et al. 1995). Insecticides available in the 1990s were not adequate to control SPWF-B. Furthermore, SPWF quickly developed resistance to the most efficacious insecticides (Prabhaker et al. 1992). Recently developed insecticides show promise of providing economic levels of control (Palumbo 2008, 2009; Castle et al. 2009), but they too may prove to be less effective after sustained use. Lightweight, fabric row covers that exclude whitefly adults from feeding on young seedling plants effectively decrease whitefly population levels and reduce or delay the incidence of whitefly-transmitted viruses on melons (Palumbo 2008). Host plant resistance is a potentially valuable tool in the integrated pest management SPWF to minimize melon yield and quality losses to this insect and to reduce insecticide applications on melon. Eleven melon accessions exhibited resistance to SPWF-B in one or more tests in Guadeloupe, French West Indies, and seven of them had fewer adults or larvae: PI 161375, PI 164723, PI 414723, 90625 (¼ PI 313970), Faizabadi Phoont, Kanro Makuwa, Meloncillo (Boissot et al. 2003). Indian snapmelon accessions PI 164723, PI 414723, and 90625 (¼ PI 313970) and PI 161375 (Korea) appeared resistant to SPWF-B regardless of the SPWF-B population pressure (Boissot et al. 2003). Resistance in 90625 is due in part to antixenosis but mainly to antibiosis expressed as survival rate from egg to adult on detached leaves: 26% on 90625 compared to 77% on ‘V
edrantais’ and 88% on ‘Top Mark’ (Boissot et al. 2000). Spider mites are major plant pests on melons worldwide (Davidson and Lyon 1979). On melon, they primarily cause damage by feeding on leaf surfaces; in severe infestations, leaves become chlorotic, epinastic, and enveloped by webs (Scully et al. 1991). East et al. (1992) identified nine melon accessions resistant to twospotted spider mite (TSSM) Tetranychus urticae Koch in greenhouse and field tests in Weslaco, Texas. Two of the accessions, BUS and CHI, which had expressed resistance to the carmine spider mite, T. cinnaharinus Boisduval, in Israel (Mansour et al. 1987), PI 136223 from Canada, and two accessions from India (PI 164343 and PI 179895) expressed resistance to TSSM in mass greenhouse tests and had significantly lower numbers of female mites per leaf in more intensive greenhouse studies. Four other lines expressed resistance to TSSM in mass greenhouse tests and had lower densities of mites in field tests: PI 124101 and PI 124431 from India, and PI 125896 and PI 125956 from Afghanistan. PI 136223 from Canada was also identified as a potential source of TSSM resistance. Inheritance of resistance TSSM in BUS, PI 136223, and PI 179895 was investigated in crosses with ‘Perlita’, a susceptible western

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N. P. S. DHILLON ET AL.

shipping-type melon adapted to Texas (Anon. 1964). These three accessions were similar for resistance to TSSM, but PI 179895 was the superior parent (Scully et al. 1991). Resistance to TSSM in PI 179895 was partially dominant for number of adult female mites and perhaps overdominant for numbers of males and immatures. The F1 with BUS expressed overdominance for numbers of adult females and male/immatures. D. Resistance to Insect Transmission of Viruses Resistance to virus transmission by vectors is a potential means of limiting spread of viruses in melon. Such resistance is distinct from resistance to virus multiplication and movement. Lecoq et al. (1979) reported resistance toCMVtransmission byCMAin melonPI 161375andthatresistance to transmission was vector-specific but not virus-specific (Lecoq et al. 1980). Subsequently, Pitrat and Lecoq (1980) reported five other sources of resistance to CMA transmission of viruses: Ginsen makuwa, Kanro makuwa, and Shiro uri okayama from Japan, and PI 164320 and PI 414723 from India. Three more Indian snapmelon landraces were reported resistant to transmission by CMA: IC 267353, IC 267384, and IC 274010 (Dhillon et al. 2007). Resistance in these lines was found to be conditioned by the Vat gene (Pitrat and Lecoq 1980). Soria et al. (2003) reported TGR-1551 resistant to CMA transmission of viruses and presented evidence of a possible second gene for this trait in TGR-1551. E. Flavor Improvement Fruit sweetness is a major determinant of the melon fruit quality (Yamaguchi et al. 1977) while the sugar:acid ratio is the indicator of sensory (flavor) quality in other horticultural fruits. A combination of high sugar and high acid was not detected in two surveys of C. melo (Stepansky et al. 1999a,b; Burger et al. 2003). The range of titrable acidity in commercial Indian melons is 0.12% to 0.2% (N. P. S. Dhillon, unpubl. data). Burger et al. (2003) demonstrated that sugar (suc/suc) and acid (So/–) accumulation in sweet melon are under independent genetic control and that it is possible to combine both in one genotype that has a unique taste due to the changed sugar:acid ratio. Their research also revealed independent control of individual organic acids, such as malic versus citric. They found high titrable acidity (0.51%) in an Israeli landrace of snakemelon (var. flexuosus) maintained by Arabic growers (Y. Burger, pers. commun.). We have found new sources of high acidity in Indian snapmelon landraces IC 274021 (0.61%) and IC 267360 (0.57%) (Dhillon et al. 2007). Additional sources of even higher (1.92%) acidity

3. MELON LANDRACES OF INDIA: CONTRIBUTIONS AND IMPORTANCE

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have also been identified in Indian ‘‘wild’’ melon accessions WM 14, WM 19, WM 22, and WM 35 and acidulus accessions AM 8 and AM 51 (Fergany et al. 2011; Anamika Roy, unpubl. data). Thus these potentially unique sources of high acidity enable new breeding for new combinations of sweet and sour flavors of potential interest for fresh and processed melon products. Syngenta released in 2008 a pleasant-tasting melon that has 700 to 800 mg citric acid per 100 g fruit flesh with a pH level of 4.5 (Patent no: EP 1587933B1) (Casanueva et al. 2010). The low-pH gene was derived from Indian melon var. momordica accession IND-35 (Jordi Garcia-Mas, pers. commun.) and introgressed through marker-assisted breeding. F. Vitamin and Mineral Content Although melon is considered a rich source of b-carotene and vitamin C (Lester 1997), there is a paucity of published data on genetic variation for vitamins and minerals in melons. Burger et al. (2004), in a survey of 350 melon accessions from different horticultural groups of C. melo, observed a 50-fold variation in ascorbic acid content, ranging from 0.7 mg to 35.3 mg100 g1 of fresh fruit weight. Ascorbic acid and b-carotene content ranged from 7.0 to 32.0 mg100 g1 and 4.7 to 62.2 mg100 g1, respectively, in sweet melons (Crosby et al. 2006). We surveyed landraces of var. momordica, var. acidulus, and ‘‘wild’’ melon from different agroecological regions of India (Dhillon et al. 2007; Fergany et al. 2011) for genetic variation for vitamins and minerals. Higher amounts of ascorbic acid were detected in the snapmelon landraces of northern India (up to 34.1 mg100 g1) compared to the accessions from eastern India (up to 19.4 mg100 g1). Accessions of acidulus melon from tropical humid regions of southern India were low in ascorbic acid (up to 9.0 mg100 g1). Ascorbic acid ranged from 3.25 to 24.4 mg100 g1 in ‘‘wild’’ melon landraces from northern India. Carotenoids are a group of plant pigments significant in the human diet as the only precursors of vitamin A whose deficiency, a serious problem in many parts of the developing countries, can lead to permanent blindness and increase the incidence of infectious diseases (West and Hill-Darnton 2001). A maximum level of 160 mg  g1 total carotenoids was achieved in ‘Golden Rice’ through genetic engineering (Ye et al. 2000), and 170 mg is the recommended daily intake of carotene for human beings. Carotenoids of mature fruits of var. momordica, var. acidulus, and ‘‘wild’’ melon accessions ranged from 34.7 to 308.2, 30.8 to 146.3, and 76.8 to 290.5 mg100 g1, respectively (Dhillon et al. 2009; Fergany 2010; A. Roy unpubl.).

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The World Health Organization (WHO) estimates that more than 2 billion people have deficiencies in key micronutrients, such as Fe and Zn (Uauy et al. 2006). We observed wide variation for P (2.6 to 26.4 mg 100 g1), K (19.7 to 294.3 mg100 g1), Fe (0.2 to 1.14 mg100 g1), Zn (0.1 to 1.29 mg100 g1), in nondessert-type Indian melons (momordica and acidulus) (Fergany et al. 2011). High intensity of Fe (1.14 mg100 g1) and Zn (0.1 to 1.29 mg100 g1) was observed in two acidulus accessions (AM 67 and AM 4, respectively) from southern India. Higher amount of P (up to 26.4 mg100 g1) and K (up to 294 mg100 g1) was reported in two other acidulus accessions (AM 70 and AM 39, respectively)from southern India. The famous mineral-rich variety Glupro of hexaploid bread wheat contains 3.5 mg100 g1 and 2.92 mg100 g1 of Fe and Zn, respectively (K. Singh, pers. commun.). The potential for increased micronutrient content of melon from genetic variation through transgressive segregation or by exploiting heterosis in melons is unknown at present. Nondessert melons (var. momordica and acidulus) are available in the Indian market for about five months of in spring and the rainy season and are utilized by poor and middle-class consumers. Mineral- and vitamin-rich cultivars in these varietas would be important supplements to the nutrition needs of these consumers. Sweet melons are low in Fe (0.4 mg.100 g1) and Zn (0.5 mg100 g1) content (Decoteau 2000). Nondessert-type melons of Indian origin are therefore promising sources of genetic variation for increased Fe and Zn content of sweet melon cultivars. G. Seedling, Vegetative, Flower, and Fruit Traits and Isozymes In melon, 174 genes have been reported (Pitrat 2005–2006). Resistance to disease and insect pests were controlled by 56 of the genes, and 36 of them described earlier in the chapter were discovered in melon germplasm from the Indian subcontinent, specifically present-day India and Pakistan. Various seedling, vegetative, flower, and fruit traits and isozymes were controlled by 118 of the genes, 35 of which were described in melon germplasm from the Indian subcontinent or in segregating progenies from complex crosses involving one or more Indian accessions (Table 3.3). Three additional genes may have been described in Indian germplasm, but the source of the var. agrestis germplasm used was not stated: short lateral branching (Ohara et al. 2001), Sour (Kubicki 1969), and White color of immature fruit (Kubicki 1969). QTL for 15 disease and fruit traits of melon have been discovered, 3 of which are disease resistances (Pitrat 2005–2006). Three fruit traits (length, shape, and width) are controlled by various numbers of QTL in the cross V
edrantais  PI 414723 (P
erin 2002; Monforte et al. 2004).

117

Aconitase-1. Isozyme variant with two alleles Bitter fruit-1. Bitterness of tender fruit in ‘‘wild’’ melon that contains 2.6  level of total crude cucurbitacins of ‘Delta Gold’. Relationships with Bi, Bif-2 and Bif-3 are unknown. Empty cavity. Carpels are separated at fruit maturity leaving a cavity. Ec in PI 414723, ec in V
edrantais. Fructose diphosphate-1. Isozyme variant with 2 alleles, each regulating 1 band. Glucosephosphate isomerase. Isozyme variant with 2 alleles, each regulating 1 band. Gelatinous sheath around the seeds. Isocitrate dehydrogenase. Isozyme variant with 2 alleles, each regulating 1 band. juicy flesh. Segregates discretely in a monogenic ratio in segregating generations. Lobed leaf. Dominant on nonlobed, linked with Acute leaf apex. (L in Maine Rock, l in P.V. Green). long mainstem internode. Affects internode length of the main stem but not of the lateral ones. Macrocalyx. Large, leaflike structure of the sepals in staminate and hermaphrodite flowers (Mca in makuwa, mca in Annamalai). Malate dehydrogenase-4. Isozyme variant with 2 alleles, each regulating 1 band.

Aco-1 Bi-f-1

Mdh-4

Mca

lmi

L

jf

Gs Idh

Gpi

Fdp-1

Ec

Description

Gene symbol

Staub et al. 1998

PI 179923y

(continued)

Ganesan and Sambandam 1979

Ganesan and Sambandam 1985 McCreight 1983

Chadha et al. 1972

Ganesan 1988 Staub et al. 1998

Annamalai

LJ 48764x

P.V. Green

Hara Madhu

‘‘wild’’ melon PI 218070y

Staub et al. 1998

Staub et al. 1998

PI 218071y PI 179680

P
erin et al. 1999

Staub et al. 1998 Chelliah and Sambandam 1974

PI 218071y ‘‘wild’’ melon

PI 414723

Reference

Source

Table 3.3. Genes and quantitative trait loci (QTL) reported for seedling, vegetative, flower, and fruit traits, and isozymes in melon accessions from the Indian subcontinent (present-day India and Pakistan) or in segregating progenies from complex crosses involving one or more Indian accessions.z

118

Malate dehydrogenase-5. Isozyme variant with 2 alleles, each regulating 1 band. Malate dehydrogenase-6. Isozyme variant with 2 alleles, each regulating 1 band. Mealy flesh texture. Dominant to crisp flesh. Mealy flesh texture-2 male sterile-1. Indehiscent anthers with empty pollen walls in tetrad stage. male sterile-2. Anthers indehiscent, containing mostly empty pollen walls, growth rate reduced. Mottled rind pattern. Dominant to uniform color. Epistatic with Y (not expressed in Y_) and st (Mt_ st st and Mt_ St_ mottled; mt mt st st striped, mt mt St_ uniform). (Mt in Anamali, mt in makuwa). Musky flavor (olfactory). Dominant on mild flavor (Mu in C. melo callosus, mu in makuwa or Annamalai). nectarless. Nectaries lacking in all flowers. Pale green foliage. Pa Pa plants are white (lethal); Pa pa are yellow. Peptidase with glycyl-leucine. Isozyme variant with 2 alleles, each regulating 1 band. 6-Phosphogluconate dehydrogenase. Isozyme variant with 2 alleles, each regulating 1 band. Relationship with Pgd-1 and 6-Pgd-2 is unknown. Phosphoglucomutase. Isozyme variant with 2 alleles, each regulating 1 band. Relationship with Pgm-1 is unknown. pH (acidity) of the mature fruit flesh. Low pH value in PI 414723 dominant to high pH value in Dulce.

Mdh-5

pH

Pgm-2

Pgd-3

Pep-gl

n Pa

Mu

Mt

ms-2

Me Me-2 ms-1

Mdh-6

Description

Gene symbol

Table 3.3 (Continued)

Danin-Poleg et al. 2002

Staub et al. 1998

PI 218070y, PI 179923y PI 414723

Staub et al. 1998

PI 218070y

Staub et al. 1998

Bohn 1961 McCreight and Bohn 1979

LJ 20991x LJ 22309x

PI 218070

Ganesan 1988

Ganesan 1988

Annamalai

Annamalai

Bohn and Principe 1964

Staub et al. 1998

LJ 39301-8x

Staub et al. 1998

Reference

Ganesan 1988 P
erin et al. 1999 Bohn and Whitaker 1949

y

PI 179923 , PI 180283 PI 179923y, PI 180283 ‘‘wild’’ melon PI 414723 LJ 16822x

Source

119

Peroxidase-2. Isozyme variant with 2 codominant alleles, each regulating a cluster of 3 adjacent bands. The heterozygote has 4 bands. sutures. Presence of vein tracts (‘‘sutures’’) on the fruit. Subtended floral leaf. The floral leaf bearing the hermaphrodite flowers is sessile, small, and encloses the flower. (Sfl in makuwa, sfl in ‘Annamalai’). Sour taste-2. spherical fruit shape. Recessive to obtuse; dominance incomplete. speckled fruit epidermis. st striped epicarp-2. Present in Dulce, recessive to nonstriped in PI 414723. White testa-2 yellow green leaves. Reduced chlorophyll content. fruit length. 4 QTL described in the cross V
edrantais  PI 161375 and 4 QTL in the cross V
edrantais  PI 414723; 1 is common to both crosses. fruit shape (ratio fruit length/fruit width). 6 QTL described in the cross V
edrantais  PI 161375 and 2 QTL in the cross V
edrantais  PI 414723, which are common to both crosses. 8 QTL described in the cross Piel de Sapo  PI 161375. fruit width. 5 QTL described in the cross V
edrantais  PI 161375 and 1 QTL in the cross V
edrantais  PI 414723. PI 414723

PI 414723

PI 414723 LJ 34417x PI 414723

PI 414723 PI 414723

PI 414723 Lucknow

Unidentified Indian accession Sarda Annamalai

y

Based on Pitrat 2006. From present-day Pakistan. x Mutants observed in progenies from complex crosses with one or more Indian accessions.

z

fw

fs

Wt-2 yg fl

spk st-2

So-2 sp

s Sfl

Prx-2

P
erin et al. 2002b

Monforte et al. 2004; P
erin et al. 2002

P
erin et al. 1999 Whitaker 1952 P
erin et al. 2002b

P
erin et al. 1999 Bains and Kang 1963; Lumsden 1914 P
erin 2002 Danin-Poleg et al. 2002

Bains and Kang 1963 Ganesan and Sambandam 1979

Dane 1983

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Cracking of mature fruit typifies var. momordica, although not all such varieties or lines exhibit this trait, and was dominant to non-cracking in crosses of severe cracking var. momordica varieties with var. reticulatus, var. utillissumus (¼ acidulus), and a noncracking inbred of var. momordica (Nath and Dutta 1971). Cracking was controlled by two genes in two var. momordica  ‘‘wild’’ melon crosses, but the gene action differed between the two crosses (Parthasarathy and Sambandam 1981).

IV. GENETIC DIVERSITY Genetic diversity is a prerequisite for the development of improved cultivars through breeding. Knowledge, access, and use of the available diversity in domesticated and ‘‘wild’’ accessions are essential for broadening the genetic base of modern melon cultivars and for sustainable genetic improvement. Melon landraces are cultivated throughout India, but previous collection efforts have focused mainly on the regions in northern India. For example, the National Bureau of Plant Genetic Resources, the national gene bank of India, stores about 1,000 melon accessions from India, the majority of which originated in North India (S. Pandey, pers. commun.). Similarly, USNPGS holds 832 melon accessions from India; merely 9% come from southern India and only four accessions are from eastern India (K. R. Reitsma, unpublished). The genetic diversity of 378 melon accessions from central and northwestern India collected in 1992 was assessed using 19 isozyme loci (McCreight et al. 2004). Cluster analysis using genetic distances among accessions yielded 11 groups of varying size from 41 sites in Rajasthan and Madhya Pradesh. These results indicated that collections of melon landraces should be made in eastern and southern India. We have collected more accessions from the different agroecological regions of southern (AM accessions), eastern (SM accessions), and northern (WM accessions) India and assessed their genetic diversity by measuring variation at nine simple sequence repeat (SSR) loci (160 alleles, polymorphisminformationcontent(PIC)value0.81).Figure3.3depictsthe neighbor-joining tree for the range of genotypes examined based on variability at these SSR loci (N. P. S. Dhillon, unpubl. data). The distribution of melon accessions fits very well with the geographical origin in India. For example, the melon accessions collected from northern (cluster A), southern (cluster B), and eastern (cluster C) regions clustered separately, demonstrating a clear genetic differentiation among gene pools. Also, reference populations from various parts of the world—for example, Spain (PS, var. inodorus), France (VED, var. reticulatus), Europe (SARDA, var. inodorus),

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Fig. 3.3. Neighbor joining tree for the set of Indian melon accessions along with other reference genotypes.

Israel (EIN, var. ameri), Japan (GIN, var. makuwa), Korea (SON, var. chinensis), Maldives (MAL, var. agrestis), Pakistan (TRI, var. agrestis), Iraq (FLEX, var. flexuosus), Zambia (ZAI, var. agrestis) and India (MOM, var. momordica; INB, var. momordica; AHK 200, var. agrestis; AHK 119, var. agrestis;AHC13,var.momordica)—weregeneticallydistinctfromtheA,B, and C clusters (N. P. S. Dhillon, unpubl. data). In parallel studies (Dhillon et al. 2009; Fergani et al. 2010; N. P. S. Dhillon, unpubl. data) based on SSR analysis, we have found a high percentage of unique alleles present in melon landraces that originated in southern (24.2%) and eastern (30.4%) India and ‘‘wild’’ melon accessions belonging to northern India (34.5%), whencomparedwithasimilarsetofinternationalreferenceaccessions.Ina similar study, Dhillon et al. (2007) found that north Indian snapmelon germplasm (IC-accessions) also contained a high degree of unique genetic variability. Using factor correspondence analysis, the IC germplasm collection was located in the center of the diversity plot, probably as a

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Fig. 3.4. Depiction of genetic relationships among melon accessions of diverse origin using factor correspondence analysis as estimated by nine SSR loci.

primary center of melon diversity with the Mediterranean and the countries around the China Sea corresponding to the two extremes of the geographical distribution of C. melo. The AM, SM, and WM germplasm collections do not, however, have a central position compared with occidental and oriental reference genotypes, which suggests that these gene pools did not contribute significantly to the origin and diversification of occidental and oriental cultivars (Fig. 3.4). Globally, the amount of genetic variability observed in the AM, SM, and WM germplasm pools is certainly higher than expected. Melon might have been introduced from Africa to India, where extensive domestication occurred. In India, several introductions may have happened from northern and southern Africa (Akashi et al. 2002, 2006; Yashiro et al. 2005). The high degree of divergence among the Indian collections supports the contention that the introduction history of melon in India was complex and might have involved several events, leading to the development of secondary and tertiary centers of diversity (Luan et al. 2008). All these results together confirm that India is the primary center of melon diversity. As a result of genetic drift and selective breeding, there is less genetic variability in the melons found in secondary centers of diversity, e.g., eastern Asia (Far East) and western Mediterranean area (Akashi et al. 2002; Lo´pez-Ses
e et al. 2003; Monforte et al. 2003)—and

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distal parts of the primary center of diversity—for example, Turkey (Esquinas-Alcazar and Gulick 1983; Sensoy et al. 2007). Introduction of unique genetic variability from Indian germplasm to the secondary centers of diversity will increase the genetic variability for solving the current and future breeding problems and introduce new traits into modern cultivars. India is divided into 21 agroecological regions comprising 131 agroecological subregions (Sehgal et al. 1992). This regions and subregions approach should be adopted for future melon explorations in India in order to retain and conserve existing genetic variability in melon. V. MELON BREEDING A. Development of Improved Salad Melons Intraspecific hybridization between different horticultural groups of C. melo can be exploited to develop high-yielding F1 hybrids of salad-type melon. Snakemelon (var. flexuosus) is important salad-type melon in north India. Its fruits are long, slender, ribbed or wrinkled, and young fruits eaten fresh in salad. The open pollinated cvs. ‘Punjab Longmelon 1’ and ‘Arka Sheetal’ have been released to growers in India, but high-yielding hybrids of this salad melon have not emerged in the market. This is attributed to the very low genetic diversity within this type of melon (S. Pandey, pers. commun.). Pandey et al. (2010) crossed a homozygous landrace of snakemelon (Punjab Long melon 1) with eight salad-type inbred landraces: var. momordica, cv. Wanga, var. acidulus, var. chate, var. conomon, var. dudaim, var. chito, and var. tibish. Two hybrids from the crosses of snakemelon  ‘Wanga’ (Punjab Wanga) and snakemelon  tibish melon (04-02) exhibited significant heterosis over the better parent, which is also the standard cultivar, for marketable fruit number per vine (205% and 224%, respectively) and marketable yield per vine (212% and 219%, respectively). Both hybrids showed high dominance for ascorbic acid (9.1 mg100 g1 of fruit flesh), and the (snakemelon  tibish) hybrid exhibited dominance for carotenoid concentration (3720 mg100 g1 of fruit flesh). This is the first demonstration of lifting yield and nutritional barriers in snakemelon by using natural variation available in other salad-type C. melo varietas. The commercial potential of these two snakemelon hybrids will be evaluated after extensive testing over environments and years. B. Melons with Stable Yield and Consistent Sweetness ‘Punjab Hybrid’, a famous F1 hybrid melon (var. reticulatus) released in India in 1982, was produced from the cross between a line with male

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Table 3.4. Sweet melon cultivars developed from Indian melon landraces through single plant selection. Cultivar

Origin of parental landrace in India

Durgapur Madhu Arka Jeet Hara Madhu Kashi Madhu Arka Rajhans Pusa Madhuras Hisar Madhu RM-43

Rajasthan Uttar Pradesh Uttar Pradesh Uttar Pradesh Rajasthan Rajasthan Rajasthan Rajasthan

Yield (tonnes/ha)

Brix (%)

20 15 20 27 25 20 20 20

14 14 13 14 13 13 9 12

Reference Bhatnagar and Singh 1968 Nath and Dutta 1971 Nandpuri and Singh 1972 Pandey et al. 2008 Nath and Dutta 1971 Sharma et al. 1972 Munshi and Alvarez 2004 Munshi and Alvarez 2004

sterile gene, ms-1 (Bohn and Whitaker 1949) and Hara Madhu, a landrace from Uttar Pradesh. This hybrid remained in cultivation for more than two decades in India and was known for consistent brix (13%) and stable yield (22 t/ha) (Nandpuri et al. 1982). Indian melon breeders have developed eight improved varieties of sweet melon through single plant selection from local landraces (Table 3.4), and 20 to 1000 ha is planted to each of these varieties every year (S. Pandey, pers. commun.). Indian farmers selected another 32 other sweet melon landraces that are popular in various parts of India (Table 3.5) (Munshi and Alvarez 2004). C. Tailoring of ‘‘Climate-Ready’’ Melons There is widespread concern about global warming, which has been predicted to change global weather patterns and result in changes in the frequency and intensity of droughts, with flooding in some areas and drought, desertification, or salinization in other areas (Le Hou
erou 1996). Moreover, groundwater supplied in the main agricultural regions of the world is being overdrawn at a greater rate than its replenishment by rains (Schiermeier 2009). For example, the Punjab state of India, considered to be the granary of the country, is facing a water deficit of 10.28 million acrefeet, a situation that threatens the sustainability of its agricultural production (Jain and Kumar 2007). Drought-/flood-/salinity-tolerant melon germplasm would make melons applicable in almost every circumstance. It is possible to develop less water-demanding melon genotypes through breeding. Snapmelon and ‘‘wild’’ melon are very drought hardy and cultivated in the arid regions of India during the rainy season (Pareek and Samadia 2002). Selection from the local material of ‘‘wild’’ melon

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Table 3.5. Popular sweet melon landraces of India developed by farmers and their place (state) of origin in India. Landrace

Origin in India

Landrace

Origin in India

Allahabad Kajara Bagpat Balteshwar Batti Bhathesa Chiranji Galteshwar Goose Hara Gola Haridhari Jam Neel Jaunpuri Jogia Kabri Gurbeli Kadapa Kajri

Uttar Pradesh Uttar Pradesh Uttar Pradesh Uttar Pradesh Andhra Pradesh Andhra Pradesh Gujarat Maharashtra Rajasthan Punjab Maharashtra Uttar Pradesh Uttar Pradesh Madhya Pradesh Karnataka Uttar Pradesh

Kanpuria Kavita Kharri Jalgaon Kutana Ladoo Lucknow Safeda Mahaban Mathuria Mau Motta Panam Papaya Sanganer Sharbat-e-Anar Sunkheda Tonk

Uttar Pradesh Madhya Pradesh Madhya Pradesh Haryana Andhra Pradesh Uttar Pradesh Uttar Pradesh Uttar Pradesh Uttar Pradesh Rajasthan Gujarat Andhra Pradesh Rajasthan Andhra Pradesh Gujarat Rajasthan

Source: Munshi and Alvarez 2004.

in arid regions of Rajasthan, India, has led to the development of two highly drought-tolerant lines, AHK 119 and AHK 200. We have further observed in our trials that snapmelon germplasm thrives well at very low levels of irrigation, compared to sweet melons, without any penalty on yield (N. P. S. Dhillon, unpubl. data). Comprehensive drought tolerance evaluation of momordica and ‘‘wild’’ germplasm from the arid areas of India is required to identify sources of genes for drought and high-temperature tolerance for breeding sweet melons suited to these abiotic stresses. Dhillon (unpubl. data) evaluated the drought tolerance of six melon accessions belonging to four horticultural varietas (reticulatus, inodorus, ‘‘wild,’’ chate) in a greenhouse, using four plants of each accessions planted in a completely randomized design. Drip irrigation was removed when the plants were 58 days old. Two accessions of ‘‘wild’’ melons (AHK 119, AHK 200) and var. chate cv. Arya exhibited high tolerance to drought stress compared to the accessions belonging to var. reticulatus and inodorus group (Table 3.6). After irrigation withdrawal, the ‘‘wild’’ accessions and ‘Arya’ wilted completely, and the leaves desiccated and senesced after 58 and 62 days, respectively, compared with 33 to 37 days for the reticulatus and inodorus accessions. In another field experiment in the arid region of Rajasthan, 60-day-old seedlings of 58 melon accessions (var. momordica, chate, reticulatus) collected from

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Table 3.6. Drought tolerance of melons after irrigation withdrawal of 58-day-old seedlings in a greenhouse.

Genotype

Origin

Variety group

Days for complete drying and death of leaves

T111 Hara Madhu Punjab Sunehri AHK 119 AHK 200 Arya

Spain India India India India India

inodorus Jacquin reticulatus Naudin reticulatus Naudin agrestis Naudin agrestis Naudin chate Hasselquist

33 35 37 58 58 62

arid regions of India were subjected to drought stress to the point of wilting three successive times in a randomized block design with two replications (N.P.S. Dhillon, unpubl. data). After each stress treatment, seedlings were irrigated with 1 liter of water per day to allow seedlings to recover. The responses of the seedlings were determined using a visual scale in which seedlings were grouped into five categories from 1 to 5 (Toker et al. 2007) where 1 ¼ highly drought susceptible (leaves and branches dried out, no recovery) and 5 ¼ highly drought tolerant (no visible drought effect and full recovery after three successive wiltings). One accession of each of var. chate (RSM 35), var. momordica (RSM 50), and ‘‘wild’’ melon (RSMDO 6) were observed as highly drought tolerant compared to var. reticulatus cultivars ‘Pusa Madhuras’ and ‘Arka Jeet’ (Fig. 3.5). Interestingly, one landrace of var. reticulatus (‘Kashi Madhu’) also exhibited a good level of drought tolerance (rating ¼ 2). Salt tolerance may become an essential trait for sustainable melon production. Indian snapmelon accession Calif. 525 was credited for contributing high-level tolerances to salt and high air temperatures as well as resistance to powdery mildew, as described earlier, in ‘PMR 45’, the first modern western U.S. shipping-type melon (Jagger and Scott 1937). In comparison to its powdery-mildew-susceptible parent, ‘Hale’s Best’, ‘PMR 45’ was adapted (tolerant) to growth in the relatively saline soils and high ambient temperatures of the arid, inland valleys of the southwestern United States (Whitaker 1979). Salt tolerance is a complex trait to evaluate and varies with plant development and media (Maas and Nieman 1978). In a survey of 43 melon genotypes from seven countries, several of 11 accessions from India exhibited salt tolerance during seed germination and/or during vegetative growth (Shannon et al. 1984). In the seedling emergence part of

Drought tolerance rating

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5 4 3 2 1 0 RSMDO 6

RSM 35

RSM 50

Kashi Madhu

Pusa Madhurus

Arka Jeet

agrestis

chate

momordica

reticulatus

reticulatus

reticulatus

Genotype and horticultural varietas Fig. 3.5. Drought tolerance after plants were subjected to three successive wiltings; rated on a 1–5 scale, where 1 ¼ highly drought tolerant (no visible drought effect and full recovery) and 5 ¼ highly drought susceptible (leaves and branches dried out, no recovery) in sweet melons, ‘‘wild’’ melon, and other nondessert melons of Indian origin.

this study, PI 313970 (¼ 90625), 91161 (var. momordica), and 91168 (var. flexuosus) emerged faster than ‘PMR 45’ at 6 bar osmotic potential. In the vegetative growth part of this study, PI 182964, PI 313970 (¼ 90625), and PI 371795 exceeded the growth of ‘Top Mark’ by 1 standard deviation at 1.7 bars osmotic potential but were comparable to ‘PMR 45’. Melon cultivars from China, Japan, and Russia exhibited comparable levels of tolerance in these tests (Shannon et al. 1984). Interestingly, ‘PMR 45’ and ‘Persian’ are adapted to saline soils. Salt tolerance can thus be transferred from these valuable accessions when used as donor parents of disease-resistance traits, as happened in the development of ‘PMR 45’. Furthermore, grafted melons have been reported to be more tolerant to salinity than the nongrafted ones (Romero et al. 1997). Melon landraces should therefore be collected from the coastal areas of India (Gujarat, Karnataka, Kerala, Andhra Pradesh, Tamil Nadu, Orissa) for identification of salt-tolerant germplasm needed for melon grafting. Tolerance to high water stress is valuable in some situations. Akashi et al. (2002) reported that most (88%) of the melon landraces collected from the Assam region (high-rainfall area in India) were tolerant to high levels of soil moisture and confirmed the wet tolerances in field tests in Japan. They concluded that this wet tolerance trait was selected by the

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farmers in the rainy areas sandwiched between the Himalayas and the Bay of Bengal. D. Molecular Markers Molecular markers became important and useful during the 1990s for genetic improvement of rice, maize, tomato, and other major crops, but it was not until the first decade of the 21st century that they had an important impact on melon genetics and breeding. Molecular markers are widely used in public and private genetics and breeding of many crops, including melon, for a wide array of applications, including cultivar identification, hybrid seed certification, genetic variability studies, marker-assisted selection, QTL mapping, and map-based cloning. The first molecular markers used in melon were restriction fragment length polymorphism (RFLP) and random amplified polymorphic DNA (RAPD) (Baudracco-Arnas and Pitrat 1996; Garcia et al. 1998; Stepansky et al. 1999a; Zheng and Wolff 2000) and inter-simple sequence repeat (ISSR) (Stepansky et al. 1999a; P
erin et al. 2002a). The pioneering work of Katzir et al. (1996) introduced SSR markers in this species. SSR markers have been the marker choice for a large number of genetic and breeding applications in recent years because they are PCR based, codominant, easily transferable among laboratories, and cost efficient and allow medium-high throughput genotyping. The large number of recently developed SSR markers (Danin-Poleg et al. 2001; Chiba et al. 2003; Ritschel et al. 2004; Gonzalo et al. 2005; Fukino et al. 2007; Fernandez-Silva et al. 2008; Harel-Beja et al. 2010) provide a rich and useful resource for breeders and geneticists. More recently, singlenucleotide polymorphism (SNP) markers are becoming more popular in plant breeding (Ganal et al. 2009) because of the possibility of high-throughput genotyping at affordable cost. SNP markers are also currently available, and they have been proven useful for both mapping and genetic variability analysis (Morales et al. 2004; Deleu et al. 2009; Harel-Beja et al. 2010). Molecular markers have been used for a large number of applications in melon, but it is out of the scope of this review to list all of them. Among them can be listed: (1) assess the relative levels of genetic diversity in primary and secondary centers of diversity (Neuhausen 1992; Garcia-Mas et al. 2000; Lo´pez-Ses
e et al. 2003; Staub et al. 2004); (2) demonstrate the reduction of genetic diversity during and after domestication (Monforte et al. 2003; Dhillon et al. 2007); (3) tag genes for resistance to diseases and insect pests (Brotman et al. 2005; Perchepied et al. 2005b); (4) develop map-based cloning of disease

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resistance (Joobeur et al. 2004; Nieto et al. 2006) and sex expression genes (Boualem et al. 2008; Martin et al. 2009); (5) develop molecular marker maps (Danin-Poleg et al. 2001; P
erin et al. 2002a; Gonzalo et al. 2005; Fukino et al. 2007; Zalapa et al. 2007; Cuevas et al. 2008; Fernandez-Silva et al. 2008; Harel-Beja et al. 2010); (6) map QTL (P
erin et al. 2002b; Monforte et al. 2004; Zalapa et al. 2007; Paris et al. 2008; Cuevas et al. 2009; Harel-Beja et al. 2010); and (7) develop introgression lines (Eduardo et al. 2005). Several molecular markers linked to host plant resistance genes have been found in Indian melon germplasm. Teixeira and Camargo (2006) and Brotman et al. (2005) developed amplified polymorphism length (AFLP) and cleavage amplified polymorphic sequence (CAPS) markers linked to Prv1 that confers resistance to PRSV in PI 180280 and PI 414723, respectively. Danin-Poleg et al. (2002) found a SSR marker tightly linked to Zym-1, which confers resistance to ZYMV in PI 414723. QTL associated with downy mildew and powdery mildew resistances have been mapped in the Indian accession PI 124112 (Perchepied et al. 2005a). Powdery mildew resistance genes derived from Indian melon germplasm have been tagged with molecular markers, and routine molecular breeding is performed by private breeding companies (J. Torbun, pers. commun.). Nevertheless, a large number of resistance genes have been discovered in Indian melon landraces for which linked molecular markers have yet to be developed. For example, the Indian landrace PI 313970 (90625) belonging to acidulus group has been described as resistant to CABYV (Dogimont et al. 1996); LIYV (McCreight 1992); CYSDV (McCreight and Wintermantel 2008); powdery mildew (McCreight 2003; Pitrat and Besombes 2008); and D. hyalinata, B. tabaci, and A. gossypii (Boissot et al. 2000). Molecular markers linked to these genes would facilitate their introgression into commercial cultivars. The Indian melon accession PI 124112 was used to clone the gene a, which controls sexual expression (monoecious versus andromonoecious flowers) in melon (Boualem et al. 2008). The causal SNP responsible for sex expression was found within a 1-aminocyclopropane-1carboxylic acid synthase (ACS), designated CmACS-7, being part of the ACS gene family. Previously, five ACS genes (CmACS-1–CmACS-5) had been described (Ishiki et al. 2000; P
erin et al. 2002b; Moreno et al. 2008), but none of them was associated with sex expression. A perfect CAPS marker, Alu1CAPS, was developed to distinguish between monoecious and andromonoecious genotypes (Boualem et al. 2008). The Korean accession PI 161375 has been extensively used to develop many of the current melon reference maps (Oliver et al. 2001; P
erin et al. 2002a; Gonzalo et al. 2005; Fernandez-Silva et al. 2008) and to develop

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and map QTL for fruit quality traits (Monforte et al. 2004). The development of an introgression line population from a cross of PI 161375 with Piel de Sapo (Eduardo et al. 2005) enabled identification and characterization of QTL involved in fruit quality and root architecture (Eduardo et al. 2007; Fernandez-Trujillo et al. 2007; Fernandez-Silva et al. 2008; Fita et al. 2008a, 2008b; Moreno et al. 2008; Obando et al. 2008). The fruit nutritional value, quality, and yield potential of U.S. western shipping (USWS) type melon could be improved through the introgression of genes from exotic germplasm. Recently, QTL controlling fruit yield (Zalapa et al. 2007), quality (Paris et al. 2008), and the quantity of b-carotene (Cuevas et al. 2008, 2009) have been identified in exotic germplasm and introgressed into a USWS genetic background. Genes for these traits were obtained from both elite USWS (‘Top Mark’) and exotic-derived lines (e.g., USDA 846-1). Line USDA 846-1 was derived from a Costa Rican accession that possesses many of the same attributes of Indian snapmelons (e.g., multiple lateral branching and monoecious sex expression). Crosses between ‘Top Mark’ and USDA 846-1 led to the development of recombinant inbred lines for QTL mapping and comparative genomic analyses of many of the current genetic maps (i.e., Spanish, French, and Chinese) (Cuevas et al. 2008, 2009). The Indian accession PI 414723 has been used to develop partial or supporting maps to those involving PI 161375 (Danin-Poleg et al. 2001; P
erin et al. 2002a; Silberstein et al. 2003), and QTL maps of fruit shape (Perin et al. 2002b). Harel-Beja et al. (2010), using a recombinant inbred population from a cross between PI 414723 and the American muskmelon cv. Dulce, developed a dense genetic map that included 386 SSR, 76 SNP, six insertion-deletion (INDEL) and 200 amplified fragment length polymorphism (AFLP) markers. Interestingly, this map includes genes involved in the metabolism of sugars (31 genes), carotenoids (11 genes), volatiles (5 genes), and ethylene synthesis and regulation (6 genes). They also described QTL for such agronomically important traits as sugar and carotenid accumulation and fruit morphology. Further research will lead to the successful exploitation of the beneficial alleles and allele combinations in Indian melon germplasm for a wide range of traits, such as disease resistance, stress tolerance, fruit quality. and yield.

VI. FUTURE ROLE OF INDIAN MELON GERMPLASM AND CONCLUSIONS A vast amount of melon genetic diversity is available in India, which has important implications for genetic vulnerability and potential for melon

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improvement. Indian melon landraces possess a significant number of unique DNA profiles distinct from that of melon germplasm from other parts of the world and contains a number of novel alleles (Dhillon et al. 2007, 2009; see also Section IV of this chapter). This germplasm most likely possesses the largest number of unique and potentially agronomically useful alleles. For example, two or three fruits per vine is a norm in modern sweet melon cultivars. Using unique Indian melon germplasm, a gene-based approach might result in development of melon cultivars with increased number of fruits per vine. In the recent past, agronomically inferior germplasm has been employed to break yield, quality, and adaptability barriers in various crops (Tanksley and McCouch 1997; Schaffer et al. 1999; Gur and Zamir 2004). Melon breeders have been effective in improving the melon crop. A significant part of this success has been from pedigree breeding through recombination and subsequent selection during inbreeding of closely related elite cultivars and further use of the derived inbreds in hybrid development programs. Repeated recycling of a relatively small number of genetically closely related melon lines in commercial breeding has reduced the genetic diversity within the melon crop. This has led to the genetic uniformity that has predisposed the crop to biotic and abiotic stresses and has restricted the long-term yield improvement. The melon germplasm pool that breeders use for the development of new cultivars is much less diverse than the overall diversity within the crop. Performance-driven selection and grower preferences create a narrow germplasm base (Duvick 2005). This is evident by the frequent regional dominance of only a few cultivars. A narrowing of the melon genetic base is under way in India as well. For example, a single sweet melon cultivar, NS 7455, has been grown over the majority of the area in India for more than a decade. If a similar trend develops in salad-type melon production in India, the result will be a real loss of genetic variation and germplasm (i.e., genetic erosion). Biofortification of salad-type melons (momordica, acidulus, flexuosus) in tropical countries needs more attention. The micronutrients Fe, Zn, and vitamin A have been recognized by WHO as limiting for human health. Indian melon landraces hold promise in providing more genetic variation for enhanced Fe and Zn. Drought tolerance in Indian melon landraces offers largely unexploited variation for sustainable production in the face of reduced water supplies for agriculture worldwide. We have found that drought-tolerant Indian melon landraces (AHK 200, Arya) and other improved material are genetically distant (Fig. 3.3). These are encouraging results for melon breeders as potential additive genetic variance for drought tolerance may

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be exploited in the crosses through field-based selection for drought tolerance. The additive nature of inheritance of most abiotic stress traits in crops such as wheat and rice suggests that insertion of a single gene through transgenesis is unlikely to provide satisfactory broad drought adaptation (Trethowan and Mujeeb-Kazi 2008). Moreover, technology transfer, regulatory and intellectual property hurdles, and unlikely public acceptance would delay or prevent its use in melons. After more than 140 transgenic melon field trials in the United States in 1996, there are still no commercial transgenic melon varieties in the marketplace (Nunez-Palenius et al. 2008). Soilborne diseases will be increasingly important as pesticide usage continues to decrease as a result of environmental concerns. Comprehensive information is needed on Indian melon landraces (momordica, acidulus, ‘‘wild’’) for vigorous root growth, resistance to soilborne pathogens (Fusarium spp., Monosporascus spp.) and nematodes (Meloidogyne spp.), and suitability for potential rootstocks for grafting. Melon rootstocks with RKN resistance are not commercially available, to our knowledge, but we have found a couple of accessions of Indian snapmelon landrace and ‘‘wild’’ melon, which is a weed in melon fields, as promising candidates for resistance to RKN (Dhillon et al. 2008). Crop germplasm treated as weeds in one area have proven useful as rootstocks in another area. For example, some lines of Solanum torvum Swartz (Turkey berry, a widespread weed in Florida) with a vigorous root system, collected from Puerto Rico and Thailand, have been successfully used for grafting solanaceous plants in Japan by Takii Seeds (Kubota et al. 2008). Multiple disease-resistant melon germplasm need to be fully exploited. Indian melon landraces have served as a unique source of resistance to several diseases. For example, PI 313970 (var. acidulus) is a source of resistance to LIYV (McCreight 2000), CuLCrV (McCreight et al. 2008), races 1, 2, 2 U.S., 3, 3.5, 4.5, 5, and S of P. xanthii (McCreight 2003; McCreight and Coffey 2007; Pitrat and Besombes 2008) and to CYSDV (McCreight and Wintermantel 2008). Another Indian melon landrace, PI 371795, and its derivative PI 414723 carry resistance to powdery mildew, downy mildew, ZYMV, WMV, CABYV, WCSV, A. gossypii, cucumber beetle, and sweet potato whitefly, and is salt tolerant (Table 3.2). Extensive collection, preservation, and evaluation of Indian melon landraces is vital to prevent further genetic erosion in this primary center of melon diversity and to help to find new resistance genes to combat new pathogens and pests and new races of pathogens (e.g., powdery mildew). Clearly, we need a conscious effort to collect and conserve

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melon diversity from the various agroecological regions of India in gene banks; otherwise, it will be permanently lost, robbing future melon cultivation of invaluable options. We ignore their conservation at our own peril. International collaborations are developing genomics tools for melon (www.icugi.org). Large collections of expressed sequence tags (EST) and SNP markers, very dense molecular marker maps, and the melon genome sequence (http://melonomics.upv.es) will be soon available. These new tools will facilitate allele mining within Indian germplasm and introduce new genetic variability in the sweet melon gene pool. The sequence of the melon genome has already been completed ( J. Garcia-Mas, unpubl. data) and sequencing the genomes of landraces and varieties will soon be possible at low cost, which offers new opportunities for genetic improvement of melon. We are on the verge of an exciting era of melon genetic improvement. Whole-plant breeding and genomics technologies are combining to preserve and fully characterize the complete array of genetic variability in melon and exploit that germplasm and information for the further improvement of salad and dessert melons for diverse markets worldwide.

ACKNOWLEDGMENTS This chapter is dedicated to the memory of late Dr. Harbhajan Singh (1916–1974), the most distinguished plant explorer of India, fondly known as the Indian Vavilov. He established a small unit of plant exploration in the Division of Botany at the Indian Agricultural Research Institute (IARI) and later became head of the Division of Plant Introduction at IARI, which eventually developed into the National Bureau of Plant Genetic Resources (NBPGR).

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4 Transgenic Vegetable Crops: Progress, Potentials, and Prospects Jo~ ao Silva Dias Technical University of Lisbon Instituto Superior de Agronomia Tapada da Ajuda 1349-017 Lisboa, Portugal Rodomiro Ortiz Department of Plant Breeding and Biotechnology Swedish University of Agricultural Sciences P.O. Box 101 SE-230 53 Alnarp, Sweden

ABSTRACT Vegetables are considered essential for well-balanced diets and are grown worldwide, on large and small farms, on good and marginal land, and by large commercial growers and small subsistence farmers. The consumption and caloric contribution of vegetables to the diet vary widely with geographical region, nationality, local customs, and cuisine. Vegetable production, due to their cultivation intensity, suffers from many biotic stresses caused by pathogens, pests, and weeds and requires high amounts of pesticides per hectare. Pesticide residues can affect the health of growers and consumers and contaminate the environment. This chapter reviews the status of transgenic vegetables to improve vegetable production, emphasizing its place in integrated pest management. Examples are drawn from advances and potentials in transgenic research on tomato, eggplant, potato, cucurbits, brassicas, lettuce, alliums, sweet corn, cowpea, cassava, sweet potato, and carrots. Highlighted are host plant resistance to pathogens and pests, tolerance to herbicide, quality (both fresh and processed), and vaccine delivery

Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick.
2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 151

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in transgenic vegetables. Although conventional plant breeding that utilizes nontransgenic approaches will remain the backbone of vegetable genetic improvement strategies, the advantages of genetically modified technology for improvement of vegetables include reduced pesticide use, increased yields, added health benefits, and lower production costs. These advantages should provide incentive for integration of this technology into vegetable breeding, if consumer resistance can be overcome or mollified. KEYWORDS: biosafety; gene flow; GM crops; horticulture; integrated pest management; plant breeding I. WORLD VEGETABLE PRODUCTION II. CASE FOR TRANSGENIC VEGETABLES A. Limiting Factors in Vegetable Production—Pathogens, Pests, and Weeds B. Problems with Pesticide Residues C. Vegetable Breeding D. Genetic Engineering E. Food Safety F. ‘‘Super-Weeds’’ III. CASE STUDIES A. Tomato 1. Fruit Ripening 2. Fruit Quality 3. Insect Resistance 4. Fungal Resistance 5. Bacterial Resistance 6. Viral Resistance 7. Plant Stress 8. Vaccines B. Eggplant 1. Insect Resistance 2. Fungal Resistance 3. Plant Stress 4. Parthenocarpy C. Potato 1. Insect Resistance 2. Late Blight Resistance 3. Host Plant Resistance 4. Other Traits D. Cucurbits 1. Summer Squash 2. Watermelon 3. Cucumber 4. Melon E. Brassicas 1. Insect Resistance 2. Disease Resistance 3. Weed Control 4. Postharvest Quality

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5. Healthy Food 6. Male Sterility and Self-Incompatability 7. Plant Stress F. Lettuce 1. Disease Resistance 2. Weed Control 3. Male Sterility 4. Postharvest Quality 5. Healthy Food 6. Plant Stress G. Alliums 1. Weed Control 2. Quality 3. Disease Resistance 4. Insect Resistance H. Sweet Corn I. Cowpea J. Root Crops 1. Cassava 2. Sweet Potato 3. Carrot IV. GM VEGETABLES AND INTEGRATED PEST MANAGEMENT V. OUTLOOK LITERATURE CITED

I. WORLD VEGETABLE PRODUCTION Vegetables are considered essential for well-balanced diets since they supply vitamins, minerals, dietary fiber, and phytochemicals and have been associated with improvement of gastrointestinal health, good vision, and reduced risk of heart disease, stroke, chronic diseases such as diabetes, and some forms of cancer (Keatinge et al. 2010). ‘‘Hidden hunger,’’ or micronutrient deficiency, is a pernicious problem that is caused by a lack of vitamins and minerals such as vitamin A, iodine, and iron in the human diet and affects the health of between 2 and 3.5 billion people in the developing world (Pfeiffer and McClafferty 2007). Vegetables are grown worldwide, on large and small farms, on good and marginal land, and by large commercial growers and small subsistence farmers. According to the Food and Agriculture Organization (FAO) statistics, the production of vegetables in the world in 2007 was almost 900 million tonnes (FAO 2009). Asia produced 74.7% of the world’s vegetables (671 million t) on 72.8% of the world’s vegetable production area (52.7 million ha). China has always been a large contributor to world vegetable production and currently produces over 50% of the world’s vegetables, which translates to

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313 kg per capita. India is the second largest producer of vegetables in the world, but at almost a sixfold lower level than China. Worldwide the area of arable land devoted to vegetables is expanding at 2.8% annually, higher than fruits (1.75%), oil crops (1.47%), root crops (0.44%), and pulses (0.39%), and at the expense of cereals (–0.45%) and fiber crops (1.82%) (FAO 2009). The consumption and caloric contribution of vegetables to the diet vary widely with geographical region, nationality, local customs, and cuisine. In China, the largest consumer, vegetables make up about 35% of per-capita food consumption, a much higher share than the world average (Gale 2002). India, Bangladesh, Cambodia, Vietnam, Laos, and the Philippines are also high producers and consumers of vegetables. For example, vegetables comprise 40% of the Bangladeshi diet (Rich 2008). Many vegetables are consumed near where they are produced, especially in Asia. The per-capita consumption of vegetables in Asia has increased from 41 to 141 kg between 1975 and 2003 (FAO 2009). As worldwide health awareness increases and household income grows, an increasing global demand for vegetables is expected. At the same time, available arable land and a suitable water supply are lessening, so energies should be directed to enhance vegetable productivity and quality. Increasingly, consumers in developed and developing countries are concerned about the quality and safety of their food as well as the social and the environmental conditions where it is produced. It is expected that the assurance of safe vegetable products will become increasingly important. Food safety legislation in the European Union and in the United States is introducing increasingly stricter standards. In general, vegetable production suffers from many biotic stresses caused by pathogens, pests, and weeds and requires high amounts of plant protection products per hectare. This chapter provides an overview on the prospects for the production of transgenic vegetables to improve vegetable production, emphasizing its place in integrated pest management.

II. CASE FOR TRANSGENIC VEGETABLES A. Limiting Factors in Vegetable Production—Pathogens, Pests, and Weeds Plants, being immobile, are unable to escape pathogens that cause plant diseases and pests that feed and damage them. Diseases of plants are caused mainly by fungi, bacteria, viruses, and nematodes. Approximately 70,000 species of pests exist in the world, but of these, only 10%

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are considered serious pests (Pimentel 1997). Synthetic pesticides have been applied to crops since 1945, and have been highly successful in reducing crop losses to some pest insects, plant pathogens, and weeds, and in increasing crop yields (Pimentel 1997). One estimate suggests that without pesticides, crop losses to pests might increase by 30%. Despite pesticide use, insects, pathogens, and weeds continue to exact a heavy toll on world crop production, approaching 40% (Oerke et al. 1994; Pimentel 1997). Preharvest losses are globally estimated as 15% for insect pests, 13% for diseases, and about 12% for weeds (Pimentel 1997). Vegetables, due to their cultivation intensity, suffer particularly from these biological stresses. Because of the high diversity of vegetable crops, pest loads are varied and complex compared to field crops. Since vegetables are high-value commodities with high cosmetic standards, the main method for controlling pathogens, pests, and weeds has been the use of pesticides. Vegetables are often consumed in fresh form, so pesticide residue and biological contamination is a serious issue. Furthermore, considerably fewer resources have been directed at improving vegetable production and pest management options compared to field crops such as rice, wheat, and maize (Lumpkin et al. 2005). Vegetables account for the major share of the global pesticide market. Almost 25 kg per ha of active pesticide substances are used on average in vegetable production in the European Union (OECD 1997). Although vegetable production accounts for less than 1% of the U.S. crop area, it accounts for 14% of total pesticide use (Osteen 2003). Nearly 20% of the worldwide annual pesticides expenditures, valued at U.S. $8.1 billion, are applied to vegetables (Krattiger 1997); only cotton used more insecticides on an area basis. Insecticides are regularly applied to control a complex of insects that cause damage by feeding directly on the plant or by transmitting pathogens, particularly viruses. B. Problems with Pesticide Residues Although pesticides have played a vital role in the production of food and in the protection of the health of population worldwide, when used carelessly or improperly, pesticide residues can affect the health of growers and consumers and contaminate the environment. Pesticide residues are often attributed to the failure of growers to restrain application before harvesting and to the use of prohibited pesticides. Human poisonings and their related illnesses are clearly the highest price paid for pesticide use. Worldwide, an estimated 26 million persons suffer from pesticide poisonings each year; approximately 3 million are poisoned seriously enough to be hospitalized and about 220,000

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severely enough to prove fatal (UNEP 1997). The situation is especially serious in developing countries, even though these nations utilize only 20% of the total pesticides applied in the world (Pimentel and Lehman 1993). A high pesticide poisoning–to–deaths ratio occurs in developing countries, where there tend to be inadequate occupational safety standards, protective clothing, and washing facilities; insufficient enforcement of safety regulations; poor labeling of pesticides; illiteracy; and insufficient knowledge of pesticide hazards. Pesticide residues in vegetables can exceed tolerance limits, especially in developing countries (Mansour 2004; Ferreira 2009). In India, a survey of pesticide residues in vegetable crops taken at the farm gate and in markets from 1999 to 2003 confirmed that of the 3,043 samples, 9% contained residues above acceptable levels (Choudhary and Gaur 2009). The increase of residues in vegetables is a major issue to consumers. There are concerns about the ability of small growers, mainly from the developing world, to meet exacting quality and safety standards of the commercial sector. The problem of residues is not restricted to developing countries. About 35% of the foods purchased by U.S. consumers have detectable levels of pesticide residues, and 1% to 3% of these foods have pesticide residue levels that are above the legal tolerance level. Residue levels may be higher because the analytical methods now employed in the United States detect only about one-third of the more than 800 pesticides in use on crops (Pimentel and Hart 1999). Both the acute and chronic health effects of pesticides warrant attention and concern. While the acute toxicity of most pesticides is well documented, information on the effects of pesticides on chronic human illnesses such as cancer is murky. There are estimates that less than 1% of human cancers in the United States are attributable to pesticide exposure. Since there are approximately 1.2 million new cancer cases annually in the United States, approximately 12,000 cases of cancer per year may be due to pesticides (Pimentel and Hart 1999). There is also growing evidence of sterility in humans and various other animals, particularly in males, related to the presence of various chemicals and pesticides in the environment. Sperm counts in the United States and Europe have declined by about 50% and continue to decrease an additional 2% per year (Pimentel and Greiner 1997). Pesticides also affect natural predators and parasites that control or help to control herbivorous pest populations in both natural and agroecosystems. Natural enemies play a major role in keeping the populations of many insect and mite pests under control, but these natural enemies can be adversely affected by pesticides. It is well known by all the growers and the scientific community that several pests reached out-

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break levels in many vegetable crops following the destruction of their natural enemies by pesticides. Sometimes when outbreaks of secondary pests occur because their natural enemies are destroyed by pesticides, additional and often more expensive pesticide treatments have to be made in an effort to sustain yields. This extra use of pesticides raises overall costs and contributes to pesticide-related problems. Many millions of dollars can be attributed to the cost of additional pesticide applications and increased crop losses, both of which result from the destruction of natural enemies by pesticides. Several studies report also that the use of herbicides in vegetable production may result in the total elimination of the weeds that harbor some predatory insects. Wild birds are also affected by pesticides, a fact that makes the birds excellent ‘‘indicator species’’ of pollutant levels in the environment. Deleterious effects of pesticides on bird wildlife include death from direct exposure or secondary poisonings from consuming contaminated prey; reduced survival, growth, and reproductive rates from exposure to sublethal dosages; and habitat reduction through elimination of food sources and refuges. Pesticides have many other effects on the environment, including: mammal, fish, and bee kills; surface and groundwater contamination; soil and air contamination; and residue contamination of animal and crop products (Pimentel et al. 1998). In South Asia, pest and disease vectors of eggplant, tomato, and legumes, notably eggplant fruit and shoot borer, cotton bollworm, root knot nematode, white fly, and legume pod borer, have been identified as the major targets of pesticide use and abuse with frequent and excessive applications of pesticide. However, eggplant fruit and shoot borer pheromone traps and net houses developed by the World Vegetable Center (formerly known as Asian Vegetable Research and Development Center (AVRDC)) have helped reduce pesticide application significantly. The promotion of integrated and biological pest control is expanding worldwide. The use of improved vegetable cultivars with resistance or tolerance to pathogens and pests can also contribute to the reduction of pesticide applications and pesticide residues (Dias and Ryder 2011). C. Vegetable Breeding The genetic improvement of vegetables through breeding has to address and satisfy the needs of both consumers and growers (Dias and Ryder 2011). The general objectives for growers are good yield, disease and pest resistance, uniformity, and tolerance to abiotic stresses. Objectives for consumers are quality, appearance, shelf life, taste, and nutritional value. Quality in vegetable crops, in contrast to field crops, is

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often more important than yield. For growers to survive, cultivars must be accepted by the market. Thus, color, appearance, taste, and shape are often more important than productivity (Dias and Ryder 2011). Since the early days of the 20th century, traditional breeding for disease resistance in vegetables has been a major method for controlling plant diseases. Cultivars that are resistant or tolerant to one or a few specific pathogens are already available for many vegetable crops. Resistant hybrids with multiple resistances to several pathogens exist and are currently used in vegetable production. Few vegetable cultivars are resistant to insects. Furthermore, resistance may be unstable due to genetic variants of the insect that are able to overcome that source of resistance. Insects, including aphids, whiteflies, thrips, and leafhoppers, are also very important in vegetables because they vector many viruses. Viruses can substantially reduce production and quality and are becoming increasingly problematic worldwide due to the absence of virus-resistant germplasm for many important vegetable crops. Aphid-vectored viruses are particularly problematic because many are transmitted in a noncirculative and nonpersistent manner (Zitter et al. 1996; Gonsalves 1998). This means that a very short time—that is, a few seconds or minutes—is sufficient for aphids to acquire virus particles when probing infected plants. A similarly short period is enough for aphids to release virus particles when probing healthy plants. The injury caused by aphids is often not from direct feeding damage but from their ability to allow virus to enter the plant and initiate the infection. The economic return of investment in breeding for disease and pest resistance may be low because it is dispersed among many different vegetable crop types. Also, resistant cultivars compete directly with nonresistant ones that may still be used by growers with minimum problems. Therefore, disease resistance is most important when the disease is a limiting factor in production and is especially important for many virus diseases. The high interest in, and the increasing present demand for breeding for disease and pest resistance, is related to a generalized interest in releasing ‘‘environmentally friendly’’ vegetable cultivars requiring sparse or no use of pesticides. Breeding for postharvest traits, mainly transport quality, shelf life, and cosmetic problems, is of increasing importance in vegetables (Dias and Ryder 2011). Vegetable products with good transport quality, better shelf life, and good appearance will be preferred by traders and by consumers. Since vegetables are rich in vitamins, minerals, and other micronutrients and therefore are vital for health, breeding objectives should include improving their nutritional value (Dias and Ryder 2011). Historically vegetable breeders have applied selection pressure to traits

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related to agronomic performance, particularly yield and quality, because these are the traits important to the producers. Growers have seldom been recompensed for nutritional factors, so there have been no economic incentives to provide significant attention to these traits. However, consumers are becoming more aware of these traits. Genetic improvement to increase levels of specific micronutrients is complex because often there is a large environmental effect when the component is present in tiny amounts. Success in vegetable breeding for higher vitamin and mineral content must consider not only substance concentration but also organic components in plants that can either reduce or increase bioavailability (Frossard et al. 2000). Enhanced nutritional content would add value for poor, malnourished populations. Breeding for provitamin A carotenoids, iron, and zinc is of keen interest as a biofortification strategy to alleviate nutrient deficiencies in developing countries (Khush 2002; King 2002; Carvalho et al. 2006; Graham et al. 2007; Hotz and McClafferty 2007). A vegetable, in order to have impact for its nutrient content, must be appealing to consumers (Dias and Ryder 2011). Sensory appeal, including color, is an attribute important to consumers. Breeding to increase consumer appeal by improving convenience and the quality factors of a moderately nutritious crop often can be a more effective approach to increase intake of shortfall nutrients (Simon et al., 2009). Conventional plant breeding that utilizes nontransgenic approaches will remain the backbone of vegetable genetic improvement strategies. However, transgenic crop cultivars should not be excluded as products capable of contributing to more nutritious and healthy food. Although transgenic plant breeding was originally used for field crops, genetic engineering has the potential to address some of the most challenging biotic and abiotic constraints faced by vegetable farmers worldwide, challenges that are not easily addressed through conventional vegetable breeding alone. A successful application of biotechnology has been the development of vegetable cultivars that resist insect-transmitted viruses as well as cultivars that directly resist insect feeding or development. Genetic transformation can also add an economically valuable trait while maintaining other desirable characteristics of the host cultivar: for example, enhanced product quality or micronutrients can be added to a well-adapted cultivar that already yields well under local conditions (Ortiz and Smale 2007). This feature is particularly attractive for semicommercial, smallholder vegetable growers in nonindustrialized agriculture, growers who are more likely to consume as well as sell their farm products. However, transgenic cultivars will have one or a few exogenous genes whereas the background genotype will be still the product of nontransgenic (or conventional) crop breeding. One should

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follow a pragmatic approach when deciding whether to engage in transgenic plant breeding. D. Genetic Engineering Many crops have been genetically modified to include resistance to insects, plant pathogens (including viruses), and herbicides and for improved features, such as slow ripening, higher nutritional status, seedless fruit, and increased sweetness. Transgenic crops, commonly referred to as genetically modified (GM), crops enable breeders to bring favorable genes, often previously inaccessible, into already elite cultivars, improving their value considerably and offer unique opportunities for controlling insects and pathogens. Vegetables growers in the United States have benefited from having GM squash (Cucubita pepo) cultivars resistant to Zucchini yellow mosaic virus (ZYMV), Watermelon mosaic virus (WMV), and Cucumber mosaic virus (CMV). These were deregulated and commercialized in 1996 (Medley 1994; Tricoli et al. 1995; Acord 1996). Bt-sweet corn (Zea mays) has proven effective for control of some lepidopteran species and continues to be accepted in the fresh market in the United States, and Bt-fresh-market hybrids are released each year. In India, genetically transformed Bt-eggplant (Solanum melongena) could be introduced (by Malarashtra Hybrid Seeds Company Limited, Mahyco) in order to reduce pesticide use. Biotechnology products will be successful if clear advantages and safety are demonstrated to consumers. However, countries vary in their market standards of acceptance of GM products. Although GM cultivars have proven to be a powerful tool for pathogen and pest management, and their use has been accompanied by dramatic economic and environmental benefits (Brookes and Barfoot 2009), many countries of the world are still engaged in discussions about potential negative impacts of these crops on the environment, nontarget organisms, food safety, the unintentional spread of transgenic traits into conventionally bred crop or landrace gene pools of the same species particularly in centers of crop diversity or origin, and questions of seed ownership. Fear about potential negative effects of GM crops has led to the implementation of very stringent regulatory systems in several countries and regulations that are far more restrictive for GM crops than for other agricultural technologies (Ortiz and Smale 2007). Consumer antagonism has precluded many farmers and consumers from sharing the benefits that these crops can provide. Critics also claim that adoption of GM crops benefits multinational biotechnology corporations while hurting small farmers because of the additional investments required for

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growing these crops successfully. These concerns are present despite the highly successful and rapid adoption of transgenics in maize, soybeans, and cotton in many countries of the world, not to mention the success of GM squash. As a result of these successes in biotechnology in the form of both breeding aids (marker-assisted selection) and the use of transgenics for herbicide resistance and insect resistance, transgenic programs are under way in many major seed companies and as part of ongoing public research. However, to reach end users, some hurdles should be overcome regarding intellectual property or biosafety guidelines that in some cases may follow an extreme ‘‘precautionary principle’’ approach; developing participatory seed delivery systems; and increasing society’s acceptance of transgenic vegetables. Likewise, when transgenic and conventional crops of the same species coexist in the same locations, appropriate measures should be taken to protect farmers who wish to grow vegetables for transgenic-free markets or avoid transgene flow to other crop genetic resources. Ortiz and Smale (2007) point out that local knowledge of growers will be needed to avoid such gene flow to hamper the efforts for supplying distinct cultivars to the marketplace. There are additional special issues regarding vegetables, which are considered minor crops and traditionally have had fewer resources channeled to them than field crops. While it is becoming less expensive to create GM crops for pest management, developing a marketable product and a regulatory package remains costly. Development and regulatory costs can be recouped more readily if the product is grown on an extensive area, as would be done with field crops, but which is not generally the case for individual vegetable crops. For example, the large agricultural biotechnology companies/corporations have for the most part abandoned the development of GM vegetable crops because of the high costs associated with product development and deregulation. For vegetables, there are many cultivars of the same crop, and the expected life of a particular cultivar can be quite limited. Introducing a GM trait into a breeding program can be complicated and cost prohibitive, especially in crops where backcrossing is difficult or impossible (e.g., potato). In most countries, deregulation of a GM trait is event specific. For many vegetable crops, it is not possible to develop a single GM event that can be converted into many different cultivars of a single or closely related group of vegetable species via conventional breeding. For example, Brassica contains about 40 closely related commercialized crops, including cabbage (B. oleracea var. capitata), cauliflower (B. oleracea var. botrytis), broccoli (B. oleracea var. italica), Brussels sprouts (B. oleracea var. gemmifera), turnip (B. rapa var. rapa), broccoletto (B. rapa ssp. utilis), Chinese cabbage (B. rapa ssp. pekinensis),

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pak-choy (B. rapa ssp. chinensis), choy-sum (B. rapa ssp. parachinensis), swede or rutabaga (B. napus ssp. napobrassica), vegetable rape (B. napus ssp. napus), and various mustards (B. juncea, B. carinata and B. nigra) (Kays and Dias 1995, 1996). No single parent exists that can be used to backcross the transgene into the many different types of Brassica botanical varieties and subspecies. Individual events would have to be developed for many of the crop types, and deregulation of more than one event for a single protein is problematic for most business models. Because of the regulatory costs currently involved with GM vegetable crops, it is difficult for either the public or private sector to develop novel products specifically for small vegetable markets, including specialty vegetable crops in the developed and developing world and almost any crop in countries with relatively small agricultural sectors. For the few transgenic vegetable crops that are being developed, novel or unconventional strategies have been employed to bring the crops to market based generally on private and public partnerships, in which the private sector would focus on selling hybrids to higher-end producers while the public sector would focus on low-resource growers. The large-scale cultivation of plants expressing viral and bacterial genes could lead to some adverse ecological consequences. The most significant risk is the potential for gene transfer of disease resistance from cultivated crops to weed relatives. Virus-resistant crops may also lead to new viruses through an exchange of genetic material or recombination between RNA virus genomes. Recombination between RNA virus genomes requires infection of the same host cell with two or more viruses. Several authors have pointed out that recombination could also occur in genetically engineered plants expressing viral sequences of infection with a single virus and that large-scale cultivation of such crops could lead to increased possibilities of combinations (Hull 1990; de Zoeten 1991; Palukaitis 1991; Tepfer 1993). E. Food Safety Food safety requires that diets are healthy and that foods are not toxic or cause health problems. Transgenic crops must pass a rigorous assessment based on scientific data of any potential risks. The objective of this appraisal is to determine whether the transgenic crop is as safe as its conventional counterpart before transgenic modification. For this purpose, scientific data are provided to be reasonably confident that it will not damage the health of consumers. The World Health Organization (WHO 2002), the FAO of the United Nations (FAO 2000), the Royal

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Society of London, the U.S. National Academy of Sciences, the Brazilian Academy of Sciences, the Chinese Academy of Sciences, the Indian National Science Academy, the Mexican Academy of Sciences and the Third World Academy of Sciences (2000), the American College of Nutrition (Chassy 2002), the Society of Toxicology (2002), the British Medical Association (2004), and the Union of German Academies of Sciences and Humanities (2006), among others, have stated that GM crops approved for commercialization, do not pose more risk to human health than conventional crops, and they should be considered as safe as conventional ones. The world has witnessed a steady increase of transgenic crop area in the last 15 years. The potential impacts on human and animal health have been subject of extensive research, and no evidence has been found against transgenic crops. Some people, however, continue to argue the potential long-term risks but without indicating what those risks may be. The Federal Office of Consumer Protection and Food Safety of Germany and partners (2009) issued the report ‘‘Biological and Ecological Evaluation towards Long-term Effects’’ (also known as the BEETLE) with the aim of providing scientific data to the European Commission. The BEETLE report reviewed in excess of 100 publications and consulted 52 experts in health issues to assess the possible long-term effect of GM crops on the health of consumers and the environment. This report concluded that so far no adverse effects to human health from eating GM food have been found. The report further stated that although unexpected negative effects are known in conventional crops, none has yet been detected in GM crops. The report concludes that there is a negligible probability for adverse effects to consumers’ health in the long term. F. ‘‘Super-Weeds’’ Another main concern of transgenic crops is the unintentional spread of transgenic traits into weedy species (Jørgensen and Andersen 1994). There are examples of transgene escape and some evidence for selective advantage of herbicide resistance picked up by weeds (Hansen et al. 2003; Stewart et al. 2003). The risk of herbicideresistant genes from a transgenic crop cultivar being transferred to weed relatives has been demonstrated in field crops such as canola/ oilseed rape (Brown and Brown 1996; Mikkelsen et al. 1996) and sugar beet (Boudry et al. 1994). However, its probability is likely to vary widely among vegetables, depending on whether crossable wild relatives are likely to be in their immediate production area or not.

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Furthermore, the risk of herbicide-resistant genes in vegetables is globaly lower than in field crops because many vegetables are consumed in the vegetative stage. Rose et al. (2009) has demonstrated that a ‘‘transgenic mitigation strategy’’ may impart a negative genetic load to hybrids ensuing from crosses between the weed field mustard and oilseed rape crop. The transgenic mitigation measure was a fitness-mitigating dwarfing gene that is beneficial for crops but deleterious for weeds (i.e., the hybrid weed is dwarfed due to this mitigation gene and is therefore outcompeted by its nontransgenic counterparts). This finding challenges the view that a transgenic plant might always endow a wild relative with a so-called fitness gene, making it harder and giving it the potential to become a ‘‘super-weed.’’ Furthermore, Palaudelm as et al. (2009) found that transgenic maize volunteers had low plant vigor, rarely had cobs, and produced pollen that cross-fertilized neighbor plants only at low levels (0.16% in the worst-case scenario, which was below the Regulation EC 1830/2003 establishing the adventitious threshold of 0.9% for coexistence). Nonetheless, transgene flow raises a new set of ecological and economic issues for scientists and policy makers to consider for transgene containment.

III. CASE STUDIES While transgenic vegetables have not been widely deployed for use in agriculture production systems to date, extensive research evaluating their potential usefulness for a wide range of traits valuable to both farmers and consumers has been published. In most examples, the transgenic traits incorporated are either beyond the range of genetic variation available in germplasm for classical plant breeding, or they are traits absent in all known intercrossable germplasm. A. Tomato Tomato is the second most consumed and widely grown vegetable in the world after potato and is grown on about 4.5 million ha worldwide, producing 130 million t globally in 2007 (FAO 2009). Tomato is popular fresh and in many processed forms (e.g., ketchup, sun-dried, canned whole or in pieces, puree, sauce, soup, juice, or dried). Tomato is an important source of vitamins and minerals in diets. Tomatoes are also rich in an antioxidant called lycopene, a carotenoid that has been found to protect cells from oxidants that have been linked to cancer

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(Gerster 1997). In laboratory tests, lycopene was found to be twice as powerful as b-carotene in neutralizing free radicals. Lycopene has been linked to risk reduction for a number of cancer types, including prostate, lung and stomach, pancreatic, cervical, colorectal, oral, and esophageal cancers (Giovannucci 1999; Rao and Agarwal 2000). In addition to its antioxidant and anticarcinogenic properties, lycopene shows an array of biological effects including cardioprotective, anti-inflammatory, and antimutagenic activities. 1. Fruit Ripening. The first commercially grown GM crop was Flavr Savr tomato, which was released by Calgene in 1994. This tomato contains an antisense version of the poligalacturonase (PG) gene that was the result of many years of research on several genes involved in fruit development and tomato ripening. These genes were identified, cloned, and characterized for developing GM tomato cultivars (Kramer and Redenbaugh 1994). However, this GM cultivar failed in the market since the cultivar was considered inferior by growers, and was rapidly withdrawn from the market. An important lesson was learned by plant genetic engineers: the importance of cooperation with breeders. Further research has been conducted to manipulate fruit ripening, texture, and nutritional quality using transgenic approaches (Table 4.1). Many of these genes targeted ethylene, a simple gaseous plant hormone that has profound effects on plant growth and development. Ethylene’s role in fruit ripening has been genetically established (Theologis 1992). Enzymes that regulate ethylene biosynthesis in plants are: S-adenosylmethionine (SAM) synthase, 1-aminocyclopropane-1-carboxylate (ACC) synthase, and ACC oxidase. The genes encoding these enzymes (Hamilton et al. 1990; Oeller et al. 1991) as well as those that metabolize SAM or ACC (Klee et al. 1991; Good et al. 1994) have been targeted in order to manipulate ethylene biosynthesis and thereby regulate fruit ripening. It has been clearly demonstrated that modulation of ethylene biosynthesis using genetic engineering can yield tomato fruits with predictable ripening characteristics. However, ripening of tomato has been shown possible by the introduction of antiripening genes rin and nor in heterozygous form, and these genes have been incorporated in many fresh and processing tomatoes. Meli et al. (2010) has demonstrated that transgenic tomato can enhance fruit shelf life by suppressing N-glycan’s (precursors of glycosylation or glycoprotein proteolysis) processing enzymes. Their transgenic tomatoes had
2.5- and
2-fold firmer fruits in the a-Man and b-Hex RNAilines RNAilines, respectively, and
30 days of enhanced shelf life. The authors further suggest that genetic manipulation of

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Apple

Escherichia coli E. coli Tomato

Tomato

ACC oxidase

b-glucuronidase

Deoxyhypusine synthase

Tomato

Tomato

Polygalacturonase and expansin

Expansin and polygalacturonase

Fruit texture Pectin methylesterase

Tomato

Tomato

Ripening/ethylene ACC synthase

b-glucuronidase ACC oxidase

Gene source

Increased juice viscosity and serum viscosity; higher total solids, decreased pectin hydrolysis in cv. Ohio 8245 Firmer fruits, better in storage, increase juice viscosity in cv. Ailsa Craig

Impaired ethylene production, fruit ripening, and extended shelf life in tomato VF36 Reduced ethylene production in tomato UC82B Decrease in fruit softening. Identification of ERE and AUXre Effect on softening Prolonged shelf life for more than 120 days in cv. Heinz 906 Delayed postharvest softening and senescence. Pleiotropic effects on growth and development: male sterility, larger and thicker leaves, higher activity of photosystem II, starch deposition in the stems in tomato UCT5.

Phenotype

CaMV 35S:LePG antisense CaMV 35S:LeEXP1 sense suppression CaMV 35S:LeExp1 and Increased juice viscosity, consistency, FMV:LePG and pectin molecular size in tomatoes T52 and T53

CaMV 35S:PME2 antisense

CaMV 35S:AP4 antisense Pp-ACO1:GUS Pp-ACO2:GUS PpACO1:GUS D35S w:ACC oxidase (RNAi) CaMV 35S:DHS antisense

CaMV 35S:LeACC2 antisense

Promoter:gene

Transgenic tomato to improve ripening, fruit texture, and nutritional quality.

Protein/enzyme

Table 4.1.

Kalamaki et al. 2003

Powell et al. 2003

Thakur et al. 1996

Wang et al. 2005

Moon and Callahan 2004 Xiong et al. 2005

Rasori et al. 2003

Bolitho et al. 1997

Oeller et al. 1991

References

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P35S:gdhA

FMV:LeAADC1A FMV:LeAADC2 antisense

Erwinia uredovora

Yeast

Thaumatococcus daniellii

Aspergillus nidulans

Tomato

Phytoene synthase

SAM decarboxylase

Thaumatin

NADP-dependent glutamate dehydrogenase Amino acid decarboxylases

CaMV 35S: thaumatin

E8:SAMDC

Tomato PG Fruit specific:CrtB

CaMV 35S:crtl

Erwinia uredovora

Phytoene desaturase (carotenoid)

Tomato Pds:b-Lcy

Arabidopsis

Nutritional quality Lycopene b-cyclase

Changes in flavor and aroma volatiles in tomato M82

Sense: increase in b-carotene Antisense: decrease in b-Lcy expression with slight increase in lycopene in cv. Money Maker Increased b-carotene with up to 45% of the total carotenoids in cv. Ailsa Craig Increased fruit carotenoids: phytoene, lycopene, b-carotene, and lutein in cv. Ailsa Craig Accumulation of polyamines: spermidine and spermine. High lycopene, improved juice quality, and longer vine life in cv. Ohio 8245 Increased fruit sweetness and a liquorices aftertaste lasting for a few minutes Higher total amino acids including glutamate in mini tomato Tieman et al. 2006

Kisaka and Kida 2003

Bartoszewski et al. 2003

Mehta et al. 2002

Fraser et al. 2002

Romer et al. 2000

Rosati et al. 2000

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N-glycan processing may reduce fruit softening and extending shelf life without any negative effect on phenotype, including yield. Textural properties of tomato fruits are important contributors to the overall quality of fresh-market tomatoes and to the properties of products processed from tomatoes. Because cell wall disassembly in ripening fruit contributes to fruit texture, modification of cell wall proteins and enzymatic activity during ripening can impact cell wall polysaccharide metabolism and influence texture. Transgenic tomato lines with altered expression of single or multiple genes have been developed. Deoxyhypusine synthase (DHS) mediates the two sequential enzymatic reactions that activate eukaryotic translation initiation factor-5A (eif-5A) by converting Lys into deoxyhypusine. In this regard, Wang et al. (2005) showed that the antisense suppression of DHS delays fruit softening and alters growth and development in transgenic tomato. 2. Fruit Quality. Carotenoids. Tomato fruit and its processed products are the principal dietary sources of carotenoids such as lycopene. Lycopene is a potent antioxidant with the potential to prevent epithelial cancers and improve human health. Therefore, there is considerable interest in elevating the levels of carotenoids in tomato fruit by genetic manipulation and thereby improving the nutritional quality of the crop. Folate biofortification of fruit will be another target for transgenic tomato breeding. Folate deficiency—regarded as a global health problem—causes neural tube defects and other human diseases. Foliates are synthesized from pteridine, p-aminobenzoate (PABA), and glutamate precursos. Dıaz de la Garza et al. (2004, 2007) developed trangenic tomatoes by engineering fruit-specific overexpression of GTP cyclohydrolase I, which catalyzes the first step of pteridine synthesis, and amynodeoxychorismate synthase, which catalyzes the first step of PABA synthesis. Vine-ripened fruits contained on average 25-fold more folate than controls by combining PABA- and pteridine-overproduction traits through crossbreeding of transgenic tomato plants. The achieved folate level provides a complete adult daily requirement with less than one standard serving. Flavonoids. Flavonoids are polyphenols whose dietary intake has the potential to prevent chronic diseases. Schijlen et al. (2006) introduced heterologous, flavonoid pathway genes—stilbene synthase, chalcone synthase, chalcone reductase, chalcone isomerase, and flavone synthase—to produce novel flavonoids in tomato fruit. These novel flavonoids -flavones and flavonols- increased threefold, mostly in the peel, which had higher total antioxidant capacity. These findings add

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further support to the potential of engineering tomato fruit for accumulation of high levels of beneficial nutrients. The first successful study conducted to engineer the taste of tomato fruit involved transformation of tomato with the thaumatin gene from the African plant katemfe (Thaumatococcus daniellii) (Bartoszewski et al. 2003). Thaumatin is a sweet-tasting protein. Fruit from T2 transgenic plants tasted sweeter than the control plants, leaving a unique and sweet-specific aftertaste. 3. Insect Resistance. Insect infestation causes significant losses in tomato, and classical breeding has had limited success in improving host plant resistance. It is therefore likely that genetic engineering approaches have the potential to substantially reduce pesticide use in the tomato crop. Likewise, much more reduction in the overall pesticide use is anticipated by engineering tomatoes that resist various fungal, bacterial, and viral pathogens. The increasing importance of integrated pathogen and pest management, largely as a result of concerns over environmental quality and food safety, together with the failure of conventional pesticides due to the development of increasing number of pathogens and insecticide-resistant species has provided a major niche for deploying transgenic tomatoes. Table 4.2 lists potential genes for host plant resistance to insects, fungi, bacteria, and viruses. Transgenic tomato plants transformed with a crystal d-endotoxin gene encoding a coleopteran insect–specific toxin from Bacillus thuringiensis subsp. tenebrionis (Btt) were shown to express a 74kD protein that crossreacted with Bt toxin antibodies. These transgenic plants exhibited a significant insecticidal activity when challenged with Colorado potato beetle larvae (Leptinotarsa decemlineata) (Rhim et al. 1995). A synthetic cry1Ac Bt gene was introduced into tomato plants using Agrobacteriummediated transformation, and high levels of Bt expression in the leaves of transgenic plants were ascertained by enzyme-linked immune sorbent assay. The transformed plant leaves and fruits were found resistant to the larvae of tomato fruit borer (Helicoverpa armigera syn. Heliotis armigera). A limited field trial of the T1 generation showed that transgenic host plant resistance works successfully against H. armigera (Mandaokar et al. 2000). Chen et al. (2005) showed that the jasmonateinducible proteins arginase and threonine deaminase act in the tobacco hornworm (Manduca sexta) midgut to catabolize the essential amino acids arginine and threonine, respectively. Transgenic plants overexpressing arginase were more resistant to M. sexta larvae, and this effect correlated with reduced levels of midgut arginine. Abdeen et al. (2005) overexpressed two different potato protease inhibitors (the serine-proteinase inhibitor PI-II and the carboxypeptidase inhibitor [PCI])

170

Tomato

Tomato

Nucleotide-binding, leucine-rich repeat PR protein

CaMV 35S:Mi-1.2

CaMV 35S:TCI21

CP:win6

Poplar

Chymotrypsin inhibitor 21 (TCI21)

StLS1:PI-II and rbcs-1A:PCI

Potato

Serine-proteinase (PI-II), carboxypeptidase (PCI) inhibitors Chitinase (Win6)

CaMV 35S:ARG2 overexpression

CaMV 35S:cry1Ac

CaMV 35S:Btt

Promoter:gene

Tomato

Bacillus thuringiensis subsp. tenebrionis (Btt) Bacillus thuringiensis (Bt)

Gene source

Arginase

Cry1Ac

Insect resistance Bt toxin

Gene product

Table 4.2. Transgenic tomato for insect, fungal, bacterial, and virus resistance.

Significant insecticidal activity with Colorado potato beetle larvae (Leptinotarsa decemlineata) High level of protection of transgenic leaves and fruits against the larvae of tomato fruit borer (Helicoverpa armigera) Limited field trial of T1 generation confirmed the high levels of insect protection Increased resistance to tobacco hornworm (Manduca sexta) larvae Resistance to Heliothis obsoleta and Liriomyza trifolii larvae Inhibition of development of Colorado potato beetle Increased mortality and delayed growth of Egyptian cotton worm (Spodoptera littoralis) Resistance to root-knot nematodes (Meloidogyne spp.), potato aphid (Macrosiphum euphorbiae), sweet potato whitefly (Bemisia tabaci)

Phenotype

Goggin et al. 2006

Lawrence and Novak 2006 Liso´n et al., 2006

Abdeen et al. 2005

Chen et al. 2005

Mandaokar et al. 2000

Rhim et al. 1995

References

171

Arabidopsis

Arabidopsis thionin (Thi2.1)

Bacterial resistance Serine/threonine protein kinase

Tomato

Ribosomal inactivating Iris, maize, Mirabilis protein (I-RIP), b-glucanase jalapa (M-GLU) and antimicrobial peptide (Mj-AMP1)

Arabidopsis

Grapevine (Vitis vinifera) Wild tomato (Solanum chilense) Collybia velutipes

Nonexpresser of PR genes

Oxalate decarboxylase

Fungal resistance Stilbene synthase (phytoalexin) Endochitinase

CaMV 35S:Pto overexpression

CaMV 35S:I-RIP, MGLU, and Mj-AMP1

Fruit inactive RB7: Thi2.1

CaMV 35S:NPR1

CaMV 35S:OXDC

CaMV 35S:vst1 and vst2 CaMV 35S:pcht28

Resistance to Xanthomonas campestris pv. Vesicatoria, Cladosporium fulvum

Resistance to Sclerotinia sclerotiorum Innate ToMV resistance, significant level of resistance to bacterial wilt (Ralstonia solanacearum) and fusarium wilt (Fusarium oxysporum), and moderate degree of resistance to gray leaf spot (Stemphylium botryosum f. sp. lycopersici) and bacterial spot (Xanthomonas campestris pv. vesicatoria) Resistance to bacterial wilt Ralstonia solanacearum and fusarium wilt Enhance resistance to Alternaria solani in M-GLU or Mj-AMP1 transgenic but not in I-RIP

Increased resistance to Phytophthora infestans Tolerance to Verticillium dahliae races

(continued)

Tang et al. 1999

Schaefer et al. 2005

Chan et al. 2005

Lin et al. 2004

Kesarwani et al. 2000

Tabaeizadeh et al. 1999

Thomzik et al. 1997

172

ToMV

Giant silk moth (Hyalophora cecropia)

Cationic lytic peptide cecropin B (CB)

Viral resistance Chimeric Tomato mosaic virus (ToMV) coat protein

Pepper

Sweet pepper ferredoxin-I protein (PFLP)

CaMV 35S:ToMV-CP

pBI121-spCB:CB

:PFLP

CaMV 35S:CaPIF1 overexpression

Fruit inactive RB7: Thi2.1

Arabidopsis

Pepper (Capsicum annuum)

ECaMV 35S:MSI-99

Synthetic

Cys-2/His-2 zinc finger protein-TF

:lactoferrin (LF)

Human

Glycoprotein antibacterial protein Magainin-antimicrobial peptide Arabidopsis thionin (Thi2.1)

Promoter:gene

Gene source

Gene product

Table 4.2 (Continued )

Resistance to ToMV; a specific attenuated ToMV mutant strain L21 was used to assay the resistance

Partial resistance to bacterial wilt R. solanacearum Resistance to bacterial speck (Pseudomonas syringae) Resistance to bacterial wilt R. solanacearum and fusarium wilt (F. oxysporum) Tolerance to cold stress and to the bacterial pathogen P. syringae in tomato DC 3000 Selected T2 transgenic lines (24-18-7 and 26-2-1a) which show high expression of PFLP in root tissue were resistant to bacterial wilt Ralstonia solanacearum; transgenic line 24-18-7 was also resistant to Erwinia carotovora subsp. carotovora Significant resistance to bacterial wilt (R. solanacearum) and bacterial spot (X. campestris pv. vesicatoria)

Phenotype

Motoyoshi 1993; Motoyoshi and Ugaki 1993

Jan et al. 2010

Huang et al. 2007

Seong et al. 2007

Chan et al. 2005

Alan et al. 2004

Lee et al. 2002

References

173

TYLCV Cucumber mosaic virus (CMV)

CMV-WL, CMV (subgroup II)

Tobacco

Tomato

CMV

TYLCV

Capsid protein CMV satellite RNA

Coat protein

Nucleoprotein

TSWV nucleoprotein (NP) gene

Capsid protein

rep protein (T-Rep)

Enhanced CaMV 35S: Cl Sense and antisens

: TSWV NP

:N POCA 28 vector

CaMV 35S:CP

CaMV 35S:V1 CaMV 35S:SCARNA 5

Delayed disease symptoms Tolerance in transgenics, which produced mature unit-length satellite RNA after CMV infection Resistance to infection by CMV-WL and CMV-China, resistance to isolates from both subgroups of CMV A hypersensitive response and components necessary for N-mediated resistance are conserved in tomato High levels of resistance to Tomato spotted wilt virus (TSWV) in hybrids derived from the parental transgenic tomato lines in field trials under high virus pressure Reduced infection of CMV under natural conditions and generally remained free of symptoms Sense: Tomato yellow leaf curl virus T-Rep accumulation is required for resistance Cross between sense and antisense produced normal phenotype but was susceptible (continued)

Brunetti et al. 1997

Murphy et al. 1997

Haan et al. 1996

Whitham et al. 1996

Xue et al. 1994

Kunik et al. 1994 McGarvey et al. 1994

174

CMV-D strain and Italian CMV isolates

Physalis mottle tymovirus (PhMV) CMV-GT (subgroupII)

Coat protein

Coat protein

Arabidopsis

TLCV

Nonexpresser of PR genes

Coat protein

Truncate replicate gene encoded by RNA2

Gene source

Gene product

Table 4.2 (Continued )

Coat protein gene of Tomato leaf curl virus (TLCV)

CaMV 35S:NPR1

: truncate replicase gene

CaMV 35S:CP

FWMV:CMV-22, FWMV:CMV-PG

Promoter:gene Resistance to CMV infection in growth chamber but resistance less effective on field Partial resistance to Physalis mottle tymovirus (PhMV) Several resistant lines of the T1 generation were resistant to CMV stain Ta-8 (subgroup II) Broad-spectrum resistance toward ToMV, BW, FW, GLS, and BS Variable resistance or tolerance to TLCV

Phenotype

Raj et al. 2005

Lin et al. 2004

Nunome et al. 2002

Vidya et al. 2000

Kaniewski et al. 1999

References

4. TRANSGENIC VEGETABLE CROPS

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in tomato plants. Leaf-specific overexpression of the PI-II and PCI resulted in increased resistance to corn earworm (Heliothis obsoleta) and to American serpentine leafminer (Liriomyza trifolii) larvae in homozygous tomato lines expressing high levels (>1% of the total soluble proteins) of the transgenes. Lawrence and Novak (2006) used a recombinant Potato virus X, carrying a gene for chitinase, WIN6, to infect tomato plants. The leaves from infected plants were tested for insecticidal properties on Colorado potato beetle. Less than half of Colorado potato beetle neonates feeding on leaves containing >0.3% w/w WIN6 developed to second instar compared to 93% on control uninfected leaves. Goggin et al. (2006) showed that transformation of the susceptible ‘Moneymaker’ tomato with the Mi-1.2 gene (NB-LRR class) resulted in resistance to nematodes and aphids. The Mi-1.2 locus confers resistance against root-knot nematodes (Meloidogyne spp.), the potato aphid (Macrosiphum euphorbiae), and the sweet potato whitefly (Bemisia tabaci). A proteinaceous aspartic proteinase inhibitor, designated as tomato chymotrypsin inhibitor 21 (TCI21), was also expressed in tomato and found to increase mortality and delay growth of Egyptian cotton worm (Spodoptera littoralis) (Lison et al. 2006). More recently, Chen et al. (2007) indicated that the root-knot nematode resistance gene CaMi from hot pepper (Capsicum annuum) confers inheritable host plant resistance to this nematode in transgenic tomato. 4. Fungal Resistance. Thomzik et al. (1997) transformed tomato with two stilbene synthase genes from grapevine (Vitis vinifera). They characterized the transgenic plants for stable integration and expression of the transgene and host plant resistance in the transgenic tomato to downy mildew (Phytophthora infestans). Upon fungal inoculation, transgenic plants accumulated the phytoalexin transresveratrol, the product of stilbene synthase, and exhibited increased resistance to P. infestans. Inoculation of transgenic tomato with Botrytis cinerea (botrytis blight or gray mold) and Alternaria solani (early blight of tomatoes) also caused accumulation of resveratrol, but plants did not show significant resistance to these fungi. Tabaeizadeh et al. (1999) observed the effect of constitutive expresion of an acidic endochitinase gene, pcht28, from Lycopersicon chilense for resistance against Verticillium dahliae (verticillium wilt). The R1 plants were tested in the greenhouse for tolerance to V. dahliae race 1, 2 whereas R2 plants tested against race 2 showed a significantly higher level of resistance to the fungi than the nontransgenic plants. The resistance was confirmed by foliar disease symptoms and vascular discoloration index. Likewise, Kesarwani et al. (2000) were able to overexpress oxalate decarboxylase

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from Collybia velutipes in transgenic tobacco and tomato, both of which developed resistance to fungal infection. These transgenic tobacco and tomato plants showed remarkable resistance to phytopathogenic fungus Sclerotinia sclerotiorum (sclerotinia stem rot or white mold), which utilizes oxalic acid during infestation. Lin et al. (2004) introduced the Arabidopsis NPR1 (nonexpresser of PR genes) gene into a tomato cultivar, which possesses heat tolerance and resistance to Tomato mosaic virus (ToMV). The transgenic lines expressing NPR1 showed normal morphology and horticultural traits for at least four generations. Host plant resistance screening against eight important tropical pathogens revealed that, in addition to the innate ToMV resistance, the tested transgenic lines conferred significant levels of enhanced resistance to bacterial wilt (Ralstonia solanacearum) and fusarium wilt (Fusarium oxysporum), and moderate degree of enhanced resistance to gray leaf spot (Stemphylium botryosum f. sp. lycopersici) and bacterial spot (Xanthomonas campestris pv. vesicatoria). Transgenic lines that accumulated higher levels of NPR1 proteins exhibited higher levels and a broader spectrum of enhanced resistance to these pathogens, and their enhanced host plant resistance was stably inherited. The spectrum and degree of these NPR1-transgenic lines are more significant than in the transgenic tomatoes bred to date. Hence, these transgenic lines may be further used as tomato stocks, aiming at building up host plant resistance to a broader spectrum of pathogens by transferring these characteristics into tomato cultivars with good agronomic and organoleptic characteristics. The Arabidopsis thionin (Thi2.1) gene was also used by Chan et al. (2005) to genetically engineer enhanced resistance to various pathogens in tomato. A construct was created in which the fruit-inactive promoter RB7 was used to control the expression of the Thi2.1 gene. In transgenic lines containing RB7/Thi2.1, constitutive Thi2.1 expression was detected in roots and a little in leaves, but not in fruits. Host plant resistance assays revealed that the transgenic lines tested showed enhanced resistance to bacterial wilt and fusarium wilt. It was found that progression of bacterial wilt in transgenic lines was delayed by a systemic suppression of bacterial multiplication. Schaefer et al. (2005) introduced genes coding for an iris ribosomal-inactivating protein (I-RIP), a maize b-glucanase (M-GLU), and a Mirabilis jalapa antimicrobial peptide (Mj-AMP1) into tomato. Selected transgenic lines were inoculated with a suspension containing 2–3  104 conidial spores/ml of the fungal pathogen Alternaria solani. Two transgenic lines carrying either M-GLU or Mj-AMP1 transgenes had enhanced resistance to Alternaria solani vis- a-vis the parental control. None of the four lines carrying the I-RIP transgene showed resistance to this pathogen.

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5. Bacterial Resistance. The tomato resistance gene Pto encodes a serine/threonine protein kinase that is postulated to be activated by a physical interaction with the AvrPto protein. In this regard, Tang et al. (1999) showed that transgenic tomato plants exhibited significant host plant resistance to Pseudomonas syringae (bacterial speck) without avrPto and reduced bacterial growth compared to nontransgenic lines. These transgenic plants also showed more resistance to Xanthomonas campestris pv. vesicatoria (bacterial spot) and Cladosporium fulvum (leaf mold of tomato). Similarly, Lin et al. (2004) transformed tomato with the Arabidopsis NPR1 gene. They found that transgenic lines had significant levels of enhanced resistance to bacterial wilt and moderate resistance to bacterial spot (BS). Seong et al. (2007) isolated a pathogenesis-induced factor (CaPIF1) from pepper leaves after infection with the soybean pathogen Xanthomonas axonopodis pv. glycines 8ra. The overexpression of CaPIF1, which encodes a Cys-2/His-2 zinc finger transcription factor, resulted in major transcriptional modulation without exhibiting any visual morphological abnormality. The transgenic plants exhibited tolerance to cold stress and to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000, whose tolerance was correlated with the expression levels of CaPIF1. The CaPIF1, a plant-specific unique Cys2/His-2 transcription factor, seems to regulate directly and indirectly gene expression, thereby leading to enhanced resistance to biotic and abiotic stresses. Huang et al. (2007) demonstrated that expressing sweet pepper ferredoxin-I protein (PFLP) in transgenic tomato plants can enhance resistance to bacterial pathogens that infect leaf tissue. In their study, PFLP was applied to protect tomato cv. Cherry Cln1558a from the root-infecting pathogen Ralstonia solanacearum. Independent R. solanacearum resistant T1 lines were selected and bred to produce homozygous T2 generations. Selected T2 transgenic lines 24-18-7 and 26-2-1a, which showed high expression levels of PFLP in root tissue, were resistant to R. solanacearum. The expansion of R. solanacearum populations in stem tissue of transgenic tomato line 24-18-7 was limited compared with the nontransgenic tomato Cln1558a. Using a detached leaf assay, transgenic line 24-18-7 was also resistant to maceration caused by Erwinia carotovora subsp. carotovora, but it was less apparent in transgenic line 26- 2-1a. The cationic lytic peptide cecropin B (CB), isolated from giant silk moth (Hyalophora cecropia), has been shown to effectively eliminate Gram-negative and some Gram-positive bacteria. Jan et al. (2009) investigated the effect of chemically synthesized CB on plant pathogens. The S50 (peptide concentration causing 50% survival rate of a pathogenic bacterium) of CB against two major pathogens of tomato R. solanacearum and X. campestris pv. vesicatoria were

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529.6 mg/ml and 0.29 mg/ml, respectively. The CB gene was then fused to the secretory signal peptide sequence (sp.) from the barley a-amylase gene, and the new construct, pBI121-spCB, was used for the transformations of tomato. Integration of the CB gene into the tomato genome was confirmed by PCR, and its expression was confirmed by Western blot analyses. In vivo studies of the transgenic tomato demonstrated significant resistance to bacterial wilt and bacterial spot. The levels of CB expressed in transgenic tomato (
0.05 mg in 50 mg leaf) are far smaller than the S50 determined in vitro. CB transgenic tomato could therefore be a new mode of bioprotection against these two tomato pathogens. 6. Viral Resistance. Substantial efforts also have been made to engineer virus resistance in tomato plants. Whitefly-transmitted geminiviruses are widely distributed in tropical and subtropical regions around the world, causing yield losses in tomato and in other important vegetable crops, such as beans, cassava, and pepper. Motoyoshi and Ugaki (1993) reported the transformation (with a chimeric Tobacco mosaic virus [TMV] coat protein gene under the control of the CaMV 35S promoter) of an F1 hybrid between tomato and its wild relative Solanum peruvianum. Transgenic line 8804-150 accumulated 2.5 mg coat protein per gram fresh weight in fully developed fresh leaves and exhibited the strongest resistance to ToMV among the plants examined. The transgenic plants did not show any morphologic or physiologic differences vis-a-vis their nontransgenic control plants. An interspecific F1 tomato hybrid derived from Solanum pennellii that was sensitive to the Tomato yellow leaf curl virus (TYLCV) was also successfully genetically transformed with a TYLCV transgene-encoding capsid protein (V1). The R1 plants inoculated with TYLCV using whiteflies showed delayed disease symptoms and increased recovery from the disease (Kunik et al. 1994). McGarvey et al. (1994) indicated that transgenic R1 tomato plants expressing CMV satellite RNA fused to the GUS gene showed mild disease symptoms in the first two weeks after inoculation with virions of RNA preparations of CMV or Tomato aspermy virus (TAV), which was followed by a decrease in symptoms. Field trials of transgenic tomato plants expressing an ameliorative satellite RNA of CMV exhibited mild or no CMV symptoms and low viral titers relative to nontransformed plants. When infected with CMV, the transgenic lines showed 40% to 84% greater total marketable yield than parent lines. A significant negative correlation between satellite RNA levels and disease severity was found in transgenic lines (Stommel et al. 1998). High levels of resistance to Tomato spotted wilt virus (TSWV) were

4. TRANSGENIC VEGETABLE CROPS

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obtained in an inbred tomato line that was transformed with a DNA construct comprising the TSWV nucleoprotein (NP) gene (Hann et al. 1996). The high levels of resistance were maintained in hybrids derived from the parental transgenic tomato lines. Moreover, the transgenic-derived hybrids remained completely free of TSWV symptoms in field trials under high virus pressure. Xue et al. (1994) also successfully developed transgenic tomato plants expressing a high level of resistance to Cucumber mosaic virus (CMV) strains of subgroup I and subgroup II. These transgenic tomatoes that are resistant to isolates from both subgroups of CMV have practical significance for controlling this serious virus. Transgenic tomato plants exhibiting a broad commercial resistance to CMV infection have been developed by expressing coat protein (CP) genes from the CMV-D strain and two Italian isolates CMV-22 of subgroup I and CMV-PG of subgroup II (Kaniewski et al. 1999). Transgenic plants generated using CP from any of the strains showed broad resistance against CMV strains from both subgroups I and II. These transgenic lines were field-tested to assess the level of resistance and agronomic performance (Tomassoli et al. 1999). The target virus spread naturally by the indigenous aphid populations in multilocation trials in Italy. These trials showed, however, that CMV resistance of the transgenic tomatoes was less effective in the field than what was observed in growth chamber experiments. Transgenic tomato resistant to CMV—through expression of the CP gene—have been released in China (Chen et al. 2003), though limited information is available on their adoption rate. Nunome et al. (2002) also transformed tomato plants with a truncate replicase gene encoded by RNA 2 of CMV strain GT, subgroup II. The truncate replicase gene does not retain a C-terminal region of the gene that contains the GDD amino acid motif and the NTP binding motif. These motifs are considered to correspond to active or recognition domains of RNA-dependent RNA polymerase. Upon transformation with Agrobacterium tumefaciens, 137 individual transgenic lines were obtained. Each transgenic line was evaluated for resistance to CMV strain Ta-8. About 10% of the transgenic lines were highly resistant, and the remaining 90% showed a moderate resistance or were susceptible. The 15 lines were selected as resistant lines. Chenopodium amaranticolor was used to analyze the multiplication of CMV in the symptomless plants. Among the selected lines, three lines did not appear to show any multiplication of CMV in both inoculated and noninoculated leaves. The T1 progeny of the selected lines harbored the transgene according to transgene amplification by PCR and the kanamycin resistance assay. Several resistant lines of the

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T1 generation were resistant to viral inoculation. These resistant lines become suitable breeding lines for resistance to CMV. There is a project on CMV-resistant transgenic tomato in Indonesia and the Philippines (ABSPII 2009) because to date conventional breeding has not been able to develop resistant germplasm. Resource-poor tomato growers in the Philippines will gain significantly if transgenic tomato with resistance to CMV and TYLCV can become available to and adopted by them (Mamaril 2009). In Indonesia, a study has shown that the adoption of a transgenic tomato with resistant to CMV and ToLCV (Tomato leaf curl virus) will have a significant potential economic impact that would increase economic welfare (Ameriana 2009). Transgenic tomato with multiple virus resistance will also reduce the use of insecticides, thereby significantly contributing to maintaining environmental quality and minimizing pesticide residues in tomato products (Ameriana, 2009). Brunetti et al. (1997) had shown that high expression of a truncated version of the Cl gene of TYLCV, which encodes the first 210 amino acids of the multifunctional rep protein, confers resistance to TYLCV in transgenic tomato plants. N genes possess a putative nucleotide binding site and leucine-rich repeats and confer a gene-for-gene resistance against TMV and most other members of the tobamovirus family. Whitham et al. (1996) also genetically transformed tomato with the N gene from tobacco. Tomato transgenics expressing the N gene exhibit a hypersensitive response and effectively restricts TMV to the sites of inoculation, as in tobacco. Transgenic tomato plants expressing the CP gene of Physalis mottle tymovirus (PhMV) showed delay in symptom development indicating partial resistance to the virus (Vidya et al. 2000). 7. Plant Stress. Plants have developed responses to environmental extremes such as drought, salinity, extreme temperatures and hypoxia, which in turn may impact their growth, productivity, and quality. Water availability is expected to be highly sensitive to climate change, and severe water stress conditions will affect crop productivity, particularly that of vegetables (De la Pen˜a and Hughes 2007). Water significantly influences fruit yield and quality of tomato. Drought therefore drastically reduces tomato productivity, and the magnitude of the yield loss will depend on its timing, intensity, and duration. About one-fifth of irrigated agricultural land is impacted by salinity, and it is rapidly expanding due to the increased use of underground water. Tomato, like most other crop plants, is sensitive to salinity (Foolad 2004, 2007). Our limited understanding of the molecular basis regulating salt tolerance in plants has hampered progress in developing

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salt-tolerant crops. Nonetheless, several genes with a potential role in imparting tolerance to salinity stress have been identified. Plants also vary in their responses to temperature extremes. Nonfreezing low temperatures also cause chilling injury while high temperatures impair crop productivity and quality in tomato. Cold damage in tomato plants occurs under temperatures below 6 C. Freezing tolerance of tomato occurs down to to 2 to 3 C whereas extended storage at temperatures below 12 C results in severe chilling injury. Temperatures over 30 C inhibit the synthesis of lycopene and affect the quality of the fruit (Almeida 2006). Furthermore, anaerobiosis occurs during waterlogging, flooding, poor drainage, or even irrigation and causes oxygen deficiency, anoxia with bare minimum oxygen availability, and hypoxia with only some oxygen availability in the rooting zone. Tomato and other plants respond to anaerobiosis in a variety of ways. There has been research on tomato responses to all these abiotic stresses. Plants show an elaborate signaling network that perceives signals from abiotic stresses and modulates the expression of select genes. Significant research advances have been made in understanding these pathways using Arabidopsis thaliana as a model system. Table 4.3 provides some highlights regarding progress on developing tolerance to abiotic stresses in tomato (e.g., to drought, salt, extreme temperatures, and hypoxia). Breeding for tolerance to drought and salt stresses could increase the productivity of tomato in many regions of the world and would help regain more arable land (Table 4.3). For example, the expression of AVP1—a vacuolar H þ pyrophosphatase from A. thaliana—in transgenic tomato led to enhanced performance under soil water deficit due to a strong and large root system allowing better use of limiting water (Park et al. 2005). Hsieh et al. (2002a,b) used CBF1 (C-repeat/dehydrationresponsive element-binding factor 1)/DREB1 genes driven by a strong constitutive 35S Cauliflower mosaic virus promoter to successfully engineer tolerance to chilling, drought, and salt stress in tomato plants showing dwarfism and low fruit and seed set. When the same gene (CBF1) was expressed using an abcisic acid (ABA)/stress-inducible promoter from barley HAV22 gene, the transgenic tomato plants showed enhanced tolerance to chilling, water deficit, and salt stress as compared to untransformed plants (Lee et al. 2003). The use of an inducible promoter eliminated the deleterious effects of the ectopic expression of CBF1 on plant growth and yield. Park et al. (2005) constitutively overexpressed the vacuolar H þ -pyrophosphatase in commercial tomato cultivars. The resulting transgenic plants exhibited greater pyrophosphate-driven cation transport into root vacuolar fractions, increased root

182

Arabidopsis

Arabidopsis

Yeast

CBF1

Hþpyrophosphatase

Trehalose-6phosphate synthase

NHX1, vacuolar Na þ /H þ antiporter

Arabidopsis

Yeast

Arabidopsis

Drought CBF1

Salt HAL1 (K þ transport regulation) gene

Gene source

:NHX1 overexpressed

CaMV 35S:HAL1

CaMV 35S:TPS1

CaMV35S:AVP1D

ABRC1:CBF1

CaMV 35S:CBF1

Promoter:gene

Tolerance to high levels of salt; maintains high levels of K þ and low levels of intracellular Na þ Salt tolerance up to 200 mM NaCl; high Na þ concentrations in leaves but very low levels in fruits

Tolerance to cold, drought, and salt stress but dwarf phenotype and reduction in fruit set and seed number per fruit Tolerance to chilling, drought, and salt stress with normal growth and yield Greater pyrophosphate-driven cation transport into root vacuolar fractions, increased root biomass, and enhanced survivability during waterdeficit stress Improved tolerance to drought, salt, and oxidative stress

Phenotype

GM tomato for tolerance to abiotic stresses such as drought, salt, extreme temperatures, and hypoxia.

Gene product

Table 4.3.

Zhang and Blumwald 2001

Gisbert et al. 2000

Cortina and CulianezMacia 2005

Park et al. 2005

Lee et al. 2003

Hsieh et al. 2002a,b

References

183

Hypoxia ACC deaminase

Cys-2/His-2 zinc finger protein-TF

sHSP (mitochondrial) CAPX (cDNA)

Extreme temperatures Heat shock factor, hsfA1b Choline oxidase

Betaine aldehyde dehydrogenase

CaMV 35S:MT-sHSP :cAPX

Tomato

Bacteria

CAMV, rolD, and PRB-1b: ACC deaminase

CaMV 35S:CaPIF1 overexpression

CaMV 35S:CodA

Arthrobacter globiformis I Tomato

Pepper (Capsicum annuum)

CaMV 35S:AtHsfA1b

CaMV 35S:BADH (2 genes)

Arabidopsis

Atriplex hortensis

Tolerance to flooding stress, rolD promoter protects to greater extent

Enhanced resistance to heat (40 C) and UV-B stress in tomato Zhongshu No. 5 compared to wild-type plants Tolerance to cold stress and to the bacterial pathogen P. syringae

Heat shock–induced chilling tolerance Improved chilling and oxidative stress tolerance Thermotolerance

Enhanced tolerance to salt stress

Grichko and Glick, 2001

Seong et al. 2007

Wang et al. 2006

Nautiyal et al. 2005

Park et al. 2004

Li et al., 2003

Jia et al. 2002

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biomass, and enhanced survivability under soil water deficit stress. Transgenic tomato plants transformed with the yeast trehalose-6-phosphate synthase (TPS1) gene exhibited improved tolerance to drought, salt, and oxidative stress, indicating a great potential of this gene to impart stress tolerance to plants (Cortina and Culianez-Macia 2005). Salt-tolerant transgenic tomatoes also ensued by increasing expression of the A. thaliana tonoplast membrane Na þ /H þ antiporter, AtNHX1, under a strong constitutive promoter (Zhang and Blumwald 2001). They were able to grow, flower, and set fruit at 200 mM NaCl. Although their leaves accumulated high concentrations of Na, the seeds showed low concentrations of this element. The tomato hairy root lines transformed with BADH-1 gene using root-inducing plasmid (pRi) plasmid accumulated betaine (Jia et al. 2003). Constitutive expression of Atriplex hortensis BADH gene in tomato led to enhanced tolerance to salt stress. Overexpression of yeast HAL1 in transgenic tomatoes, which is involved in the regulation of K þ transport, also imparted tolerance to high levels of salt (Gisbert et al. 2000). Similar to yeast, these transgenic tomatoes were able to maintain higher levels of K þ and decreased levels of intracellular Na þ than the control. Mishra et al. (2002) showed that heat stress transcription factor (HsfA1) underexpressing plants as well as their fruits exhibited extreme sensitivity to elevated temperatures. Cosilencing of HsfA1 by its transgenes resulted in reduced heat stress–induced accumulation of chaperones and heat shock factors, suggesting a unique function of HsfA1 as a master regulator for inducing thermotolerance. The effect of heat shock factor on chilling tolerance has also been studied by expressing AtHsA1b and gusA under CaMV 35S promoter. The transformed tomato showed more accumulation of heat shock–induced gene transcripts and enzymes, including a twofold increase in the specific activity of soluble isoforms of ascorbate peroxidase (Li et al. 2003). Reactive oxygen species (ROS), such as hydrogen peroxide, superoxide, and hydroxyl radicals, are byproducts of biological redox reactions. ROS can denature enzymes and damage important cellular components. Plants develop antioxidant enzymes, such as superoxide dismutase (SOD) and ascorbate peroxidase (APX), to scavenge ROS and detoxify them. Wang et al. (2006) studied the effect of increased cytosolic ascorbate peroxidase (cAPX) on heat and UV-B stress tolerance using transformed tomato cv. ‘Zhongshu No. 5’ plants. This research demonstrated in laboratory or field tests the potential to enhance tolerance to heat, UV-B, and sunscald stress by genetic engineering. Overexpression of cAPX in transgenic tomato enhanced resistance to heat (40 C) and UV-B stress compared to wildtype plants. When leaf disks were placed at 40 C for 13 hours, the

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electrolyte leakage of disks from wild-type was 93%, whereas two tested transgenic lines (A9, A16) exhibited 24% and 52% leakage respectively. When fruits of wild-type and transgenic plants were exposed to UV-B (2.5mW cm-2) for 5 days, the extent of browning was 95%, 33%, and 37%, respectively. In field tests, the detached fruits from field-grown transgenic plants showed more resistance to exposure to direct sunlight than fruits from wild-type plants. APX activity in leaves of cAPX transgenic plants was several times higher than in leaves of wild-type plants when exposed to heat, UV-B, and drought stresses. Nautiyal et al. (2005) developed transgenic tomato lines overexpressing tomato MT-sHSP and showed that vegetative tissues of T0 and T1 lines exhibited enhanced thermotolerance, whereas Zhaoa et al. (2007) tested the function of endoplasmic reticulum (ER)–located small heat shock proteins (ER-sHSPs) in ER stress by overexpressing LeHSP21.5 in tomato plants. ER stress is basically an imbalance between the cellular demand for protein synthesis and the capacity of the ER to promote protein maturation and transport, which leads to an accumulation of unfolded or malfolded proteins in the ER lumen. Gene expression in the transgenic lines greatly attenuated the lethal effect of tunicamycin (a potent inducer of ER stress) on tomato seedlings. Moreover, tunicamycin treatment led to lower levels of the chaperone-binding protein, protein disulfide isomerase, and the chaperone calnexin transcripts in transgenic tomato plants than in the nontransgenic tomato plants. These results suggest that the HSP LeHSP21.5 can alleviate the tunicamycin-induced ER stress by promoting proper protein folding. Transformation of ‘Moneymaker’ tomato with a chloroplast targeted codA gene of Arthrobacter globiformis encodes choline oxidase that catalyzes the conversion of choline to glycine betaine and improves chilling and oxidative stress tolerance of transgenic plants (Park et al. 2004). These authors saw that transgenic tomato plants accumulated up to 1.2 mM of glycine betaine per gram of fresh weight with the chloroplasts containing up to 86% of total leaf glycine betaine. These transgenic tomato lines produced 10% to 30% more fruit compared to untransformed plants. The overexpression of CaPIF1 enhanced tolerance to cold stress, which was correlated with CaPIF1 expression levels in transgenic plants (Seong et al. 2007). Grichko and Glick (2001) showed that a bacterial ACC deaminase under the transcriptional control of double CaMV 35S, the rolD promoter from Agrobacterium rhizogenes (root-specific expression), produced tomato plants with increased tolerance to flooding stress and lesser deleterious effects of root hypoxia on plant growth than the nontransformed plants.

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8. Vaccines. Plant delivery of oral vaccines has attracted much attention because this strategy offers several advantages over vaccine delivery by injection (Langridge 2000; Pascual 2007; Sunil Kumar et al. 2007). Oral vaccines also offer the hope of more convenient immunization strategies and a more practical means of implementing universal vaccination programs worldwide. Tomato has been tested for expression of vaccines that can address human health issues of the developing world. Transgenic tomato plants potentially can bring several positive effects and improve human health. McGarvey et al. (1994) engineered tomato plants of cv. ‘UC82b’ to express a gene encoding a glycoprotein (G-protein), which coats the outer surface of the rabies virus. The recombinant constructs contained the G-protein gene from the environmental risk assessment strain of rabies virus. The G-protein was expressed in leaves and fruit of the transgenic plants, and it was found localized in Golgi bodies, vesicles, plasmalemma, and cell walls of vascular parenchyma cells. Ma et al. (2003) overexpressed hepatitis E virus (HEV) open reading frame 2 partial gene in tomato plants, to investigate its expression in transformants, the immunoactivity of expressed products, and explore the feasibility of developing a new type of plant-derived HEV oral vaccine. The recombinant protein was produced at 61.22 ng g1 fresh weight in fruits and 6.37–47.9 ng g1 fresh weight in the leaves of the transformants. It was concluded that the HEV-E2 gene was correctly expressed in transgenic tomatoes and that the recombinant antigen derived had normal immunoactivity. These transgenic tomato plants are a valuable tool for the development of edible oral vaccines. Chen et al. (2006) developed an effective antiviral agent against enterovirus 71 (EV71), that causes seasonal epidemics of hand, foot, and mouth disease associated with fatal neurological complications in young children, by transforming the gene for VP1 protein—a previously defined epitope and also a coat protein of EV71—in tomato plant. VP1 protein was first fused with sorting signals to enable it to be retained in the endoplasmic reticulum of tomato plant, and its expression level increased to 27 mg g1 in fresh tomato fruit. Transgenic tomato fruit expressing VP1 protein was then used as an oral vaccine, and the development of VP1specific fecal IgA and serum IgG were observed in BALB/c mice. Additionally, serum from mice fed transgenic tomato could neutralize the infection of EV71 to rhabdomyosarcoma cells, indicating that tomato fruit expressing VP1 was successful in orally immunizing mice. Moreover, the proliferation of spleen cells from orally immunized mice was stimulated by VP1 protein and provided further evidence of both humoral and cellular immunity. Results of this study not only demonstrated the feasibility of using transgenic tomato as an oral vaccine to generate

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protective immunity in mice against EV71 but also the probability of enterovirus vaccine development. The Gram-negative bacterium Yersinia pestis causes plague, which has affected human health since ancient times. It is still endemic in Africa, Asia, and the American continent. There is the urgent need for a safe and cheap vaccine due to the increasing reports of the incidence of antibiotic-resistant strains and concern with the use of Y. pestis as an agent of biological warfare. Out of all the Y. pestis antigens tested, only F1 and V induce a good protective immune response against a challenge with the bacterium (Benner et al. 1999). Alvarez et al. (2006) reported the expression in tomato of the Y. pestis F1-V antigen fusion protein. The immunogenicity of the F1-V transgenic tomatoes was confirmed in mice that were injected subcutaneously with bacterially produced F1-V fusion protein and boosted orally with transgenic tomato fruit. Expression of the plague antigens in the tomato fruit allowed producing an oral vaccine candidate without protein purification and with minimal processing technology, offering a good system for a largescale vaccination programs in developing countries. The future of edible plant-based vaccines through transgenic approaches will depend on producing them safely on sufficient amounts. B. Eggplant The eggplant, known as aubergine in Europe and brinjal in South Asia, is a popular vegetable crop grown in many countries throughout the subtropics, tropics, and Mediterranean area, since it requires a relatively long season of warm weather to give good yields. It was produced on 2 million ha in 2007 (Choudhary and Gaur 2009), with a global harvest of 32 million t. Asia contributed 91.5% of the world production (FAO 2009). India, the second largest producer in the world after China, produces 8 to 9 million t, a quarter of global production. A total of 1.4 million small marginal and resource-poor growers grow eggplant in all eight vegetable growing zones of India. The crop is often considered a poor person’s vegetable and is cultivated mainly on small family farms. It is an important source of nutrition and cash income for many resource-poor growers, since they transplant it from nurseries at different times of the year to produce two or three crops, each of 150 to 180 days’ duration. Growers start harvesting fruits at about 60 days after planting and continue the harvest for 90 to 120 days, thereby providing a steady supply of food for the family and a stable income. Eggplant was one of the first vegetable crops adopted by growers in India to be used as hybrids. Hybrids now occupy more than 50% of the eggplant-planted area.

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1. Insect Resistance. Eggplant is attacked by a number of insects including thrips, cotton leafhopper, jassids, and aphids. The most damaging pest is the eggplant fruit and shoot borer (FSB), Leucinodes orbonalis (Palada et al. 2006). Infestation is caused by adults migrating from neighboring fields, from eggplant seedlings, or from previously grown eggplants in the same planting area. Damage from L. orbonalis starts at the nursery stage and continues after crop transplanting until harvest. Losses have been estimated to be between 54% and 70% in India and Bangladesh and up to 50% in the Philippines (Choudhary and Gaur 2009). Recommended insect pest management practices include the prompt manual removal of wilted shoots, trapping male moths using pheromones to prevent mating, ensuring regular crop rotation, and using nylon net barriers. These methods, however, are not widely adopted by growers because of time and resource constraints or lack of awareness. There are no known eggplant cultivars resistant to the FSB, so the use of insecticide sprays continues to be the most common control method used by growers. The borers are vulnerable to sprays only for a few hours before they bore into the plant. Therefore, growers in India spray insecticides as many as 40 to 80 times over a 7-month cropping season (AVRDC 2001; Choudhary and Gaur 2009). Growers may even spray every other day, particularly during the fruiting stage, which contributes to the presence of pesticide residues. But despite the application of many insecticides, the eggplant fruits sold in the Indian market are still of inferior quality, infested with larvae from the borer (Choudhary and Gaur 2009). A survey of pesticide use in Central Luzon in the Philippines indicates that growers there spray up to 56 times with insecticides during a crop season to protect their eggplant crops against the borer (Palada et al. 2006). The decision of growers to spray is influenced more by subjective assessment of visual presence of the insect rather than methodology based on threshold levels. This reliance on visual assessment leads to gross overspraying with insecticides, higher insecticide residues, and unnecessary increase in growers’ exposure to insecticides. On average, 4.6 kg of active ingredient of insecticide per hectare per season is applied on eggplant (Choudhary and Gaur 2009). Such pesticide use, besides being detrimental to the environment and human health, also increases the cost of production, making this humble vegetable expensive for poor consumers. In Asia, chemical spraying for this insect accounts for 24% of the total cost of production (Choudhary and Gaur 2009). Intensive use of improperly applied insecticides raises serious concerns for environmental and human health. A study conducted in the Jessore district of Bangladesh found that 98% of farmers felt sickness and more than 3%

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were hospitalized due to various problems related to pesticide use (AVRDC 2003). FSB-resistant Bt eggplant was genetically engineered by Mahyco under a collaborative agreement with Monsanto , and the first Bt transgenic eggplant with resistance to FSB was produced in 2000. This GM eggplant incorporates the cry1Ac gene expressing insecticidal protein to confer resistance against FSB. This Bt-eggplant was effective against FSB, with 98% insect mortality in Bt-eggplant shoots and 100% in fruits compared to less than 30% mortality in non-Bt counterparts (ISAAA 2008). Similar to Bt-sweet corn, it is expected that Bt-eggplant cultivars will reduce pesticide applications and contribute to poverty reduction and overcoming food insecurity. Krishna and Qaim (2008) indicated that simulations using farm-survey data suggest the aggregate economic surplus gains of Bt-eggplant hybrids could be around U.S. $ 108 million per year in India. Eggplant consumers will capture a large share of these gains, but farmers and the seed company will also benefit. By sharing this technology with the public sector, Bt openpollinated eggplant cultivars eventually may become available (Krishna and Qaim 2007; Kolady and Lesser 2008), thereby making this technology more accessible for resource-poor farmers. The genetic engineering approach for eggplant improvement seems promising since it might also incorporate resistance or tolerance to other insects, nematodes, diseases, and abiotic stress as well as incorporating parthenocarpy. Recently, a gene-encoding oryzacystatin was introduced in eggplant, and the effect on Myzus persicae and Macrosiphum euphorbiae was examined (Ribeiro et al. 2006). The transgenic eggplant reduced the net reproductive rate, the instantaneous rate of population increase, and the finite rate of population increase of both aphid species compared with a control eggplant line. Age-specific mortality rates of M. persicae and M. euphorbiae were higher on transgenic plants. These results indicate that expression of oryzacystatin in eggplant has a negative impact on population growth and mortality rates of M. persicae and M. euphorbiae and could be a source of plant resistance for pest management of these aphids. Expression of Mi-1 gene isolated from tomato in eggplant cv. HP 83 conferred resistance to root knot nematode Meloidogyne incognita (Goggin et al. 2006). 2. Fungal Resistance. Attempts have also been made to engineer eggplant for fungal resistance. Overexpression of a yeast dD-9 desaturase gene in eggplant has resulted in higher concentrations of 16 : 1, 18 : 1, and 16 : 3 fatty acids, and such transgenics exhibited increased resistance to Verticillium wilt (Xing and Chin 2000). Transgenic plants challenged by

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Verticillium could also result in a marked increase in the content of 16:1 and 16:3 fatty acids. They have shown that cis-D9 16 : 1 fatty acid was inhibitory to Verticillium growth. Transgenic eggplants resistant to Verticillum and Fusarium wilts by overexpression of pathogenesisrelated genes, such as glucanase, chitinase, and thaumatin (singly and in combination), have been also produced (Rajam and Kumar 2007). 3. Plant Stress. Tolerance against osmotic stress induced by salt, drought, and chilling stress was achieved in eggplants expressing the bacterial mannitol-1-phosphodehydrogenase (mtlD) gene, which is involved in mannitol synthesis (Prabhavathi et al. 2002). Interestingly, these transgenic plants also showed enhanced resistance to fungal wilts caused by V. dahliae and F. oxysporum. Further, various transgenic eggplants overexpressing different genes (namely, arginine decarboxylase, ornithine decarboxylase, S-adenosylmethione decarboxylase, and spermidine synthase) encoding enzymes in the polyamine metabolic pathway have also been generated. These transgenic plants showed increased tolerance to multiple abiotic (salinity, drought, extreme temperature, and heavy metals) as well as biotic (fungal pathogens) stresses. More recently Prabhavati and Rajam (2007) showed that such transgenics expressing the mtlD gene with mannitol accumulation exhibit increased host plant resistance against three fungal wilts caused by F. oxysporum, V. dahliae, and Rhizoctonia solani under both in vitro and in vivo growth conditions. Mannitol levels could not be detected in the wild-type plants, but the presence of mannitol in the transgenics could be positively correlated with the disease resistance. These results and the previous data suggest that the mtlD gene can be used for engineering crop plants for both biotic and abiotic stress tolerance. 4. Parthenocarpy. Transgenic eggplants with parthenocarpic fruits were also developed by manipulating the auxin levels during fruit development through the introduction of iaaM gene from Pseudomonas syringae pv. savastanoi under the control of the ovule-specific promoter DefH9 from Antirhinum majus (Rotino et al. 1997). These transgenic eggaplants produced seedless parthenocarpic fruit in the absence of pollination without the external application of plant hormones, even at low temperatures, which normally prohibit fruit production in untransformed lines. Furthermore, these transgenic eggplants have exhibited significantly higher winter yields than the untransformed plants and a commercial hybrid under an unheated glasshouse trial (Donzella et al. 2000). Trials in open field for summer production and greenhouse for

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early spring production confirmed that transgenic parthenocarpic eggplant F1 hybrids gave a higher production coupled with an improved fruit quality with respect to the untrasformed controls (Acciarri et al. 2002). C. Potato Potato ranks as the third most important food crop after wheat and rice. The total 2007 potato harvest worldwide was about 323.5 million t in a total area of approximately 19 million ha. The top-ranking potato producers were China (approximately 65 million t in 4.4 million ha), Russia (37 million t in 2.9 million ha), and India (29 million t in 1.7 million ha); the highest national yields were recorded in New Zealand (50.3 t ha1), Belgium (46.9 t ha1), and France (45.4 t ha1). Potatoes yield on average more food energy per hectare than cereals as well as more edible protein and energy on a per-hectare and a per-day basis than either cereals or cassava (Horton 1988). Moreover, the biological value of potato protein is the best among vegetable sources and comparable to cow’s milk. The lysine content of potato complements cereal-based diets, which are deficient in this amino acid. 1. Insect Resistance. After the first Bt tomato was reported with partial resistance to lepidopteran insects, improvements through truncation of the Bt gene and codon modification were made to optimize protein expression in plants, and Bt potatoes expressing cry3A gene were developed. Bt-potato cultivars expressing resistance to Colorado potato beetle (Leptinotarsa decemlineata)—the most destructive insect pest of potato in North America—and aphids associated with Potato virus Y and Potato leafroll virus were approved for sale in the United States in 1995. On average, reported profits in United States were U.S. $ 55 ha1 for Bt-potato (Gianesi and Carpenter 1999), and ex-ante analysis suggested an average profit of U.S. $ 117 ha1 for virus-resistant potato in Mexico (Qaim 1998). These cultivars were marketed and sold under the trade names NewLeaf , NewLeafY, and NewLeafPlus by NatureMark , a subsidiary of Monsanto (Thomas et al. 1997). When NewLeaf cultivars were introduced in 1995, about 600 ha were grown commercially. As seed stocks increased, the commercial acreage reached 20,000 ha. Market success of the NewLeaf , NewLeafY, and NewLeafPlus potatoes could be attributed to the difficulty in controlling L. decemlineata and also high pest populations of aphids and associated virus problems due to mild winters in the Pacific Northwest (Thornton 2003). The added virus resistance benefited seed producers,

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while commercial growers benefited from higher yields and reduced need for insecticides (Thornton 2003). The processing industry and consumers benefited from improved quality. Potatoes were one of the first foods from a GM crop that was commonly served in restaurants. NewLeaf potato cultivars were the fastest cultivar adoption in the history of the U.S. potato industry (Thornton 2003), until potato processors, concerned about antibiotech organizations, consumer resistance, and loss of market share in Europe and Japan, suspended contracts for Bt-potatoes with growers in 2000, and they were taken off the market (Grafius and Douches 2008). Likewise, the crop area of GM insect- and virus-resistant potatoes did not increase at the same rate as in GM maize or GM cotton—irrespective of being highly effective and growers increasingly using them. This market growth for GM potatoes was not as rapid as the owners of the proprietary transgenic technology would have liked for four reasons: (1) growers’ ability to save potato tubers for future plantings; (2) the registration of a new insecticide (imidacloprid) that gave excellent control in the same year that Bt potato became available to growers; (3) consumer requests to segregate GM potatoes; and (4) trade issues driven by international consumers (Thornton 2003; Grafius and Douches 2008). International trade barriers were more substantial for GM potatoes than for other technology adoptions (Guenthner 2002). Thus, more than 60% of the U.S. market was closed to GM potatoes. This led to the processor and commercial grower discontinuing use, hence the loss of a market for NatureMark potatoes. One additional factor that led to the rapid demise was that only 3% of the U.S. potato area was Bt potatoes (Guenthner 2002). The major impact came when the leading fast food chaing, McDonald’s, decided to ban GM potatoes from its menu. NatureMark dissolved after the 2001 season. This initial failure of GM potatoes shows that consumer acceptance should be regarded as key for adopting transgenic crop technology. Guenthner (2002) indicated that although growers accepted GM potatoes, processors had little to gain by accepting GM raw materials but exposed themselves to significant risk in marketing because they did not have a ‘‘consumer-acceptance accelerator.’’ Nonetheless, the transgenic potato cultivar ‘Elizabeth’, bred at the Center of Bioengineering of the Russian Academy of Sciences and displaying resistance to Colorado potato beetle, was released recently for sale and is being used by the potato industry in Russia (http://www. potatopro.com/Lists/News/DispForm.aspx?ID¼3336). Cooper et al. (2007) evaluated natural host plant resistance mechanisms such as glandular trichomes and Solanum chacoense-derived resistance and genetically engineered resistance (cry3A and cry1Ia1) against Colorado potato beetle in a no-choice cage study. Their research

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suggest that Bt transgenes can provide high levels of host plant resistance and that available S. chacoense–derived resistance mechanisms seems to be variable to control Colorado potato beetle larvae in no-choice situations. The protein avidin—found in the whites of chicken eggs—has a broadspectrum insecticidal activity against arthropod pests, including Lepidoptera, Coleoptera, Diptera, and Acari. Avidin sequesters biotin, which is needed for cell growth and development of insects. Cooper et al. (2009a) incorporated a transgene for this protein in two potato clones: a susceptible genotype and a resistant one with S. chacoense as ancestor. They used leaf bioassays with first-stage Colorado potato beetle larvae to test. Their research showed significantly less survival as well as significantly lower survivors’ mass for larvae feeding on transgenic avidin lines vis- a-vis nontransgenic controls. Significantly fewer larvae fed on transgenic avidin plants survived to adulthood than those feeding on nontransgenic susceptible or S. chacoense–derived plants. The potato tuber moth (PTM, Phthorimaea operculella) or potato tuberworm is the most common and destructive insect pest of potatoes in tropical and subtropical areas worldwide (Visser 2005; Douches and Grafius 2005). The larvae mine the foliage, stems, and tubers in the field and in storage. Significant losses occur after tuber infection because the damaged tubers are attacked by various secondary pathogens and pests. Currently, the only available means to control P. opereculella and avoid major crop losses is the use of chemical insecticides. Combining natural resistance mechanisms with Bt cry genes could be a potential solution to improve potato resistance to PTM. Indeed, potatoes with cry1Ia1, cry1Ac, cry1Ac9, cry5 or cry9Aa2 transgenes—mostly under the transcriptional control of the CaMV 35S promoter but also with the Gelvin super promoter pBIML1-vector or the light-inducible Lhca3 promoter— showed enhanced host plant resistance to PTM larvae in detached-leaf or tuber bioassays (Jansen et al., 1995; Douches et al. 1998, 2002; Wedstedt et al. 1998; Can˜edo et al. 1999; Li et al. 1999; Lagnaoui et al. 2000; Mohammed et al. 2000; Davidson et al. 2002a,b, 2004; Meiyalaghan et al. 2006; Estrada et al. 2007). Field and storage trials in Egypt—under natural infestation—revealed that Bt-cry5 transgenic potatoes derived from the cv. ‘Spunta’ (‘Spunta-G2’, ‘Spunta-G3’, and ‘Spunta-6a3’) had the highest host plant resistance to PTM, with almost 100% of their tubers showing no insect damage in the field and about 90% free of insect damage after 3-month storage (Douches et al., 2004). Likewise, ‘SpuntaG2’ and ‘Spunta-6a3’ were higher yielding than’Spunta’ in field trials in Michigan (USA), but both transgenic clones had lower specific gravity— an important tuber quality trait—than the original cultivar from which they derive. South Africa was selected as the target country for releasing

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and marketing transgenic PTM-resistance potato because of its previous in-country experience with GM potato research (Douches et al. 2008). Multilocation yield trials and PTM efficacy trials (field and storage) have been conducted at six locations in South Africa since 2001. Complete control of the PTM was found at all locations in all years, and there was no infestation in the field when examining the foliage and tubers of ‘Spunta-G2’ and no infestation found in tubers stored up to 6 months. The cry1Ia1 transgene was used to transform two popular South African potato cultivars to ensure a greater impact. Further research by Cooper et al. (2009b) shows that expression of avidin combined with natural host plant resistance (from S. chacoense) in transgenic potato could be useful for controlling PTM. The cry1Ac transgene has been also used to engineer resistance in Andean potato cultivars ‘Diacol Capiro’, ‘Pardo Pastusa’, and ‘Pandeazu´car’ to Tecia solanivora, whose larvae attack potato tubers (Valderrama et al. 2007). Bioassays of T. solanivora larvae on transgenic potato tubers showed 83.7% to 100% mortality, whereas the mortality levels on nontransgenic counterparts were 0% to 2.7%. Data indicate the ability of cryAC transgenes to control T. solanivora while reducing the use of insecticides. However, a specific issue needs to be addressed regarding the potential use of these transgenic potatoes in the Andean region—the center of origin of this crop— because of potential gene flow to wild relatives growing near potato crops (Celis et al. 2004). In this regard, Scurrah et al. (2008) suggest the use of sterile cultivars with scarce flower production and lacking seed production to minimize the risk of gene flow from transgenic potato. 2. Late Blight Resistance. Late blight, caused by the oomycete pathogen Phytophthora infestans, is the most devastating potato disease in the world. Transgenic potato plants expressing soybean b-1,3-Endoglucanase gene exhibited enhanced host plant resistance to late blight (Borkowska et al. 1998). The wild diploid potato species S. bulbocastanum is highly resistant to all known races of P. infestans, and derived potato germplasm has shown durable and effective resistance in the field. Song et al. (2003) cloned the major resistance gene RB in S. bulbocastanum using a map-based approach in combination with a long-range (LR) PCR strategy. A four-gene resistance cluster of the coiled coil-nucleotide binding site-Leu-rich repeat class was found within the genetically mapped RB region. Transgenic plants using Agrobacteriummediated transformation containing the full-length gene coding sequence (including the open reading frame and promoter) were integrated into a cultivar (Halterman et al. 2008). All transgenic plants containing

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RB exhibited high foliar resistance whereas RB-containing tubers did not exhibit increased resistance. Furthermore, Kuhl et al. (2007) indicated that RB-transgenic plants showed increased resistance in field trials and variable results in laboratory tests using different P. infestans isolates. They also pointed out that the use of the RB gene for transformation creates a partially cisgenic event in potato because the gene’s native promoter and terminator are used. Such type of genetic transformation provides an opportunity to generate greater public approval of genetically engineered approaches to trait introgression in potato. 3. Host Plant Resistance. There are other transgenic potatoes with host plant resistance to both Potato virus X and Potato virus Y using markerfree and gene-silencing technology (Bai et al. 2009). Virus resistance in GM potatoes will be especially valuable because there are no pesticides for control of viruses, in contrast to insect pests or fungal diseases. Since potatoes are repeatedly propagated by tuber cuttings, viruses are easily spread during the seed multiplication process. Transgenic potatoes resistant to eelworm (Heterodera rostochiensis), to cyst (Globodera spp.) and root knot nematodes (Urwin et al. 2001, 2003; Simon 2003; Lilley et al. 2004) that do not alter susceptibility to nontarget insect herbivores or affect nontarget organisms in the potato rhizosphere (Cowgill et al. 2002a,b, 2003, 2004) and do not possess a risk to human diet (Atkison et al. 2004) are also available. In western Europe, late blight and eelworm resistance could be the primary drivers for market penetration of GM potatoes (Simon 2003). When consumers have confidence in the technology, it will spread quickly due to the environmental and production benefits. These two GM opportunities would greatly reduce pesticide use and would be extremely attractive to potato growers. 4. Other Traits. There are also other research advances on GM potatoes. For example, salt-tolerant potatoes are being bred using the DREB1A transgene driven by the stress-inducible rd29A promoter (Behnam et al. 2006). Likewise, increased nutritive value may be achieved in potato by expressing a nonallergenic seed albumin gene from Amaranthus hypochondriacus (Chakraborty et al. 2000), by protein-rich potato expressing the seed protein gene AmA1 (Amaranth Albumin 1) (Chakraborty et al. 2010), or by enhancing levels of carotenoid and lutein due to a crtBtransgene derived from Erwinia uredovora that encodes phytoene synthase (Ducreux et al. 2005). Moreover, tuber quality can be improved by reducing polyphenol oxidase activity associated with reduced woundinducible browning (Arican and Gozukirmizi 2003), or decreasing the

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amount of reducing sugars due to a bacterial-derived transgene coding for phosphofructokinase under a tuber-specific promoter (Navratil et al. 2007). Furthermore, potato researchers are genetically engineering potatoes producing dextran using a dextransucrase DsrS transgene initially isolated from Leuconostoc mesenteroides (Kok-Jacon et al. 2005), inhibiting the expression of the gene for granule-bound starch synthase (GBSS) using antisense constructs (Visser et al. 1991), or expressing full-length spike protein of infectious bronchitis virus (IBV) that may allow a new delivery system of Coronaviridae IBV vaccine (Zhou et al. 2004). Catchpole et al. (2005) used hierarchical metabolomics to demonstrate the substantial compositional similarity between conventional and transgenic potato bioengineered to contain high levels of inulin-type fructans (Hellwege et al. 2000), a prebiotic food supplement. Such comparisons are needed for determining whether any transgenic potato diplays alterations in metabolite composition outside the range of the cultigen pool. Recently the European Union has approved the planting of the amylose-free starch transgenic potato ‘Amflora’, which produces large amounts of pure amylopectin that can be used in technical applications by the paper industry (http://www.foodnavigator.com/news/ng. asp?n¼78450&m¼1FNE724&c¼huokmwqnnbjptez). D. Cucurbits Old World cucurbits, including watermelon (Citrullus lanatus), melon (Cucumis melo), cucumbers and gherkins (Cucumis sativus), and various gourds (Lagenaria and Momordica spp.), and New World cucurbits, such as pumpkin and squash (Cucurbita maxima, C. pepo and C. moschata), are grown throughout the temperate, subtropical, and tropical regions of the world. Cucurbits collectively rank among the top five vegetable crops produced worldwide with nearly 10 million ha devoted to production (FAO 2009). Watermelon ranks first in area (3.3 million ha) with a total production (93.7 million t), followed by cucumbers and gherkins (2.6 million ha and 44.4 million t), pumpkins plus squashes and gourds (1.6 milliom ha and 21.1 million t), other melons (1.2 million ha and 27.8 million ha), and melonseed (1.1 million ha and 0.7 million t). China is the top producer of watermelon (62.2 million t), cucumbers and gherkins (28 million t), and pumpkins plus squashes and gourds (6.3 million t), whereas Indonesia and Nigeria are the top producers of other melons (16.9 million t) and melonseed (490,000 t). Transgenics have become important in four cucurbits: summer squash, watermelon, cucumber, and melon.

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1. Summer Squash. In the United States, declines in yields of summer squash (Cucurbita pepo) due to viruses often range from 20% to 80% with a reported U.S. $ 2.6 million loss alone in the state of Georgia in 1997 (Gianessi et al., 2002). Three of the most important viruses affecting squash production are Zucchini yellow mosaic virus (ZYMV), Watermelon mosaic virus (WMV), and CMV (Zitter et al. 1996). Summer squash cultivars with satisfactory resistance to CMV, ZYMV, and WMV are yet to be developed by conventional breeding (Gaba et al. 2004). Control of squash viruses has focused on cultural practices, including delayed transplanting relative to aphid flights, use of reflective film mulch to repel aphids, and application of stylet oil to reduce virus transmission, in combination with insecticides to reduce aphid vector populations (Perring et al. 1999). In the state of Georgia, it is estimated that 10 stylet oil and insecticide sprays are made routinely to control aphids, thereby limiting virus incidence and transmission (Gianessi et al. 2002). Two lines of squash expressing the coat protein (CP) gene of ZYMV, WMV, and CMV were deregulated and commercialized in 1996 (Medley 1994). Subsequently, many squash types and cultivars have been developed, using crosses and backcrosses with the two initially deregulated lines. This material is highly resistant to infection by one, two, or all three of the target viruses (Clough and Hamm 1995; Fuchs and Gonsalves 1995; Ochoa et al. 1995; Tricoli et al. 1995; Fuchs et al. 1998; Schultheis and Walters 1998). Virus-resistant transgenic squash limits virus infection rates by restricting challenge viruses, reducing their titers, or inhibiting their replication or cell-to-cell or systemic movement. Therefore, lower virus levels reduce the frequency of acquisition by vectors and subsequent transmission within and between fields. Consequently, virus epidemics are substantially limited. The adoption of virus-resistant squash cultivars has steadily increased in the United States since 1996. In 2005, the adoption rate was estimated at 12% (approximately 3,100 ha) across the country with the highest rates in New Jersey (25%), Florida (22%), Georgia (20%), South Carolina (20%) and Tennessee (20%) (Shankula 2006). Virus-resistant transgenic squash has allowed growers to achieve yields comparable to those obtained in the absence of viruses with a net benefit of U.S. $ 22 million in 2005 (Shankula 2006). Engineered resistance was the only practical approach to development of cultivars with multiple sources of resistance to CMV, ZYMV, and WMV in those markets where GM squash is allowed. 2. Watermelon. Field trials have been conducted on transgenic watermelons containing genes conferring virus resistance and parthenocarpy (ISB 2007). Virus-resistant lines containing the coat protein genes from

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ZYMV and WMV2 were mechanically inoculated with both viruses and displayed resistance to both ZYMV and WMV2 (Tricoli et al., 2002). Control vines were highly symptomatic, producing very few fruits, and the fruits that were produced were very small in size. 3. Cucumber. Field trials were conducted with transgenic cucumbers engineered for viral resistance, herbicide tolerance, and increased salt tolerance. Slightom et al. (1990) and Gonsalves et al. (1992) tested transgenic cucumber lines derived from ‘Poinsett 76’ expressing the CMV coat protein gene for host plant resistance to CMV. These plants were compared to nontransgenic ‘Poinsett 76’ and the traditionally bred CMV-resistant line ‘Marketmore’. The level of CMV infection was determined at the end of the trial by enzyme-linked immune sorbent assay. The transgenic lines had significantly lower rates of infection than either ‘Marketmore’ or nontransgenic ‘Poinsett 76’. Virus-resistant lines of pickling, slicing, and beit alpha types were tested for resistance to virus in the field using paired plot designs in which each transgenic line was paired with its nontransgenic counterpart. Transgenic lines containing the coat protein genes from CMV, ZYMV, WMV2, and the nuclear inclusion protein A or B from PRSV exhibited high field resistance against all four viruses, including PRSV (Tricoli et al. 2002). 4. Melon. There have been field tests of male-sterile, long-shelf-life and virus-resistant transgenic melon lines (ISB 2007). Field testing of virusresistant transgenic melon lines showed no detrimental effects associated with the transgene. Nutritional analysis conducted on fruits harvested from transgenic and control lines showed no alteration in any of the nutritional components measured. However, in contrast to squash, high levels of virus resistance were achieved only in plants that were homozygous for the transgenes (Clough and Hamm 1995; Fuchs et al. 1997). Plants homozygous for the CMV, ZYMV, and WMV2 coat protein genes (designated CZW-30) never exhibited systemic symptoms of virus, whereas symptoms that did develop late in the season were the result of a single infection of one of the three viruses present in the field as opposed to mixed infections seen in the control lines. Hemizygous lines derived from CZW-30 developed systemic symptoms late in the season but still exhibited a 7.4-fold increase in fruit yields compared to control lines (Fuchs et al. 1997). Very recently, Wu et al. (2009) bred a transgenic melon with resistance to ZYMV by an improved cotyledon-cutting method. This transgenic melon has a great potential for controlling ZYMV in East Asia. Li et al. (2006) provided an update on transgenic approaches for improving quality traits of melon. They indicated that

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transgenic technology seems to be promising for sensory attributes and shelf life of melon fruit. E. Brassicas Vegetable brassicas include cabbage, cauliflower, broccoli, Brussels sprouts, tronchudas, collards, kales, kohlrabi, Chinese kale (B. oleracea), turnip, broccolettos, Chinese cabbage, pak-choi, choy-sum, komatsuna, yellow sarson (B. rapa), rutabaga or swedes, vegetable rape and mustards. They are economically important and grown worldwide for consumption as both fresh and frozen produce. In 2007, their production was 87 million t and the total harvest area of cabbages, cauliflower, and broccoli was 4.5 million ha worldwide (FAO 2009). Of this total area, 80% was grown in the developing world. Cabbages and cauliflower are important vegetable cash crops for low-income farmers throughout Asia, Africa, Latin America, and the Caribbean. They serve as important staple dietary items and are high in folate, vitamins B and C, and other micronutrients. In addition, vegetable brassicas are gaining popularity as they contain glucosinolates with anticancer properties. Protoplast fusion has been investigated as a means to introgress disease and pest resistance from other Brassicaceae species (Christey 2004), but transformation technology offers an alternative approach. 1. Insect Resistance. Lepidopteran larvae are the most problematic insect pests of vegetable brassicas worldwide. The diamondback moth Plutella xylostella is considered the most destructive insect pest of vegetable brassica and has severely limited its production, especially in resource-poor regions (Talekar and Shelton 1993). P. xylostella occurs in excess of 80 countries where brassicas are grown and causes losses to the world economy of over U.S. $1 billion yearly (Talekar and Shelton 1993), a figure that continues to rise. In India, the losses of cabbage and cauliflower due to P. xylostella frequently reach 90% without the use of insecticides (CIMBAA 2010). Significant losses occur and threaten food security even after the frequent use of insecticides. In tropical areas where pest pressure is high, it is not uncommon to apply insecticides every other day or at least 2.5 times per week (Rauf et al. 2004; Sandur 2005). In India, about 6,000 t of active ingredient of insecticides are used annually for diamondback moth control alone (Mohan and Gujar 2003). The cost of cabbage and cauliflower protection is greater than U.S. $168 million annually in India alone. A study undertaken for the Collaboration on Insect Management for Brassicas in Asia and Africa (CIMBAA) found that in a typical production area in the state of Karnataka (India),

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the average number of insecticide applications was 13 per crop (Sandur 2005) or more than 1 weekly. In areas of diamondback moth outbreak, application frequency is often much higher (e.g., up to 30 applications per crop is common). The cost of buying and applying insecticies was 38% of the total variable costs of production. Every year, spraying diamondback moth with insecticide consumes more than 33,000 person-years of labor in India alone. In Sandur’s study, one-third of farmers reported symptoms of pesticide poisoning in the previous year (conjunctivitis, headache, dermatitis, and stomach pains). Farmers widely disregard the ‘‘no-spray periods’’ before marketing brassicas, and twothirds of vegetables tested between 1988 and 1998 were contaminated by pesticide residues, with 11% of the samples exhibiting levels over the maximum residue level (Agnihotri 1999). The situation is undoubtedly worse now, as diamondback moth continues to develop serious resistance to all classes of compounds sprayed to control it, thus increasing the pressure to spray more intensively. Such intense use of insecticides poses hazards to farmers, consumers, and the environment and has caused populations of this insect to become resistant to most of the major insecticides. Diamondback moth has developed resistance to almost all insecticides in many parts of the world. Conventional crop breeding programs have failed to develop cultivars with really useful resistance to diamondback moth. Alternative pest management solutions based on agronomic regimes, biological control, or chemical pesticides have proven effective in some areas, especially in the highlands, but they are insufficient in lowland areas and cumbersome to implement successfully, especially by poorer farmers in developing countries. Various cry genes (cry1A, cry1Ab, cry1Ac, cry1A(b), cry1Ab3, cry1Ba1, cry1C, cry1Ba1, cry1Ia3, and cry9Aa) from Bt have been introduced into cabbage (Metz et al. 1995; Jin et al. 2000; Bhattacharya et al. 2002; Paul et al. 2005; Christey et al. 2006), cauliflower (Khuvshinov et al. 2001; Chakrabarty et al. 2002, Christey et al. 2006), broccoli (Cao et al. 2001, Christey et al. 2006), collards (Cao et al. 2005), Chinese cabbage (Cho et al. 2001), choy-sum (Xiang et al. 2000), and rutabaga or swede (Li et al. 1995). Bt-vegetable brassicas successfully control important insect pests such as diamondback moth (P. xylostella) and other lepidoptera and cabbage white butterfly (Pieris rapae) (Earle et al. 2004). Several field tests with Bt-vegetable brassicas using cry1C and cry1B transgenes, which are effective against P. xylostella, are in progress in Asia, Africa, and Oceania by CIMBAA. Cross-resistance between both cry-derived toxins was not detected (Zhao et al. 2001), Nunhems Inc. Seed Company (one of the partners of CIMBAA) in India has produced cabbage and cauliflower lines that express both proteins at levels sufficient to control

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not only populations of susceptible P. xylostella but also populations of P. xylostella that are resistant to cry1C transgene. None of the populations of P. xylostella has developed resistance to cry1B transgene. Laboratory and greenhouse studies with CIMBAA breeding lines have shown excellent control of P. xylostella and P. rapae. In addition to cry Bt genes, the cowpea trypsin inhibitor has been shown to confer insect resistance in cauliflower (Iingling et al. 2005) and in Chinese cabbage (Zhao et al. 2006). A trypsin inhibitor is a type of protease inhibitor that is capable of controlling a wide spectrum of insect pests. Ding et al. (1998) produced insect-resistant transgenic cauliflower expressing a sweet potato trypsin inhibitor gene. Transgenic cauliflower plants were obtained with a high degree of protection against the lepidoptera pests Spodoptera litura (cut worm) and P. xylostella. 2. Disease Resistance. Downy mildew (Peronospora parasitica), clubroot (Plasmodiophora brassicae), alternaria blight (Alternaria brassicicola), black rot (Xanthomonas campestris pv. campestris), stem rot and watery soft rot (Sclerotinia sclerotiorum), Cauliflower mosaic virus (CaMV), and Turnip mosaic virus (TuMV) are other pathogens affecting vegetable brassicas. Chitin is an important component of fungal cell walls. Chitinase genes cloned from plants and fungi have been transferred into a number of plant species and resistance to a broad range of fungal pathogens obtained. Mora and Earle (2001) produced transgenic broccoli plants expressing an endochitinase gene from the biocontrol fungus Trichoderma harzianum. Transgenic plants were obtained with 14 to 37 times higher endochitinase levels than controls. Transgenic plants inoculated with A. brassicicola showed significantly less severe disease symptoms than controls. Interestingly, polyploid plants were highly susceptible regardless of their endochitinase activity. In contrast, lesion size of plants inoculated with S. sclerotiorum was not statistically different from controls. Braun et al. (2000) introduced antibacterial genes from nonplant sources into cauliflower in an attempt to produce black rot–resistant cauliflower. They introduced the Shiva protein, which is a synthetic analog of cecropin B from the giant silkworm moth, and the magainin II peptide derived from the African clawed frog. In vitro bacterial assays using crude leaf extracts confirmed increased resistance to black rot, but greenhouse screening failed to show any increased resistance compared to controls. Likewise, Zhao et al. (2006) introduced Shiva and cecropin B into Chinese cabbage. Gene expression in the transgenic plants was

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confirmed by Northern blot analysis, but bacterial assays were not undertaken. Glucose oxidase catalyzes the oxidation of glucose generating H2O2 as a by-product. H2O2 effectively inhibits bacterial and fungal growth, and plants transgenic for glucose oxidase show enhanced host plant resistance to pathogens. However, some deleterious phytotoxic effects of glucose oxidase have been noted in transgenic plants. Cabbage expressing a glucose oxidase gene from Aspergillus niger showed enhanced resistance to black rot but also showed phytotoxic effects (Lee et al. 2002). Plants showed significant growth retardation, and seed set was dramatically reduced, with only a few seed produced. Passel egue and Kerlan (1996) transformed cauliflower with two CaMV-derived genes in an attempt to produce CaMV-resistant cauliflower. They used the capsid gene and the antisense gene VI of CaMV. While reverse transcriptase polymerase chain reaction demonstrated the presence of CaMV gene transcripts in all plants, the amount of RNA transcribed was very low, in contrast to the hygromycin resistance (hpt) gene transcript. In plants transformed with the capsid gene, the capsid protein could not be detected. The response to CaMV infection was not tested. In contrast, Zhandong et al. (2007) successfully obtained high levels of resistance to TuMV in Chinese cabbage plants transformed with the antisense TuMV replicase (NIb) gene. Plants were transformed using marker-free A. tumefaciens–mediated floral dipping. 3. Weed Control. The incorporation of herbicide resistance into vegetable brassicas would enable growers to control weeds more efficiently. Basta -resistant broccoli has been produced and field-tested by Christey et al. (1997) and Waterer et al. (2000). Waterer et al. (2000) field-tested six transgenic lines and noted that herbicide application had little effect on head quality and marketable yield of most lines. Christey et al. (1997) field-tested four transgenic lines and also noted that the phenotype was normal although plants were not sprayed in the field. Spraying of Basta on seedlings demonstrated they were resistant in greenhouse trials. 4. Postharvest Quality. Postharvest traits such as transport quality and shelf life are of increasing importance mainly in inflorescence brassicas like broccoli. Postharvest senescence of broccoli is rapid with loss of chlorophyll resulting in yellowing of the head. Ethylene plays an important role in the yellowing of broccoli as chlorophyll loss is associated with an increase in floret ethylene synthesis. Chlorophyll loss can be delayed through the use of inhibitors of ethylene action and biosynthesis. Several groups are conducting transgenic research aimed at

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increasing the shelf life of ethylene-sensitive broccoli. Antisense versions of two key regulatory genes in the ethylene biosynthesis pathway ACC oxidase and ACC synthase have been used to produce transgenic broccoli plants with reduced ethylene synthesis. However, the reduction in ethylene production resulted in increases in shelf life of only 1 or 2 days. In order to delay postharvest senescence in broccoli, Henzi et al. (1999a,b) used A. rhizogenes–mediated transformation to express an antisense ACC oxidase gene from tomato in broccoli. Plants showed reduced ethylene production but little effect on postharvest senescence (Henzi et al. 2000b). Gapper et al. (2002) used A. tumefaciens–mediated transformation to introduce an antisense ACC oxidase gene (driven by the asparagine synthetase promoter from asparagus) from broccoli into broccoli. Several lines were obtained with reduced ethylene production and delayed postharvest senescence (Gapper et al. 2002). Higgins et al. (2006) have also shown that broccoli transgenic for antisense versions of ACC synthase and ACC oxidase have reduced ethylene production, which correlates with delayed chlorophyll loss. Cytokinin has also been shown to be involved with broccoli senescence, as application of cytokinin to broccoli heads can delay postharvest yellowing. Gapper et al. (2002) introduced an isopentenyl phosphotransferase (IPT) gene into broccoli, but their results on the effect of postharvest senescence were not indicated. Some plants had an abnormal phenotype typical of constitutive IPT expression. Chen et al. (2001) also introduced an IPT gene into broccoli under the control of senescence-associated promoters and demonstrated retardation in postharvest yellowing in broccoli heads and leaves. About 31% of transformants exhibited delayed yellowing in detached leaves, 16% in floret branchlets, and 7% in both leaves and floret branchlets. Eason et al. (2005) and Chen et al. (2004) delayed senescence in broccoli through genetic transformation with either an antisense cysteine protease or mutant ethylene response sensor gene, respectively. In both cases, senescence was delayed only by 1 or 2 days. As there are several other genes whose expression is increased at broccoli harvest, it is likely that down-regulation of these genes through antisense or RNA interference will also lead to the production of broccoli with delayed senescence. It is likely that future research will involve the introduction of these genes into green leafy vegetables such as Chinese cabbage and pak-choi, which also show postharvest deterioration due to ethylene. Nutritional quality and health benefits are becoming very important for consumers. Current advances in genetic engineering have enabled the production of plants with alterations in a range of vitamins or amino acids for improved human or animal nutrition. Lu et al. (2006) developed transgenic cauliflower

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with b-carotene accumulation, and Wahlroos et al. (2004) produced oilseed B. rapa with increased histidine content. It is likely in the future that more transgenic vegetable brassicas with altered vitamin or amino acid content also will be developed. 5. Healthy Food. Flavonoids such as anthocyanins are known as antioxidants in vitro and can reduce the risk of many diseases related to aging. However, some vegetable brassicas, such as cauliflower, are low in anthocyanins. In an attempt to manipulate pigment biosynthesis to increase the health benefits of vegetables, the effect of a regulatory locus of flavonoid content was assessed. Agrobacterium tumefaciens– mediated transformation of a Brassica oleracea line, selected for high transformation ability by Sparrow et al. (2004), was used to produce plants transgenic for the maize lc (leaf color) locus. Lc is a regulatory gene in the anthocyanin pathway, and it is expected that its presence will increase the flavonoid content. Seedling explants were cocultivated with Agrobacterium tumefaciens strain LBA4404 containing a binary vector with a neomycin phosphotransferase II (NPTII) gene. Under tissue culture conditions, lc-containing plants were green with no visible increase in anthocyanin production. However, after transfer to the greenhouse, the exposure to high light intensity led to visible signs of pigmentation within one week. Increased pigmentation was apparent in stems, petioles, main leaf veins, and sepals. Lc-containing lines had 10 to 20 times higher levels of total anthocyanins than controls. In addition, antioxidant activity of lc-containing lines was 1.5 times higher than that of controls (Braun et al. 2006). 6. Male Sterility and Self-Incompatability. Hybrid seed production is an important breeding goal in vegetable brassicas as hybrid seed offers many benefits, including increased vigor and greater uniformity. The introduction of male sterility and self-incompatibility (which prevents self-fertilization and promotes outcrossing) into vegetable brassicas would aid production of hybrid seed. Transformation approaches have been used in cabbage, cauliflower, and Chinese cabbage to induce male sterility. In cauliflower, Bhalla and Smith (1998) introduced an antisense pollen-specific gene linked to a pollen-specific promoter and obtained the expected sterility in 50% of the pollen. In Chinese cabbage, introduction of an antisense version of the CYP86MF gene linked to a tapetum-specific promoter induced male sterility (Yu et al. 2004). Lee et al. (2003) also used a tapetum-specific promoter to induce male sterility in cabbage through the introduction of the cytotoxic diphtheria toxin A chain. Self-incompatibility has a number of drawbacks, includ-

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ing breakdown of incompatibility, labor intensiveness, and genetic complexity of the system. In brassicas, self-incompatibility is sporophytically controlled by multiallelic genes at the S-locus. Two genes have been identified at the S-locus: S-locus glycoprotein (SLG) and S-locus receptor kinase (SRK). SLG and SRK encode a secreted glycoprotein in the wall of the stigma papillary cells and a transmembrane receptor kinase, respectively. A self-incompatible response occurs when the same S-allele is expressed in pollen and stigma. Toriyama et al. (1991) introduced an SLG gene from B. rapa S8 homozygote and were able to alter the self-incompatibility phenotype of pollen and stigma. Self-incompatible Chinese kale and partial compatible broccoli plants were fully compatible upon self-fertilization. 7. Plant Stress. Salinity and drought can limit brassica vegetable production. Bhattacharya et al. (2004) produced cabbage plants with enhanced salt tolerance through the introduction of the bacterial glycinebetaine biosynthesis (BetA) gene for biosynthesis of glycinebetaine. Detailed analysis of three independent transgenic lines showed improved growth and development under salt stress compared with the control. Park et al. (2005a) developed transgenic Chinese cabbage with the B. napus late embryogenesis abundant (LEA) gene that showed enhanced tolerance to both drought and salt. F. Lettuce Lettuce (Lactuca sativa) is the most important leafy vegetable worldwide, being grown extensively as a salad crop and consumed primarily in the fresh state. The worldwide estimated production of lettuce is about 23 million t (FAO 2009). In the last decade, the market and area of production for lettuce has expanded quite a bit with more cultivars being cultivated in line with consumer requirements for novel produce. Currently, young leaves of lettuce are becoming popular components (individually or in mixtures) of leafy ‘‘baby salad’’ packs. 1. Disease Resistance. Experiments were undertaken in the 1990s for introducing virus resistance into lettuce using a coat protein genemediated approach. Pang et al. (1996) transferred the nucleocapsid (N) protein gene of the Lettuce Tospovirus (TSWV) into two lettuce breeding lines. Transgenic plants expressing the nucleocapsid (N) protein gene were protected against TSWV. Dinant et al. (1993) introduced a Lettuce mosaic virus (LMV) coat protein (LMV-CP) gene into LMVsusceptible lettuce, but the transgene conferred only poor resistance to

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this virus. Loss of virus resistance was more pronounced in lettuce during subsequent seed generations, an observation also made by Gilbertson (1996). Likewise, Dinant et al. (1997) introduced the coat protein gene from LMV strain O into the virus susceptible cvs. ‘Girelle’, ‘Jessy’, and ‘Cocarde’. Several transgenic plants accumulated LMV-CP. As in other examples of potyvirus sequence-mediated protection, some plants were completely virus resistant, but in others this resistance was not sustained, with the development of viral infection symptoms. The efficiency of this strategy to induce LMV resistance was considered to be related to the developmental stage of the transgenic plants at the time of their inoculation with the virus. Sesquiterpene lactones play a role in host plant resistance to pathogens through the hytoalexin response. Such compounds include lactucin and lettucenin A. Bennett et al. (2002) cloned genes for germacrene A synthases in order to change the profile of these latex-expressed compounds and to enhance host plant resistance to pathogens using sense and antisense approaches. Dias et al. (2006) also introduced the decarboxylase (oxdc) gene from Flammulina spp. into lettuce and showed that leaves from two transgenic plants inoculated with agar plugs of a 2-day old culture of Scierotinia sclerotiorum failed to develop disease symptoms. Transformation of plants with proteinase inhibitors that act on proteolytic enzymes may confer resistance to pests and pathogens. In studies of the role of the proteinase inhibitor II, SaPIN2a, from Solanum americanum, Xu et al. (2004) transformed lettuce with the SaPIN2a gene driven by the CaMV 35S promoter and suggested that this approach may be exploited to counteract pest and pathogen attack. Subsequently, Fan and Wu (2005) also introduced a PIN2 gene into lettuce, while Chye et al. (2006) extended these investigations to show that expression of SaPIN2a in lettuce conferred resistance to cabbage looper (Trichoplusia ni) caterpillars. 2. Weed Control. Lettuce shows a very low competitive ability against weeds. Hence, tolerance to herbicides is a prime target for genetic manipulation in lettuce since weeds cause severe crop losses. Herbicide tolerance by genetic manipulation has been introduced into lettuce from both academic and commercial perspectives. Mohapatra et al. (1999) introduced the bar gene from the bacterium Streptomyces hygroscopicus into seedling cotyledons of the cv. ‘Evola’ by Agrobacterium-mediated transformation with strains 0310 and 1310. The strain 1310 carried the hypervirulent pTOK47 in addition to the binary vector with the nptII and bar genes. Plasmid TOK47 in strain 1310 gave multiple insertions of

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T-DNA into some plants, whereas strain 0310 gave single-gene inserts in all plants analyzed by DNA-DNA hybridization. Axenic seedlings grew on medium with glufosinate ammonium at 5 mg l1, while glasshousegrown plants were resistant to the herbicide when the latter was sprayed on the plants at 300 mg l1. This research confirmed that herbicide resistance can be introduced into lettuce with stable expression in seed generations. 3. Male Sterility. The introduction of male sterility for hybrid seed production is another objective in lettuce breeding. In experiments to induce male sterility in lettuce, a pathogenesis-related b-1,3-glucanase gene linked to a tapetum-specific promoter, A9, was cloned into the binary vector pBIN19 and the latter introduced into A. tumefaciens carrying pGV2260, prior to transformation of the cv. ‘Lake Nyah’ (Curtis et al. 1996b). Transgene expression resulted in dissolution of the callose wall of developing microspores, inhibiting pollen grain development, resulting in male sterility. This or a similar approach may eliminate the need to remove pollen from the stigmatic surface of recipient plants to avoid self-pollination prior to application of donor pollen. 4. Postharvest Quality. Breeding lettuce for postharvest traits, mainly transport quality, shelf life, and cosmetic problems, is of increasing importance. Lettuce used for packaged salads deteriorates rapidly following harvest, requiring a considerable investment of effort to maintain quality and shelf life of cut material. Harvesting increases respiration, thereby stimulating deterioration with an increase in the synthesis of phenylalanine ammonia lyase and phenolic compounds, such as chlorogenic acid, which cause tissue browning (Kang and Saltveit 2003). Delaying leaf senescence in lettuce is therefore an important target for genetic manipulation because lettuce with appropriate transport quality, better shelf life, and good appearance will be preferred by traders and consumers. Curtis et al. (1999b) introduced the T-cyt gene (synonym ipt, tmr, or gene 4) coding for isopentenyl phosphotransferase, which is involved in cytokinin biosynthesis, from the T-DNA of A. tumefaciens on the binary vector pMOG23 into the lettuce cv. ‘Saladin’. Transgenic plants were phenotypically normal following transfer to the glasshouse, set viable seed, and had increased cytokinin and chlorophyll contents in their leaves compared to nontransformed plants. Such results indicated the possibility of delaying senescence in lettuce, possibly reducing the requirement for postharvest controlled environmental conditions to prolong the shelf life of harvested plants. In subsequent research, the ipt gene driven by the senescence-specific promoter SAG12 from

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A. thaliana (pSAG12-IPT) was introduced into the lettuce cv. ‘Evola’. Plants homozygous for the transgene exhibited significantly delayed postharvest leaf senescence (McCabe et al. 2001). Importantly, the transgene was activated only during senescence, particularly when the latter process commenced in the outer (lower) leaves, initiating cytokinin biosynthesis, which inhibited leaf senescence, simultaneously attenuating activity of the pSAG12-IPT gene, thereby preventing cytokinin overproduction. Heads of transgenic plants retained chlorophyll in their outer leaves after harvest 7 days longer than leaves of the nontransgenic plants. Mature plants were morphologically normal at harvest and did not show significant differences in head diameter or fresh weight of leaves or roots compared to their nontransgenic counterparts. Although during storage, heads of transgenic plants showed a threefold increase in the concentrations of acetaldehyde, ethanol, and dimethyl sulfide, increase in the latter compound was paralleled by an accumulation of reactive oxygen species. This research emphasizes the importance of detailed metabolite profiling of plants following transgene insertion, as the integration of a gene to modify one or more traits may affect other biosynthetic pathways. 5. Healthy Food. Nutritional quality as understood by the consumers and available at a moderate price may encourage enhanced consumption, thereby conferring an important marketing incentive to plant breeding. For example, vitamin E—which includes tocopherols—is a lipid-soluble antioxidant. There are a, b, g, and d isoforms of tocopherol with relative vitamin E potencies of 100%, 50%, 10%, and 3%, respectively. Conversion of g-tocopherol to a-tocopherol in food crops could increase their value and importance in human health because vitamin E reduces the risk of several serious disorders (e.g., cardiovascular diseases and cancer), slows aging, and enhances the function of the immune system. Cho et al. (2005) developed transgenic lettuce plants of the cv. ‘Chungchima’ expressing a cDNA encoding g-tocopherol methyltransferase from A. thaliana to improve tocopherol composition. Transgene inheritance and expression in transformed plants increased enzyme activity and conversion of g-tocopherol to the more potent a form. Similalry, resveratrol—a stilbenes—shows cancer chemopreventive activity and may prevent coronary heart disease and arteriosclerosis. Stilbene synthase is the key enzyme in resveratrol biosynthesis, with several stilbene synthase genes being isolated recently. Although lettuce contains the substrates for stilbene synthase, resveratrol is not synthesized. Thus, in order to engineer lettuce for synthesis of this compound, Liu et al. (2006) fused a cDNA encoding

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stilbene synthase from Parthenocissus henryana to the CaMV 35S promoter with the bar gene as a selectable marker. The expression construct was flanked by matrix attachment regions to maximize expression of the gene of interest in transgenic plants. Quantitative analysis showed that resveratrol in transgenic plants was 56.0  5.52 mg1 leaf fresh weight, which is comparable to that in the skin of grapefruit (Citrus  paridisi Macfad.). Zinc is also an essential element in human nutrition, as its deficiency severely impairs organ function. In experiments to fortify lettuce with this element, Zuo et al. (2002) used Agrobacterium-mediated gene delivery of a mouse metallothionein mutant b-cDNA in the cv. ‘Salinas 88’. The concentration of zinc in the transgenic plants increased to 400 mg g1 dry weight, which is considerably higher than in wild-type plants. In attempts to reduce bitterness, Sun et al. (2006) cloned the gene for the sweet and taste modifying protein miraculin from the pulp of berries of Richadella dulcifica, a West African shrub. This gene, with the CaMV 35S promoter, was introduced into the cv. ‘Kaiser’ using A. tumefaciens GV2260. Expression of this gene in transgenic plants led to the accumulation of significant concentrations of the sweetenhancing protein. Miraculin, which is active at extremely low concentrations, may be used by people suffering diabetes as a food sweetener. Nitrate content is also important for product quality and consumer health. Accumulation of nitrate in lettuce and other vegetables is undesirable, since in humans, nitrate produces nitrite, which hinders the binding of oxygen to hemoglobin. Lettuce often accumulates nitrate to concentrations that exceed the maximum permitted concentration. Indeed, nitrate concentration is one of several parameters that govern the marketability of this crop, especially in winter, when plants accumulate nitrate because of low light conditions. In experiments to reduce nitrate accumulation in lettuce, Curtis et al. (1999a) introduced the nia2 cDNA for nitrate reductase from tobacco driven by the 35S promoter into the cv. ‘Evola’. Unfortunately, none of the transgenic plants exhibited a reduction in nitrate content compared to the wild-type plants at harvest, although plants with nitrate concentrations slightly less than those of wild-type plants were observed during cultivation. Subsequently, Dubois et al. (2005) investigated nitrate accumulation in the cv. ‘Jessy’ using a similar 35S::nia2 construct. They also concluded that none of the plants carrying the transgene exhibited a reduction in nitrate accumulation, although the transgene was expressed. Transgene-specific silencing extended to the homologous endogenous nitrate reductase mRNA (messenger RNA) resulting in chlorosis and eventual death of the

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transgenic plants, which reveals the difficulty of this approach for reducing nitrate accumulation in lettuce. 6. Plant Stress. Salinity limits crop production in many vegetable areas, particularly in those that have been intensively used. Lettuce is highly sensitive to salinity. In addition, drought and cold restrict its growth in the field. Park et al. (2005b) introduced a late-embryogenesis abundant protein gene from Brassica napus into lettuce. Six transgenic plants generated exhibited enhanced growth compared to nontransformed plants under salt stress imposed by exposure to 100 mM sodium chloride. Furthermore, Curtis et al. (1996a) transformed the lettuce cv. ‘Lake Nyah’ with the rolAB genes from Agrobacterium rhizogenes to stimulate root formation, with the aim of increasing drought tolerance, whereas Pileggi et al. (2001) focused attention on drought, salinity, and cold by transforming the lettuce cv. ‘Grand Rapids’ with a mutated P5CS gene for d-1-pyrroline-5-carboxylate synthase, which catalyzes two steps of proline biosynthesis in plants. This mutated gene is insensitive to feedback inhibition by proline. Increased concentration of proline acts like an osmoprotectant that could confer resistance to drought, salinity, and cold on transgenic plants. Transgenic lettuce plants were tolerant to freezing. Vanjildorj et al. (2005) also targeted drought and cold tolerance in lettuce by overexpressing the Arabidopsis ABF3 gene—encoding a transcription factor for the expression of ABA-responsive genes—in the lettuce cv. ‘Chongchima’. Transgenic plants were phenotypically normal, produced seed, and were more tolerant than wild-type plants to drought and cold stresses. G. Alliums The total production of alliums was 85 million t annually in 2007 including 66 million t for onion and 16 million t for garlic (FAO 2009). Production of these two major allium crops occurs in 175 countries with China the largest world producer, producing 32% of onions and 76% of garlic (FAO 2009). 1. Weed Control. Alliums are monocots and they show a poor competitive ability with weeds. Herbicide-resistant onion germplasm has been bred by using the CP-4-derived gene construct that confers resistance to the systemic herbicide glyphosate (Eady et al. 2003). The enolpyruvylshikimate-3-phosphate synthase (EPSPS) enzyme, which is involved in the production of aromatic amino acids in plants, is inhibited by glyphosate. Tolerance to glyphosate is achieved either

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through the overexpression of the CP-4 EPSPS enzyme (Hetherington et al. 1999) or by detoxification of the glyphosate by either the glyphosate oxidoreductase (GOX) gene or the glyphosate acetyl transferase (GAT) gene. Onion plants containing a CaMV 35S-bar gene construct and the constitutively expressed CP-4-derived glyphosate resistance gene have been produced. All plants that have been confirmed by Southern analysis as containing the bar or CP-4-derived transgenes (one or two copies) have shown a strong tolerance to the herbicides Buster or Roundup , respectively. Initially, a 0.5% solution of the contact herbicide Buster was sprayed onto the leaves of the transformed onion plants. Plants that tolerated this treatment were then sprayed with commercially recommended concentrations of Buster for generalpurpose weed control to confirm their resistance to this herbicide (Eady et al. 2003). The level of resistance achieved indicated that the commercial production of transgenic onions containing a bar resistance gene is a feasible option for weed control in this crop. Glyphosatetolerant plants produced to date, which were tested in a similar manner (Eady et al. 2003), have proven to be tolerant to twice the recommended field application rates required for general weed control. F1 seed has recently been produced from these plants, and they are currently being field-tested for further assessment. The deployment of glyphosatetolerant lines could substitute for the application of toxic and persistent herbicides. Savings in herbicide usage of up to 75% for this crop have been projected, which equates to an economic saving of about U.S. $250 per hectare (Eady 2001). In addition, glyphosate is a short-lived, lowtoxicity herbicide compared with many of the persistent toxic herbicides that are currently used in many developed countries to control onion weeds. 2. Quality. The unique flavor and odor of alliums is derived from the hydrolysis of ACSOs [S-alk(en)yl-L-cysteine sulphoxides], which produces pyruvate, ammonia, and volatile sulfur compounds (Randle and Lancaster 2002). This reaction is catalyzed by the enzyme alliinase (alliin alkyl-sulphenate-lyase, E.C. 4.4.1.4), which is contained in vacuoles within cells and released upon disruption of the tissue (Lancaster and Collin 1981). Four different ACSOs have been identified in alliums (Bernhard 1970): ( þ )-S-methyl-L-cysteine sulfoxide, ( þ )-Spropyl-L-cysteine sulfoxide, trans-( þ )-S-(1-propenyl)-L-cysteine sulfoxide, and ( þ )-S-(2-propenyl)-L-cysteine sulfoxide (2-PECSO or alliin). Variations in the ratios of these volatile sulfur compounds are responsible for the difference in flavors and odors between Allium species (Randle and Lancaster 2002). Along with health and nutritional

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benefits associated with these compounds, these polyphenols are also major contributors to the bitter taste of some onions (Randle and Lancaster 2002; Almeida 2006). Three sets of transgenic onion plants containing antisense alliinase gene constructs (a CaMV 35S-driven antisense root alliinase gene, a CaMV 35S-driven antisense bulb alliinase, and a bulb alliinase promoter-driven antisense bulb alliinase) have been recently produced (Eady 2002). Results from the antisense bulb alliinase lines have been much more encouraging, and three lines were produced with barely detectable bulb alliinase levels and activity. Progress has been confounded by the poor survival of transgenic plants. Transgenic hybrid onion seed from these transgenic lines has been developed by crossing a nontransgenic open-pollinated parental line with a transgenic parental plant carrying a single transgene in the hemizygous state. Some resulting seed produced by the nontransgenic parents will be hemizygous for the transgene and can be selected to give F1 heterozygous individuals containing the transgene. Self-fertilization of these individuals produces homozygous, hemizygous, and null F2 progeny for the transgene locus. These homozygous individuals can then be used to generate the bulk seed required for the production of commercial transgenic lines. 3. Disease Resistance. Improving resistance to Sclerotium cepivorum, which causes allium white rot, can be achieved by overexpressing a germin protein with oxalate oxygen oxidoreductase (OXO) activity (Bidney et al. 1999) and the antimicrobial magainin (MGD) peptide (Zasloff et al. 1988). OXO degrades oxalic acid, the fungal toxin produced by S. cepivorum and many other plant fungal pathogens, to form carbon dioxide, hydrogen peroxide, and oxygen. The concomitant production of hydrogen peroxide further enhances host plant resistance (Peng and Kuc 1992; Levine et al. 1994). MGD peptides act by preferentially integrating into acidic phospholipid bilayers of microbial membranes, thus destabilizing the cell membranes and causing cell lysis. The tospovirus Iris Yellow Spot Virus is an emerging disease of allium crops that is spreading rapidly (Du Toit et al. 2004; Schwartz et al. 2007). DNA sequence information from this virus has been isolated (Pappu et al. 2006), which, in combination with gene-silencing technology, could be used to control this virus in the future. Multiple tospoviruses have already been targeted and successfully controlled in tomato using gene silencing (Bucher et al. 2006). Garlic mosaic virus, caused principally by the potyviruses Leek yellow stripe virus and Onion yellow dwarf virus, is another major viral disease of alliums (Takaki et al. 2005). The development of gene-silencing technology to combat this virus in garlic would

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revolutionize the production of garlic, which currently relies on costly continual regeneration of virus-free meristematic cultures in order to avoid the proliferation of garlic mosaic virus. 4. Insect Resistance. Transgenic garlic containing the Bacillus thuringiensis cry1Ca and H04 hybrid gene constructs produced at Plant Research International (PRI; Wageningen, the Netherlands) showed complete resistance to beet armyworm (Zheng et al. 2004). H. Sweet Corn Diverse maize types are ingredients of a wide range of traditional diets and provide a means for new market opportunities elsewhere in the world (Ortiz et al. 2007). A wide range of vegetable maize products are also harvested before maturity—most important of these are baby corn, sweet corn, and green-pick maize, of which the first two are traded internationally. Initial estimates of the global value of sweet corn, baby corn, and green maize suggest that maize is one of the five most profitable vegetables in the world (Ortiz et al. 2007). The ‘‘big five’’ producers of vegetable maize are China, the United States, Mexico, Peru, and Thailand. Sweet corn appears as the most popular specialty maize due to its high sugar content, conferred by the homozygous recessive sugary1 (su1) genes, in the kernels at the milky stage, which allows its harvest as vegetable (Ortiz et al. 2007). Another recessive mutant, shrunken-2 (sh2), may double the sugar content of the kernels at the roasting-ear stage. Slowing conversion of sugar into starch at ambient temperature reduces the need for refrigeration of the produce after harvest. Sweet corn genotypes combining the recessive allele sugary-enhancer (se) together with su1 can show twice the sugar content and phytoglycogen levels, thereby conferring a creamy texture. The global retail value of vegetable maize is estimated to range from U.S. $13 billion to U.S. $ 2 billion, which ranks second after tomato (U.S. $56 billion) and compares favorably to watermelon, onions, and brassicas (each worth about U.S. $18 billion). In 2004, about 148 countries were involved in the international trade of sweet corn products with a total value in excess of U.S. $573 million (for a total volume of 603,327 t), whereas frozen sweet corn exports of 65 countries included 244,618 t for a total value exceeding U.S. $212 million. Sweet corn, expressing cry1Ab endotoxin, was introduced commercially in the United States in 1998 into an industry that is highly sensitive to damage to corn ears from lepidopteran pests (Lynch et al. 1999). Research showed that this endotoxin was very effective against the European corn borer (Ostrinia nubilalis) in the state of

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New York, providing 100% clean ears when no other lepidopteran species were present and in excess of 97% when the two noctuids, corn earworm (Helicoverpa zea) and fall armyworm (Spodoptera frugiperda), were also present (Musser and Shelton 2003). Studies in other states in the United States have shown that Bt-sweet corn provided consistently excellent control of the lepidopteran pest complex and the potential for 70% to 90% reductions in insecticide requirement (Lynch et al. 1999; Burkness et al. 2001; Hassell and Shepard 2002; Musser and Shelton 2003; Speese et al. 2005; Rose and Dively 2007). Although it was estimated that of the 262,196 ha of sweet corn (fresh and processing) grown in the United States, less than 5% was Bt-sweet corn in 2006 (NASS, 2007); processors have avoided growing Bt-sweet corn due to concerns about export markets. Since then it has been grown only as a fresh-market vegetable crop. By using appropriately timed insecticide applications with Bt-sweet corn cultivars, fresh-market sweet corn growers in South and North Carolina have been able to extend their production later into the season when populations of H. zea and S. frugiperda are generally too high to control satisfactorily with insecticide applications alone (Hassell and Shepard 2002). Even when two insecticide sprays are required on Bt-sweet corn (e.g., for late season control of H. zea), an economic assessment in Virginia found a gain of US$ 1,777 ha1 for fresh-market sweet corn versus non-Bt-sweet corn sprayed up to six times with pyrethroid insecticides (Speese et al. 2005). Bt-sweet corn has also proven to be soft on the major predators of O. nubilalis, including the lady beetles Coleomegilla maculata and Harmonia axyridis, the hemipteran Orius insidiosus (Musser and Shelton 2003; Hoheisel and Fleischer 2007), and a complex of epigeal coleopterans (Leslie et al. 2007). Overall, Bt-sweet corn was much better at preserving these predators while controlling O. nubilalis than were the commonly used insecticides lambda-cyhalothrin, indoxacarb, and spinosad. Bt-sweet corn can replace the traditional method of controlling Lepidoptera with broad-spectrum insecticides. It may, however, allow secondary pests to arise. Results from these studies led to the development of a decision guide for sweet corn growers that uses information on biological control and advises them on the economic return of using various options, including Bt-sweet corn (Musser et al. 2006). These results demonstrate also that some of the new Bt-sweet corn hybrids allow a truly integrated biological and chemical pest control program in sweet corn, making future advances in conservation, augmentation, and classical biological control more feasible. The use of Bt-sweet corn has proven to be very effective against the targeted lepidopteran key pests, and plantings of Bt-sweet corn

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continue to rise in the United States, with new Bt-fresh-market hybrids being released each year. I. Cowpea Cowpea (Vigna unguiculata) remains as the most important legume of sub-Saharan Africa drylands, accounting for about two-thirds of the world’s harvest of this crop and providing a source of protein in the diet of 200 million Africans. Cowpea leaves as well green pods and peas are eaten as fresh vegetables too. Yield losses due to insect pests, particularly the legume pod borer (Maruca vitrata), can exceed 90% in cowpea (Murdock et al. 2001). A Bt transgene conferring resistance to this pod borer, bred into popular African cowpea cultivars, could eliminate the need for spraying insecticides, with significant advantages to smallholder growers (Simiyu-Wafukho et al. 2008). Popelka et al. (2006) adapted features of several legume and other genetic transformation systems to obtain transgenic cowpeas. These follow Mendelian inheritance for transmitting the transgene to their progeny. The rate of transgenic cowpeas that transmit the transgenes to their progeny was 1 fertile plant per 1,000 explants. Their ultimate aim is to incorporate two or more Bt genes into cowpeas to provide long-term protection against legume pod borer. The International Institute of Tropical Agriculture (IITA; Nigeria) and research partners started preliminary biosafety assessments that consider development of resistance by the target insect pest to the insecticidal protein expressed in the plant, negative effects of the insecticidal protein on nontarget organisms in the same agroecosystem (e.g., natural enemies or pollinators), accidental introduction of the gene expressing the toxic protein into wild relatives of cowpea (i.e., gene flow), and negative effects on human and animal health (Tamo 2009). In this regard, Pasquet et al. (2008) found that bees visited wild and domesticated cowpea populations, thereby mediating gene flow and, in some instances, allowing transgene escapes over several kilometers. Nonetheless, as stated by the authors of this gene flow research, most between-flower flights occur within plant patches, while very few occur between plant patches. Furthermore, when the plant patches are at least 50 m apart, the probability of gene flow by pollen appears to be low. Tamo (2009) indicates that there are several alternative host plants in the wild where M. vitrata is exposed to the attacks of natural enemies throughout the year, thereby providing natural refugia and thus avoiding potential negative impacts of the Bt-toxin from transgenic cowpea.

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J. Root Crops 1. Cassava. The root crop cassava (Manihot esculenta) is among the most important vegetatively propagated food crops for tropical agriculture, especially sub-Saharan Africa, but it is also important in Asia and Latin America (Ortiz 2005). The total production for 2007 was 224 million t, with Nigeria and Brazil accounting together for about onethird of the global production. More than 800 million people depend on this starchy root staple, also known as tapioca, manioc, or yuca (not to be confused with the succulent plant yucca) (Nassar and Ortiz 2010). In Africa and Latin America, cassava is used mostly for human consumption, while in Asia and parts of Latin America, it is also used commercially for the production of animal feed and starch-based products. Roots are processed into granules, pastes, and flours or eaten freshly boiled, fermented, or raw. The leaves are also eaten in Africa and some Asian locations as a green vegetable, which provides protein and vitamins A and B. Fregene and Puonti-Kaerlas (2002) highlight the potential of cassava biotechnology, including the potential for a more rapid and efficient improvement through genetic transformation. The first transgenic cassava plants became available in the mid-1990s (Li et al. 1996; Raemakers et al. 1996; Schopke et al. 1996) as plants with reduced cyanogenic content (Siritunga and Sayre 2003, 2004; Siritunga et al. 2004), resistance to infection by geminiviruses (Chellappan et al. 2003), modified starch content (Raemakers et al. 2003), enhanced starch production (Ihemere et al. 2006), elevated protein content within the storage roots (Zhang et al. 2003), and vitamin A (P. Chavarriaga, CIAT, pers. commun.). Transgenic cassava technology represents proof of concept for traits in this species, but its efficacy has been demonstrated only at the laboratory or greenhouse level (Taylor et al. 2004). The delivery of genetically modified planting materials to cassava farmers remains as a main challenge. The impact of transgenic cassava will depend on successfully transferring this capability to local cultivars. In this regard, there are advances for genetically engineering cassava cultivars from Africa (Hankoua et al. 2006; Ingelbrecht 2009) and Brazil (Ibrahim et al. 2008). 2. Sweet Potato. Sweet potato (Ipomoea batatas), the seventh most important food crop, ranks third among root and tuber staples worldwide, after sweet potato and cassava, with China accounting for 65% of total crop area. The total production for 2007 was about 100 million t. The crop is grown at high density in the central Africa highlands. Elsewhere in the tropics it is grown at a lower density. Protocols for

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genetic engineering of sweet potato to express the coat protein gene of Sweet potato feathery mottle virus (SPFMV)—one of the most serious constraints to the production and the quality of this crop when accompanied by other viruses, such as Sweet potato chlorotic stunt virus (SPCSV)—are available (Okada et al., 2001). Researchers at the Kenya Agricultural Research Institute in collaboration with Monsanto incorporated in the 1990s genes for resistance to SPFMV in eight sweet potato cultivars. Field-testing started in 2001 with materials already screened under containment in the greenhouse (Wambugu 2001). Ex ante analysis suggests a benefit ranging from U.S. $42.31 to U.S. $101.12 per acre (Qaim 1998; Marra 2001). Field trials showed, however, that transgenic sweet potatoes were no less vulnerable than ordinary cultivars to this virus, and sometimes their yields were also lower. Recently Cuellar et al. (2009) showed that transformation of an SPFMV-resistant sweet potato cultivar with the double-stranded RNA (dsRNA)-specific class 1 RNA endoribonuclease III (RNase3) of SPCSV broke down resistance to SPFMV, leading to high accumulation of SPFMV antigen and severe symptoms. This is similar to the synergism in plants coinfected with SPCSV and SPFMV. They also indicated that RNase3-transgenic sweet potato plants also accumulated higher concentrations of two other unrelated viruses and developed more severe symptoms than nontransgenic plants. Their research provides some insights on how SPCSV causes the significant loss of sweet potato resistance to SPFMV. Transgenic herbicide-resistant sweet potato plants were also produced using the Agrobacterium-mediated transformation system (Jin Choi 2007). This technology may allow a more convenient and efficient weed control in the field than was previously available. Berberich et al. (2005) were able to breed transgenic sweet potato plants producing mouse adiponectin, an anti-diabetic protein whose large-scale production is sought for pharmaceutical applications. The production of adiponectin did not cause obvious differences in growth rate or morphology in the transgenic sweet potato plants. 3. Carrot. Vegetables offer consumers a diverse mixture of nutrients that promote human health more beneficially than dietary supplements. However, the ingestion of plant-based diets rather than diets that rely primarily on animal products could limit the intake of essential nutrients such as calcium (Ca). Consequently, genetically engineering vegetables containing increased Ca levels may boost Ca uptake, thereby reducing the incidence of Ca deficiencies such as osteoporosis. In this regard, Park et al. (2004) modified carrots to express increased levels of the plant Ca transporter sCAX1. These carrot lines were fertile and displayed no

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adverse phenotypes. Further mice and human feeding trials demonstrated increased Ca absorption from sCAX1-expressing transgenic carrots vis- a-vis controls (Morris et al. 2008). This research supports alternative means of biofortifying vegetables with bioavailable Ca.

IV. GM VEGETABLES AND INTEGRATED PEST MANAGEMENT Integrated pest management (IPM) can be defined broadly as ‘‘the careful consideration of all available pest control techniques and subsequent integration of appropriate measures that discourage the development of pest populations and keep insecticides and other interventions to levels that are economically justified and reduce or minimize risks to human health and the environment. IPM emphasizes the growth of a healthy crop with the least possible disruption to agro-ecosystems and encourages natural pest control mechanisms’’ (FAO 2002). Hence, GM vegetable crops that target one or a few key production pests and pack GM pest management technology into the seed provide a useful tool to be included with other IPM-compatible approaches. The excessive use of insecticides in response to a resistance problem also decreases the effectiveness of biological control agents and increases the risk of environmental and human health impacts, increasing the utility of GM vegetable cultivars with resistance to pests. For example, Musser et al. (2006) in New York State show how Bt-sweet corn combined with the action of auxiliary predators can provide a truly IPM system with only one foliar insecticide required. Both conventionally bred and GM insect-resistant plants have been developed with the objective of reducing pest densities below damage thresholds. If successful, reduced pest densities will inevitably lead to a reduction in the abundance of some natural enemies, particularly the parasitoids and predators that are host/prey specific to the target pest(s). This is an obvious and unavoidable consequence of virtually any pest management system, irrespective of the mechanism, and should not be of particular concern related to the use of GM plants (EFSA 2006; Kennedy and Gould 2007; Romeis et al. 2006, 2008a,b) The advantages of GM technology to improve vegetables, reduce pesticide use, increase yields, add health benefits, and lower production costs should provide incentive for integration of this technology into vegetable breeding and commercial crop production, if consumer resistance can be overcome or mollified. It would be expected that as consumers become more accustomed to other GM crops, concerns about GM vegetables are likely to lessen, and markets will accept the new products.

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However, the opposition to GM crops is well organized by advocates of the environmental and the organic movements. Vegetables, as minor crops by themselves, are unable to lead the campaign to change consumer acceptance of GM vegetables The production of vegetables worldwide tends to be on smaller areas and in more diversified holdings than field crops such as cotton, maize, soybean, rice, and wheat. Vegetables are often in more complex agricultural systems where insects may move from one crop to the next within the same farm. How this will impact the use and effects of GM vegetable plants in the agricultural landscape can be complex. Growing multiple insect-resistant GM vegetable plants in the same area and exposed of a polyphagous insect to the same Bt protein expressed in the different vegetable species will challenge conventional strategies developed for GM cotton or maize cultivars. Thoughtful consideration therefore will be needed before choosing which toxins vegetable plants should express. The selection should be based not only on what will be an effective toxin against the target insect but what toxins are already in use in other vegetable crops that may be hosts for the target insect. Additionally, the difficulty of sampling insect populations for resistant alleles will take on a higher level of complexity in a diversified vegetable system. Further consideration should also be given to the effects on nontarget organisms within diversified GM vegetable plantings. In a study conducted in the northeastern United States, Hoheisel and Fleischer (2007) investigated the seasonal dynamics of coccinellids and their food (aphids and pollen) in a vegetable farm system containing plantings of Bt-sweet corn, Bt-potato, and GM insect-resistant squash. Their results indicated that the transgenic vegetable crops provided conservation of cocinellids and resulted in a 25% reduction in insecticide use. In a similar study with these same crops, Leslie et al. (2007) compared the soil surface–dwelling communities of Coleopetera and Formicidae in the transgenic crops and their isolines and found no differences in species richness and species composition but found that the transgenic vegetables required fewer insecticide applications. Such results make clear that GM technology can be introduced within vegetable IPM systems and that GM vegetables can offer novel and effective ways of controlling insects and the pathogens they transmit. Virus-resistant transgenic plants are particularly valuable if no genetic source of resistance has been identified or if host resistance is difficult to transfer into elite cultivars by traditional breeding approaches due to genetic incompatibility or links to undesired traits. In such cases, engineered resistance may be the only viable option to develop virusresistant cultivars. Growers can also use virus-resistant transgenic

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vegetables as a trap crop by growing it as a border around the non-GM vegetable crop and allowing it to cleanse viruliferous aphids, as it is done in Hawaii with Papaya ringspot virus (PRSV)-resistant transgenic papaya (Gonsalves 1998; Fuchs and Gonsalves 2007). In Hawaii, the papaya industry—after two decades of field and biosafety testing—can now produce and market both transgenic and conventional papaya in the same field and even organic papaya in adjacent fields if other organic practices are performed. This is a case in which organic agriculture directly benefits from GM crops, which are not allowed as part of the organic production philosophy. In small, diversified vegetable plantings typical of those found throughout the developing world, the challenges for regulatory oversight of GM plants are immense. In these countries, farmers will likely save GM seed and move GM seed between locations, and some GM products may move into markets that do not permit these products. These concerns will be lessened if GM vegetable plants are consumed locally and in accordance with national biosafety regulatory policies. However, it is likely that violations will occur, and this will challenge legal systems. While each vegetable has its own set of one or more key pests, other pests can also be problematic. Traditional broad-spectrum insecticides often control a suite of pest insects. Thus, when Bt- or other GM vegetables are introduced into production systems, other methods of control will have to be applied or developed for secondary pests. Because the current GM technologies have proven to be less harmful to natural enemies, biological control of secondary pests may be more achievable, but other tactics, such as the use of selective insecticides, applied either as seed treatments or foliar sprays, may be necessary (Romeis et al. 2006, 2008a,b). In conclusion, GM vegetables can have a major role in the management of insects and the diseases they transmit. When the markets have allowed the production of GM plants, farmers have readily adopted the technology as part of their pest management practices. This is likely to continue with GM vegetables. IPM could benefit from some herbicide-resistant crops, if alternative nonchemical methods can be applied first to control weeds and the specific herbicide could be used later, only when and where the economic threshold of weeds is surpassed (Krimsky and Wrubel 1996). Generally, though, the use of herbicide-resistant crops will lead to increased use of herbicides and environmental and economic problems (Altieri 1998; McCullum et al. 1998; Pimentel and Ali 1998). Repeated use of herbicides in the same area may also create problems of weed herbicide resistance (Wrubel and Gressel 1994). In addition, farmers will suffer because of the high costs of employing herbicide-resistant

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crops—in some instances, weed control with herbicide-resistant crops may increase weed control costs for the farmer twofold (Pimentel and Ali 1998).

V. OUTLOOK Both pesticides and biotechnology have definite advantages in reducing crop losses to pests. At present, pesticides are used more widely than biotechnology, and thus they are playing a greater role in protecting world food supplies. In terms of environmental and public health impacts, pesticides probably have a greater negative impact at present because of their more widespread (and sometimes careless) use. GM vegetable crops for resistance to insect pests and plant pathogens could, in most cases, be environmentally beneficial, because these more resistant crops could allow a reduction in the use of hazardous insecticides and fungicides in crop production. In time, there may also be economic benefits to farmers who use genetically engineered crops; this will depend, though, on the prices charged by the biotechnology firms for these modified, transgenic crops. There are, however, some environmental problems associated with the use of genetically engineered crops in agriculture, as discussed. A major environmental and economic concern associated with genetically engineered crops may be the development of herbicide-resistant crops. Although in rare instances herbicide-resistant crops may result in a beneficial reduction of toxic herbicide use, it is more likely that the use of herbicide-resistant crops can increase herbicide use and environmental pollution. Of great interest and importance for the future of GM vegetables will be the course set by developing countries, since nearly 60% of the world’s vegetables are grown in China and India, which account for nearly 40% of the world’s population and where pest and viruses are severe. Both countries have readily adopted Bt-cotton, and it is likely that Bt-rice will be commercialized in China in the very near future, since China is the first country in the world to give biosafety approval (BSA) for the development of Bt-rice cultivars. Acceptance of GM field crops in these two large, highly populated countries will make it more likely they will adopt GM vegetables. This in turn likely will hasten their adoption in other parts of the world and allow farmers to use this technology. With the eventual acceptance of GM technology, it is expected that the costs associated with deregulation will become more affordable and that the biotechnology industry, in the hands of huge corporations, will become

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more interested in developing GM vegetables, especially for the developing world, where more than 80% of the world’s 6.8 billion people live. These populations will increase rapidly in the next several decades. Reasonable profit margins are necessary to pay back the research-fordevelopment costs, to fund future research on developing even better GM vegetable cultivars, and to stay competitive. The proportion of the economic benefits that accrue to the farmer, the consumer, and the technology company or corporation also varies among countries, depending on the degree of protection provided for intellectual property rights and the degree of government control over commodity prices. In the United States, plant breeding companies can take advantage of the U.S. utility patent law to protect not only the cultivar itself but all of the plant’s parts. Such product protection options have presented a business incentive to corporations to invest in the seed industry, leading to an enormous increase in private research and development, insuring strong competition in the marketplace among the major seed companies. Such patenting must be moderated to eliminate coverage so broad that it stifles innovation. Direct health benefits accrue from the reductions in insecticide use on Btcrops and other virus-resistant transgenic vegetables as a result of lower pesticide residues in food and water, and reduced exposure of farm workers and vegetable growers during pesticide applications. These benefits are especially great in developing countries in which pesticide regulation is weak, the education of farmers is generally low, and pesticides are usually applied manually. The full potential of GM technology to reduce exposure to pesticide residues in foods as not yet been realized because pesticide residues on food are of greatest concern in vegetables, and few insect-resistant GM vegetable crops are commercially available. Developing country public research is focused on crops for the poor and traditionally has been considered a government investment, with returns coming back to the public in the form of food security, better health, and greater subsistence farmer income, compared to product research by the private sector. Much of this research, however, has been supported by foundations and governments in the developed world. Unfortunately, support resources have diminished in the last few decades. The challenge, therefore, especially for developing country regulatory agencies, is to examine where data collection requirements can be reduced or streamlined without compromising the level of safety achieved by current developed world regulatory requirements, in order that the investments made by governments are fully realized. The GM eggplant in India is an excellent working example of a model pro-poor

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philanthropic-public-private sector partnership. Bt-egg plant technology has been generously donated by its private sector developer, Mahyco, to public sector institutes in India, Bangladesh, and the Philippines for incorporation in open-pollinated cultivars of eggplant for the use of farmers and especially small, resource-poor farmers. The regulation of Bt-eggplant in India is the key barrier that denies growers in this country timely access to the significant benefits that this biotech vegetable crop offers. Sharing of knowledge and of experience with the regulation process could greatly simplify and lighten the regulatory burden by eliminating duplication of this significant effort, thereby contributing to the important goal of harmonizing simplified, responsible, and appropriate regulations among countries. Molecular tools will be useful for selecting resistance genes and increasing quality, nutritional value, and yields. These value-added traits plus food safety will be important aspects of future GM vegetable breeding efforts. Biotechnology provides the ability to produce a broad array of insect-resistant and pathogen-resistant cultivars that also express a variety of other value-added traits, such as nutritional and postharvest traits. As the number of value-added, GM traits increases, the number of potential combinations of traits that could be stacked within individual cultivars increases geometrically, as to the cost associated with maintaining inventories of geographically adapted cultivars expressing different combinations of traits. Consequently, we can expect that commercially available, GM vegetable cultivars of the future will express multiple, unrelated, transgenic traits, and farmers in many cases likely will not have the option of planting cultivars expressing only single traits. To the extent that this occurs, insect-resistant GM vegetable crops are likely to be widely used in situations where they are neither needed nor appropriate. Then the decision to use an insect-resistant GM vegetable crop must be made prior to planting. It involves weighing the cost of implementing the technology against the risk of experiencing a yield-suppressing infestation of the targeted pest species during the season. The costs of using a GM vegetable crop for crop protection include both the fee premium charged for the GM trait and the costs, if any, associated with any undesirable agronomic characteristics of the GM cultivar compared to non-GM cultivars. The availability of transgenic vegetable crops does not, however, ensure that they will be adopted by growers (Ortiz and Smale 2007). To be widely adopted, the benefits of their adoption must exceed their costs for a large proportion of vegetable growers from one season to the next. As suggested by this chapter, the most promising traits seem to be host plant resistances to insects and pathogens,

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5 Millets: Genetic and Genomic Resources Sangam Dwivedi, Hari Upadhyaya, Senapathy Senthilvel, and Charles Hash International Crops Research Institute for the Semi-Arid Tropics Patancheru PO Hyderabad 502324, AP, India Kenji Fukunaga Faculty of Life and Environmental Sciences Prefectural University of Hiroshima 562 Nanatsuka, Shobara Hiroshima 727-0023, Japan Xiamin Diao Lab of Minor Cereal Crops Institute of Crop Sciences Chinese Academy of Agricultural Sciences 12 Zhongguancun South Street, Haidian Beijing 100081, People’s Republic of China Dipak Santra University of Nebraska–Lincoln Panhandle Research and Extension Center 4502 Avenue I Scottsbluff, Nebraska 69361, USA David Baltensperger Soil and Crop Sciences Texas A&M University 2472 TAMU College Station, Texas 77843-2474, USA Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick.
2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 247

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Manoj Prasad National Institute of Plant Genome Research Aruna Asaf Ali Marg JNU Campus, PO Box 10531 New Delhi 110067, India

ABSTRACT Small-grained millets, comprising ten annual grasses from the family Poaceae and grown for grain, contribute
13% of annual global cereal production. Some are widely grown, while cultivation of others is restricted. They differ in ploidy, genome size, and breeding system, but their grains are all highly nutritious. Their most common nonfood uses are in brewing and as livestock feeds. Millets are C4 plants adapted to marginal lands in hot, drought-prone arid and semiarid regions. Selection for plant phenology and architecture, panicle shape, spikelet structure and reduced shattering, seed dormancy, and seed coat hardness contributed to their domestication. Approximately 161,708 millet accessions are preserved in gene banks globally. These show exceptional diversity associated for phenology, photoperiod sensitivity, tolerance to abiotic stresses, resistance to biotic stresses, seed storability and shelf life, and specific grain characteristics associated with end user preferences. Contributions from wild relatives’ toward enhancing cultivated gene pools have been limited to pearl millet and foxtail millet. Core or minicore/reference collections have been used to identify new sources of biotic stress resistances and abiotic stress tolerances. Waxy mutants have been selected in barnyard millet, foxtail millet, and proso millet for specific food uses. Pearl millet hybrids and open pollinated varieties (OPVs) with high iron and zinc grain densities will soon be available in India. While no transgenic work has reached field level, DNA markers are routinely used to assess millets’ population structure and genetic diversity. Genetic maps of varying density are reported in finger millet, foxtail millet, pearl millet, proso millet, and tef. Major quantitative trait loci associated with resistance to downy mildew, rust, and blast and tolerance to terminal drought stress have been backcrossed into elite inbred pearl millet hybrid parents. Markerassisted backcrossing has been used to improve downy mildew resistance in pearl millet. Cytoplasmic-genetic male sterility (CMS)–based hybrids of pearl millet are extensively cultivated, and CMS systems for foxtail millet are under development. An aligned genome sequence of foxtail millet will be released in the near future as this millet is closely related to several polyploid bioenergy grasses. This foxtail millet genome sequence is highly syntenic with those of rice, sorghum, and maize, which should allow comprehensive surveys of genetic diversity for identifying and conserving diversity in grass germplasm with bioenergy crop potential.

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KEYWORDS: diversity; domestication; genetic markers; genome synteny; phylogeny; population structure; quantitative trait loci; stress tolerance LIST OF ABBREVIATIONS I. INTRODUCTION II. NUTRITIONAL QUALITY AND FOOD, FEED, MEDICINAL, AND OTHER USES III. DOMESTICATION, PHYLOGENETIC, AND GENOMIC RELATIONSHIPS IV. ASSESSING PATTERNS OF DIVERSITY IN GERMPLASM COLLECTIONS V. IDENTIFYING GERMPLASM WITH BENEFICIAL TRAITS A. Resistance to Biotic Stresses 1. Phenotypic Screening 2. Natural Genetic Variation 3. Pathogen Variability, Mechanism, and Genetics of Resistance B. Tolerance to Abiotic Stresses 1. Drought 2. Salinity 3. Low Temperature 4. Lodging 5. Waterlogging C. Seed Quality VI. GENOMIC RESOURCES A. Markers and Genetic Linkage Maps B. Characterization and Functional Validation of Genes Associated with Important Traits C. Genomic and Genetic Tools to Sequence the Foxtail Millet Genome VII. ENHANCING USE OF GERMPLASM IN CULTIVAR DEVELOPMENT A. Core, Mini-Core and Reference Sets for Mining Allelic Diversity and Identifying New Sources of Variation B. Assessing Population Structure and Diversity in Germplasm Collections C. Promoting Use of Male Sterility as an Aid in Crossing VIII. FROM TRAIT GENETICS TO ASSOCIATION MAPPING TO CULTIVAR DEVELOPMENT USING GENOMICS A. Markers/QTL Associated with Agronomic Traits, Abiotic Stress Tolerance, Biotic Stress Resistance, and Product Quality B. Marker-Aided Introgressions of Disease Resistance C. Marker-Aided Introgressions to Enhance Drought Tolerance D. Use of Rice, Maize, Sorghum, and Foxtail Millet Genome Sequences to Strengthen Molecular Breeding Tools E. Exploiting Variation at Waxy Locus to Diversify Food Uses F. Foxtail Millet, Sorghum and Maize Genome Sequences as Resources for Identifying Variation Associated with High Biomass Production in Bioenergy Grasses IX. CONCLUSIONS AND FUTURE PROSPECTS ACKNOWLEDGMENTS LITERATURE CITED

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LIST OF ABBREVIATIONS AFLP AICPMIP BEP BP Bp cDNA cDNA–AFLP CISP CMS CO2 DArT DNA DM EST FAO WHO Fe GBSS I GCP HDL ISSR ITS LDL LG MABC Mbp MRL mRNA Na NC7 NSSL OA PACCAD PCR PGQO P5C QTL QTL-NIL

Amplified fragment length polymorphism All India Coordinated Pearl Millet Improvement Project Bambusoideae, Ehrhartoideae, Pooideae Before present Base pair Complementary deoxyribonucleic acid Complementary deoxyribonucleic acid–amplified fragment length polymorphism Conserved intron scanning primers Cytoplasmic-genetic male sterility Carbon dioxide Diversity arrays technology Deoxyribonucleic acid Downy mildew Expressed sequence tag Food and Agriculture Organization World Health Organization Iron Granule-bound starch synthase I Generation Challenge Program High-density lipoprotein Inter-simple sequence repeats Internal transcribed spacer Low-density lipoprotein Linkage group Marker-assisted backcrossing Million base pair Maximum root length Messenger ribonucleic acid Sodium North Central Regional PI Station National Center for Genetic Resource Preservation Osmotic adjustment Panicoideae, Arundinoideae, Chloridoideae, Centothecoideae, Aristidoideae, Danthonioideae Polymerase chain reaction Plant Germplasm Quarentine Program Pyrroline-5-carboxylate Quantitative trait loci QTL near-isogenic line

5. MILLETS: GENETIC AND GENOMIC RESOURCES

RAPD rDNA RFLP RILs S9 SNP SSCP–SNP SSR TILLING Tr UPGMA VPD W6 WUE Zn

251

Rapid amplified polymorphic DNA Ribosomal deoxyribonucleic acid Restriction fragment length polymorphism Recombinant Inbred Lines Southern Regional PI Station Single-nucleotide polymorphism Single-strand conformation polymorphism–single nucleotide polymorphism Simple sequence repeat Targeting Induced Local Lesions in Genomics Transpiration rate Unweighted pair group method arithmetic mean Vapor pressure deficit Western Regional PI Station Water use efficiency Zinc

I. INTRODUCTION Cereals (rice, wheat, maize, barley, sorghum, millets, oats, rye, and triticale) contributed on average 255.1 million tonnes annually to world food production during the period from 2004 to 2008, of which the millet share was 12.7% (32.3 mt). Millets are comprised of a number of smallgrained, annual cereal grasses that include several distinct species: pearl millet (Pennisetum glaucum), finger millet (Eleusine coracana), foxtail millet (Setaria italica), proso millet (Panicum miliaceum), little millet (Panicum sumatrense), barnyard millet [Echinocloa crus-galli (Japanese) and E. colona (Indian)], kodo millet (Paspalum scrobiculatum), tef (Eragrotis tef), fonio [Digitaria exilis (white fonio) and D. iburua (black fonio)], guinea millet (Brachiaria deflexa), and Job’s tears (Coix lacrymajobi). Taxonomically, these millets belong to the Poaceae but differ either at species, genus, tribe, or subfamily hierarchy; ploidy levels (pearl millet and foxtail millet are diploids; finger millet, proso millet, tef, fonio, and Job’s tears are tetraploids; barnyard millet is hexaploid); genome size [foxtail millet has the smallest genome, 490 million base pair (Mbp) (Bennett et al. 2000) while finger millet, 2509 Mbp (Bennett and Leitch 1995) and pearl millet, 2352 Mbp (Bennett et al. 2000) have the largest genomes among other millets studied for genome size variation); and breeding systems (pearl millet being highly outbreeding, Job’s tears with mixed mating—inbreeding and outbreeding, and the

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remaining millets with high levels of inbreeding with some outcrossing (0.3%– 4%) in foxtail millet, Setaria italica, and its wild ancestor, S. virdis (Li et al. 1945; Till-Bottraud et al. 1992) (Table 5.1). Natural outcrossing in the range of 0.2% to 1% has also been reported for tef (Ketema 1993). Wild relatives of these millets possess even greater taxonomic diversity. For example, barnyard millet relatives vary from tetraploid to octaploid; those of finger millet are all diploid; relatives of foxtail millet and Job’s tears vary from diploid to octaploid; those of pearl millet from diploid to hexaploid; while kodo millet, little millet, proso millet, and tef are tetraploid (Table 5.2). Furthermore, both sexual and asexual (apomictic) forms of reproduction have been reported among pearl millet’s wild relatives. Most of these wild species are annuals; however, some of the foxtail millet and pearl millet wild relatives have both annual and perennial life-forms (Table 5.2). Other minor millets include Brachiara ramosa, Setaria glauca, Echinochloa turneriana, Echinochloa oryzicola, and Panicum hirticaule var. hirticaule (Hirosue and Yabuno 2002; Kimata et al. 2000). Brachiara ramosa is cultivated in pure stands while Setaria glauca in mixed stands along with little millet, and the grains are used as traditional foods in southern India (Kimata et al. 2000). The cultivated form of E. oryzicola is characterized by large spikelets with nonshattering habit and no innate dormancy (Hirosue and Yabuno 2002). The millets have abundant within-species racial diversity. In finger millet, there are five races (coracana, which resembles the subsp. africana, vulgaris, compacta, plana, and elongata) (Dida and Devos 2006) and 10 subraces (laxa, reclusa, and sparsa in elongata; seriata, confundera, and grandigluma in plana; liliacea, stellata, incuriata, and digitata in vulgaris). The race compacta in finger millet has no subraces. Foxtail millet has three races (moharia, maxima, and indica) and ten subraces (aristata, fusiformis, and glabra in moharia; compacta, spongiosa, and assamense in maxima; and erecta, glabra, nana, and profusa in indica). Proso millet has five races: miliaceum, patentissimum, contractum, compactum, and ovatum, while little millet (subsp. sumatrense) has two races, nana and robusta, each with two subraces: laxa and erecta in the former and laxa and compacta in the latter. Barnyard millet has two cultivated species, the Indian barnyard millet (Echinocloa colona) and Japanese barnyard millet (E. crus-galli), each with two ssp.: colona and frumentacea in the former and crus-galli and utilis in the latter. Subspecies colona has no races, while ssp. frumentacea has four races: stolonifera, intermedia, robusta, and laxa. Both ssp. crus-galli and utilis each have two races: crus-galli and macrocarpa in the former and utilis and intermedia in the latter. The three races in kodo millet are

253

Subfamily

Panicoideae

Chloridoideae

Panicoideae

Panicoideae

Maydeae

Panicoideae Panicoideae

Panicoideae

Panicoideae

Chloridoideae

Barnyard millet

Finger millet

Fonio

Foxtail millet

Job’s tears

Kodo millet Little millet

Pearl millet

Proso millet

Tef

Eragrosteae

Paniceae

Paniceae

Paniceae Paniceae

Andropogoneae

Paniceae

Paniceae

Eragrosteae

Paniceae

Tribe

Eragrostis

Panicum

Pennisetum

Paspalum Panicum

Coix

Setaria

Digitaria

Eleusine

Echinochloa

Genus

E. tef

P. miliaceum

P. glaucum

P. scrobiculatum P. sumatrense

C. lacryma-jobi

S. italica

D. exilis D. iburua

E. colona E. crus-galli E. coracana

Species

Taxonomic relationships of ten cereals belonging to millets group of crops.

Common name

Table 5.1.

Tetraploid

Tetraploid

Diploid

Tetraploid

Tetraploid

Diploid

Tetraploid

Tetraploid

Hexaploid

Ploidy

40

36

14

36

20

18

36

36

36

Chrom. no.

Wanous 1990; de Wet et al. 1983 Wanous 1990; Bisht and Mukai 2001 Adoukonou-Sagbadja et al. 2007; Wanous 1990 Wanous 1990; Bennett et al. 2000 Clayton 1981; Wanous 1990 Wanous 1990 Wanous 1990; Hiremath et al. 1990 Wanous 1990; Bennett et al. 2000 Baltensperger 1996; Hiremath et al. 1990; Zeller 2000 Wanous 1990; Ingram and Doyle 2003

Reference

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Finger millet E. indica (A genome) E. floccifolia E. tristachya E. intermedia E. verticillata E. multiflora E. jaegeri E. coracana subsp. africana E. spontanea E. kigeziensis

E. oryzoides

E. crusgalli

Barnyard millet E. colona

Species

18 18 18 18 18 16 20 36 Not reported 36

Diploid Diploid Diploid Diploid Diploid Diploid Tetraploid

Not reported Tetraploid

36

36, 54

36, 54, 72

Chromosome number

Diploid

Tetraploid, hexaploid, octaploid Tetraploid, hexaploid Tetraploid

Ploidy

Sexual Not reported

Not reported Not reported Not reported Not reported Not reported Not reported Sexual

Sexual

Sexual

Sexual

Reproductive behavior

Inbreeder Not reported

Not reported Not reported Not reported Not reported Not reported Not reported Inbreeder

Not reported

Inbreeder

Inbreeder

Mating system

Annual Perennial

Perennial Annual Perennial Not reported Annual Perennial Annual

Annual

Annual

Annual

Life form

Table 5.2. Differences in ploidy level, chromosome number, reproductive behavior, mating system and life form among selected wild relatives of millets species.

NRC 1996; Bisht and Mukai 2001; Neves et al. 2005; Anderson and de Vicent 2010

Wanus 1990; de Wet et al. 1983

Reference

255

Foxtail millet S. virdis (A genome) S. faberii (AB genome) S. verticillata (AB genome) S. glauca (S. pumela) S. adhaerans (B genome) S. holstii S. woodii S. chevalieri S. incrassata S. leiantha S. neglecta

Fonio D. longiflora D. ternata D. lecardii D. ciliaris reported reported reported reported

Sexual Sexual

36, 54 36–72 18 18 18 36 36 36 36

Tetraploid and hexaploid Complex ploidy

Diploid

Diploid Diploid Tetraploid Tetraploid Tetraploid Tetraploid

Sexual Sexual Sexual Not reported Not reported Not reported

Sexual

Sexual

36

Sexual

Not Not Not Not

Tetraploid

reported reported reported reported

18

Not Not Not Not

Diploid

Not reported Not reported Not reported Not reported

Inbreeder Not reported Not reported Not reported Not reported Not reported

Inbreeder

Inbreeder

Inbreeder

Inbreeder

Inbreeder

Not reported Not reported Not reported Not reported

Perennial Not reported Perennial Not reported Not reported Not reported

Annual

Not reported

Annual

Annual

Annual

Not reported Not reported Not reported Not reported

(continued )

Hacker 1967; Till-Bottraud et al. 1992; Le Thierry d’Ennequin et al. 1998; Benabdelmouna et al. 2001a; Wang et al. 2007b; Jia et al. 2009a; Wang et al. 2009; http://database. prota.org

Adoukonou -Sagbadja et al. 2007

256

palmifolia parviflora sphacelata macrostachya pumila

Job’s tears C. aquatica C. aquatica C. aquatica C. aquatica

S. finita S. sphacelata S. grisebachii (C genome) S. queenslandica (AA genome) S. verticillata (B genome) S. leucopila (A genome)

S. S. S. S. S.

Species

Table 5.2 (Continued)

18 18

Diploid

Diploid

10 20 30 40

36

Tetraploid

Diploid Tetraploid Hexaploid Octaploid

Not reported Not reported 18

36 36 18 to 90 54 36, 54

Chromosome number

Tetraploid Tetraploid Complex ploidy Hexaploid Tetraploid and hexaploid Not reported Not reported Diploid

Ploidy

Not Not Not Not

reported reported reported reported

Sexual

Not reported

Sexual

Not reported Not reported Sexual

Not reported Not reported Sexual Not reported Sexual

Reproductive behavior

Not reported Not reported Not reported Not reported

Inbreeder

Not reported

Inbreeder

Not reported Not reported Inbreeder

Not reported Not reported Outbreeder Not reported Inbreeder

Mating system

Not reported Not reported Not reported Not reported

Annual

Not reported

Annual

Not reported Not reported Annual

Perennial Perennial Perennial Perennial Annual

Life form

Reviewed in Han et al. 2004

Reference

257

Tetraploid Triploid Hexaploid Tetraploid Tetraploid Tetraploid Diploid Hexaploid

P. P. P. P. P. P. P. P.

28 27 54 36 36 36 16 54

14 14 10

Diploid Diploid Diploid

purpureum setaceum setaceum villosum pedicellatum orientale mezianum squamulatum

14

36 36

49

Diploid

Tetraploid Tetraploid

Tetraploid

P. glaucum ssp. monodii P. violaceum P. mollissimum P. ramosum

Pearl millet

Little millet P. sumatrense P. psilopodium

Kodo millet Paspalum scrobiculatum

Sexual Sexual sexual and apomictic Sexual Apomictic Apomictic Apomictic Sexual Sexual Sexual Apomictic

Sexual

Sexual Sexual

Sexual

Inbreeder Inbreeder Inbreeder Inbreeder Inbreeder Inbreeder Inbreeder Inbreeder

Inbreeder Inbreeder Inbreeder

Inbreeder

Inbreeder Inbreeder

Inbreeder

Annual Annual Annual, Biennial Perennial Perennial Perennial Perennial Annual Perennial Perennial Perennial

Annual

Annual Annual

Annual

(continued )

Martel et al. 1997; http:// cropgenebank. sgrp.cgiar.org

Wanous 1990; Hiremath et al. 1990; Wanous 1990

Wanous 1990

258

Tetraploid

Tetraploid Not reported Not reported Not reported Not reported Not reported Not reported Not reported

Tef E. pilosa E. cilianensis E. ciliaris E. curvula E. cylendriflora E. gengetica E. tremula E. turgida

Ploidy

Proso millet P. miliaceum

Species

Table 5.2 (Continued)

40 Not Not Not Not Not Not Not

36

reported reported reported reported reported reported reported

Chromosome number

Not Not Not Not Not Not Not Not

reported reported reported reported reported reported reported reported

Sexual

Reproductive behavior

Not reported Not reported Not reported Not reported Not reported Not reported Not reported Not reported

Inbreeder

Mating system

Not reported Not reported Not reported Not reported Not reported Not reported Not reported Not reported

Annual

Life form

http://database. prota.org

Baltensperger 1996

Reference

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regularis, irregularis and variabilis. All these races and subraces can be recognized by variation in panicle morphology (Prasad Rao et al. 1993). The two most recognized and widely cultivated species in fonio are white and black fonio, differentiated by seed color (Murdock 1959). The millets growing area worldwide has declined by 18% over a period of 45 years, from the average of 43.7 million ha in 1964 to 1968 to 35.82 million ha in 2004 to 2008; however, production during the same period has increased by 20.5%, from 26.9 million t in 1964 to 1968 to 32.3 million t in 2004 to 2008, largely due to increased productivity, which raised from 0.61 t ha1 in 1964 to 1968 to 0.9 t ha1 in 2004 to 2008 (Table 5.3). Globally, the millets are grown in 90 countries (http:// faostat.fao.org/). The major countries for production of millets are India, China, Nepal, Pakistan, and Myanmar in Asia; Burkina Faso, Cameroon, Chad, Ghana, Kenya, Mali, Namibia, Niger, Nigeria, Senegal, Sudan, Tanzania, Togo, Uganda, and Zimbabwe in sub-Saharan Africa; and Argentina and the United States on the American continent (Table 5.4). The production trends of 45 years (1964–2008) from these countries reveal interesting patterns. For example, China recorded the highest average annual production of 8.4 million t during the 1969–1973 period, which gradually declined to 1.7 million annual t in the period between 2004 and 2008. In contrast, India has shown a consistently upward trend in millets production, with marginal variation, increasing from 7.8 million t annually in the 1964 to 1968 period to 11.1 million t annually between 2004 and 2008 (i.e., an increase of
43%). The increased production of millets in India, particularly pearl millet with substantial production, is due to large-scale adoption of hybrid cultivars with inherent resistance/tolerance to biotic and/or abiotic stresses, which Table 5.3. Five-yearly averages of world area, production, and productivity of millets for the period from 1964 to 2008. Year 1964–1968 1969–1973 1974–1978 1979–1983 1984–1988 1989–1993 1994–1998 1999–2003 2004–2008

Area (million ha)

Production (million tons)

Yield (t ha1)

43.71 44.25 40.61 37.26 36.75 37.10 36.59 35.77 35.82

26.84 29.94 27.52 26.67 27.26 28.12 27.81 28.57 32.34

0.61 0.68 0.68 0.72 0.74 0.76 0.76 0.80 0.90

Source: http://faostat.fao.org.

260

1964–1968

Source: http://faostat.fao.org.

South and Southeast Asia Afghanistan 0.024 Bangladesh 0.050 China 7.946 India 7.791 Myanmar 0.044 Nepal 0.108 Pakistan 0.386 Sub-Saharan Africa Burkina Faso 0.325 Cameroon 0.082 Chad 0.290 Ghana 0.074 Kenya 0.133 Mali 0.433 Namibia 0.020 Niger 0.875 Nigeria 2.435 Senegal 0.427 Sudan 0.299 Tanzania 0.119 Togo 0.133 Uganda 0.545 Zimbabwe 0.215 American continent Argentina 0.188 USA 0.137 CIS countries Ukraine 0.000 Russia 0.000

Country 0.035 0.043 6.454 9.491 0.050 0.137 0.304 0.360 0.090 0.241 0.128 0.129 0.485 0.030 0.947 3.175 0.521 0.458 0.231 0.096 0.598 0.186 0.278 0.088 0.000 0.000

0.319 0.083 0.236 0.113 0.130 0.418 0.026 0.894 3.041 0.400 0.382 0.131 0.132 0.701 0.186

0.167 0.137

0.000 0.000

1974–1978

0.029 0.056 8.356 9.901 0.044 0.132 0.335

1969–1973

0.000 0.000

0.214 0.112

0.401 0.090 0.163 0.117 0.062 0.511 0.036 1.307 2.570 0.486 0.339 0.358 0.047 0.473 0.131

0.032 0.055 6.299 9.677 0.122 0.120 0.248

1979–1983

0.000 0.000

0.112 0.164

0.617 0.047 0.238 0.135 0.050 0.775 0.047 1.274 3.780 0.565 0.304 0.304 0.072 0.467 0.169

0.026 0.088 5.300 8.754 0.172 0.147 0.222

1984–1988

0.260 1.331

0.081 0.178

0.726 0.061 0.216 0.140 0.059 0.752 0.043 1.675 4.624 0.567 0.245 0.235 0.071 0.598 0.106

0.023 0.064 3.814 10.009 0.129 0.239 0.176

1989–1993

0.220 0.617

0.051 0.190

0.791 0.064 0.282 0.175 0.044 0.760 0.063 1.848 5.572 0.534 0.622 0.274 0.055 0.565 0.076

0.022 0.057 3.143 10.102 0.146 0.274 0.192

1994–1998

0.268 0.773

0.035 0.291

0.972 0.052 0.378 0.160 0.057 0.885 0.060 2.328 5.948 0.575 0.588 0.189 0.045 0.591 0.040

0.021 0.028 2.106 10.227 0.168 0.282 0.207

1999–2003

0.200 0.660

0.014 0.319

1.106 0.060 0.497 0.163 0.068 1.136 0.060 2.874 7.745 0.469 0.644 0.226 0.043 0.707 0.048

0.017 0.016 1.746 11.142 0.181 0.288 0.251

2004–2008

Table 5.4. Five-yearly averages of the millets production from the major millets producing countries in South and Southeast Asia, sub-Saharan Africa, the American continent, and CIS countries for the period from 1964 to 2008.

5. MILLETS: GENETIC AND GENOMIC RESOURCES

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have shown 25% to 30% yield advantage over open-pollinated varieties (Gowda and Rai 2006), while maize largely replaced millets in large acreage in China mainly due to its high yield potential, ease of cultivation, and better agronomic management practices including use of herbicides, thus reducing production cost (Diao 2007). Production of millets in Nepal almost tripled from the 1964–1968 period to the 2004–2008 period. In sub-Saharan Africa, Burkina Faso, Chad, Niger, Nigeria, Mali, Senegal, and Uganda are the largest producing countries, recording consistently increasing production. For example, millets production increased by 218% in Nigeria and by 240% in Burkina Faso, largely because of increased productivity (Table 5.4). Although the millet production in Niger and Mali increased by 228% and 162%, respectively, this increase probably was largely due to increased acreage. In many other sub-Saharan African countries, however, production either remained stagnant or has declined since the 1960s. The millets in these countries are still grown on marginal lands, low in soil fertility, poor crop management practices adopted, and unavailability of seeds of improved cultivars. The millets production in Argentina and America also showed variable trends. Production in Argentina reached its highest peak in the 1970s and then declined rapidly, with an average annual production of only 14,000 t for the 2004–2008 period. Annual millets production in the United States, except for periods in the 1970s and early 1980s, largely remained between 137,000 t to 319,000 t, and the highest average annual production was recorded for the period between 2004 and 2008. Millets production in Ukraine remained at below 300,000 t annually for the last 20 years while production declined by 50.4% in Russia. The economic development around the world brought dietary changes—those of hunter-gatherers containing large amounts of fiber and low amounts of sugar and fat to energy diets composed predominantly of highly processed foodstuffs, driven by a variety of culturally specific factors, including the increased production, availability, and marketing of processed foods and the complex effects of urbanization (Drewnowski and Popkin 1997; Popkin 2004, 2006; Finnis 2007). Global food consumption patterns have been shifting from food grains to highvalue crops/animal products in developing countries while it is from animal/fish-based to crop-based foods in the developed countries. Worldwide, per-capita cereal consumption declined by 5.6% between 1990 to 2003 while fruit consumption increased by 55% and vegetable consumption by 26% during the same period, with more pronounced effect noted in developing than developed countries. While meat, dairy, and seafood/fish consumption increased remarkably—55%, 29%, and

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44% in developing countries—it declined by 1.2%, 0.6%, and 11.5% in developed countries (https://www.ifama.org/events/conferences/2010/ cmsdocs/a72_pdf). Women’s opportunity cost of time—that is, the extent of women working outside the home generating income for the family— has also emerged as a key determinant in the shift from coarse-grain cereals to nontraditional grains (wheat and rice) and convenience foods (Senauer et al. 1986; Kennedy and Reardon 1994). For example, sustained economic growth, increasing population, and changing lifestyles has caused significant changes in the Indian food basket, away from staple foodgrains toward high-value horticultural products (Kumar et al. 2007; Mittal 2007). More important, the production of minor millets, for example, in the Kolli Hills region of Tamil Nadu, India, has declined substantially due to changing consumption preferences in favor of other crops, such as cassava, rice, and pineapple (Gru
ere et al. 2009). The erratic rainfall and drudgery associated with processing of minor millets also contributed to decline in production of these millets species (S.B. Ravi, MSS Research Foundation, Chennai, India). The changes in the dietary pattern also led to an increased demand of food grains as feed (Dikshit and Birthal 2010), with a steeper decline in per-capita consumption of coarse-grain cereals than that of rice and wheat, in both rural and urban India (Kumar et al. 2009). Millets productivity in the last five decades showed consistent increases in China, India, Burkina Faso, Nigeria, Uganda, Argentina, and the United States (Table 5.5). However, the percentage increase varied— 76% in China; 132% in India; 183% in Nigeria; 80% in Uganda; 40% in Argentina; and 20% in the United States. In Kenya, productivity remained on average at 1.7 t ha1 until the 1970s, but then substantially declined to 40% and 71% for the early 1980s and the last decade. In contrast, millets productivity remained constant at around 1 t ha1 in Nepal. Millet yield in Namibia among the African countries remained the lowest (0.20–0.30 t ha1) (Table 5.5). Isolated cases of very high grain yield under reasonably good management conditions have also been reported: finger millet grain yield as high as 4.2 t ha1 in Uganda (Odelle 1993), 6 t ha1 in Zimbabwe (Mushonga et al. 1993), 3.7 t ha1 in Ethiopia (Mulatu and Kebebe 1993), and 4 to 6 t ha1 in India (Seetharam and Prasada Rao 1989; Bondale 1993); foxtail millet grain yield as high as 9 t ha1 in China (Diao and Cheng 2008), and up to 11 t ha1 in breeding trial with the newly released hybrid cultivar ‘‘Zhangzagu 8’’ (Diao 2007). Pearl millet, finger millet, foxtail millet, and proso millet are grown widely (pearl millet in south Asia and sub-Saharan Africa; finger millet in South and Southeast Asia and East Africa; foxtail millet in South and

263

1964–1968

Source: http://faostat.fao.org.

South and Southeast Asia Afghanistan 0.847 Bangladesh 0.870 China 1.150 India 0.404 Myanmar 0.289 Nepal 1.108 Pakistan 0.455 Sub-Saharan Africa Burkina Faso 0.443 Cameroon 0.750 Chad 0.586 Ghana 0.571 Kenya 1.788 Mali 0.745 Namibia 0.225 Niger 0.482 Nigeria 0.563 Senegal 0.459 Sudan 0.503 Tanzania 0.636 Togo 0.482 Uganda 0.911 Zimbabwe 0.557 American continent Argentina 1.106 USA 1.284 CIS countries Ukraine 0.000 Russia 0.000

Country 0.848 0.680 1.323 0.517 0.315 1.111 0.488 0.426 0.790 0.508 0.619 1.618 0.706 0.232 0.394 0.864 0.587 0.390 0.836 0.686 1.184 0.502 1.217 1.217 0.000 0.000

0.400 0.688 0.559 0.552 1.710 0.736 0.226 0.399 0.633 0.452 0.458 0.631 0.714 1.121 0.491

1.041 1.308

0.000 0.000

1974–1978

0.836 0.764 1.249 0.502 0.273 1.125 0.481

1969–1973

0.000 0.000

1.178 1.327

0.473 0.701 0.531 0.659 0.883 0.718 0.251 0.429 1.293 0.543 0.303 1.151 0.624 1.519 0.417

0.860 0.718 1.567 0.546 0.648 0.966 0.495

1979–1983

0.000 0.000

1.240 1.439

0.575 0.949 0.502 0.652 0.649 0.859 0.309 0.394 1.255 0.590 0.178 0.996 0.831 1.401 0.572

0.866 0.750 1.724 0.544 0.933 0.933 0.448

1984–1988

1.335 0.814

1.453 1.501

0.599 1.044 0.403 0.697 0.610 0.658 0.285 0.378 1.026 0.635 0.200 0.881 0.522 1.542 0.406

0.839 0.724 1.836 0.683 0.693 1.147 0.422

1989–1993

1.173 0.791

1.233 1.501

0.682 1.005 0.418 0.935 0.482 0.720 0.236 0.367 1.048 0.606 0.240 1.033 0.499 1.410 0.282

0.815 0.701 2.073 0.774 0.641 1.060 0.449

1994–1998

1.102 0.960

1.689 1.431

0.739 1.004 0.495 0.805 0.552 0.691 0.252 0.428 1.221 0.663 0.243 0.798 0.585 1.519 0.274

0.821 0.693 1.792 0.823 0.703 1.081 0.515

1999–2003

1.151 1.169

1.547 1.546

0.853 1.134 0.541 0.869 0.650 0.743 0.245 0.463 1.596 0.599 0.301 0.799 0.700 1.645 0.226

0.905 0.693 2.023 0.937 0.772 1.100 0.548

2004–2008

Table 5.5. Five- yearly averages of the millets productivity (t ha1) from the major millets-producing countries in South and Southeast Asia, sub-Saharan Africa, the American continent, and CIS countries for the period from 1964 to 2008.

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Southeast Asia; proso millet in Asia, Europe, and North America), while other millets are mostly confined to specific geographic regions: for example, fonio in West Africa; tef predominantly in Ethiopia; Job’s tears and barnyard millet in South and Southeast Asia; and little millet and kodo millet in South Asia (Table 5.6). India is the largest producer of pearl millet and finger millet, while China is the largest producer of foxtail and proso millet. Millets species are known by different vernacular names across regions and countries within regions (Table 5.7). Like other cereals, millets are also adversely affected by diseases, including downy mildew, rust, smut, ergot, and leaf blight in pearl millet; blast (leaf, neck, and finger) and leaf blight in finger millet; blast, downy mildew, rust, and leaf spot in foxtail millet; and rust, head smudge, and damping-off diseases in tef (Table 5.8). Major insect pest damage has been limited in millets but does impact regions of production. Proso millet is limited to less humid environments of the United States by chinch bugs, and this impact has been reported to impact pearl millet as well (Ni et al. 2009). Stem-boring insects have also been reported in proso, foxtail, and pearl millet (Adugna and Hofsvang 2000). Aphids have been limiting to grain and forage production and interact with the spread of plant viruses (www.ars.usda.gov/Research/ docs.htm?docid¼8927). Foraging insects, such as grasshoppers, also occasionally have been severe for proso millet in the U.S. Great Plains (Lyon et al. 2008) and pearl millet in Mali (Coop and Croft 1993). Some pest damage has been reported in tef and fonio from Africa, or during storage conditions. Additionally, the millets grain retains viability for long periods even under poor storage conditions. Most of the millets species are considered to be hardy crops adapted to marginal lands in the hot, drought-prone arid and semiarid regions of Africa, Asia, and the American continent (http://www.underutilized-species.org/documents/ millet_mssrf.pdf); however, drought and heat stresses adversely affect millets productivity. For example, postflowering drought stress in pearl millet causes substantial grain and stover yield losses (Mahalakshmi et al. 1987), and tef is highly sensitive to water stress during grain filling (Mengistu 2009). Lodging adversely affects finger millet, foxtail millet, proso millet, tef, and fonio production. Parasitic weeds, Striga spp., are serious constraints to finger millet, pearl millet, and fonio cultivation in Africa. Millets are C4 plants (Roder 2006; Osborne and Freckleton 2009), which have competitive advantage (better adaptation) over C3 plants under conditions of drought, high temperature, and nitrogen or carbon dioxide (CO2) limitation. C4 plants utilize their specific leaf anatomy, known as Kranz anatomy, to fix CO2 around rubisco, thus reducing photorespiration (Osborne and Beerling 2005). Millets are considered to provide more grain

5. MILLETS: GENETIC AND GENOMIC RESOURCES

Table 5.6.

265

Major regions/countries with substantial millets production.

Major geographical regions and countries with substantial production Barnyard millet South and Southeast Asia: China, Korea, Japan, India Finger millet South and Southeast Asia: India, China, Nepal, Myanmar, and Sri Lanka Eastern Africa: Uganda, Kenya, Sudan, and Eritrea Southern Africa: Zimbabwe, Zambia, Malawi, and Madagascar Central Africa: Rwanda and Burundi

Reference Prasad Rao et al. 1993

Prasad Rao et al. 1993; http:// afriprod.org.uk/ paper02obilana.pdf

Fonio West Africa: Benin, Burkina Faso, Chad, Guinea, Gambia, Mali, Nigeria, Senegal, and Togo

http://underutilized-species.org

Foxtail millet China, South and Southeast Asia: India, Nepal, Afghanistan, Korea, and Japan East Asia: China Other regions/countries: Russian Federation, USA, and France

http://hort.purdue.edu/ newcrop/proceedings1997/ v3-182html; Prasad Rao et al. 1993

Job’s tears South and Southeast Asia: Burma, China, India, Malaysia, the Philippines, Thailand, and Taiwan South America: Brazil

Venkateswarlu and Chaganti 1973; Wanous 1990 iat.sut.ac.th/food/FIA2007/ FIA2007/paper/P1-07-CP.pdf

Kodo millet South Asia: widely grown in India

Prasad Rao et al. 1993

Little millet South Asia: India (Eastern Ghats), Nepal, Myanmar, and Sri Lanka Pearl millet South Asia: India (Rajsthan, Gujarat, Maharashtra, Haryana and Uttar Pradesh), Afghanistan, Bangladesh, Myanmar, and Pakistan Sub-Saharan Africa: Grown in 28 countries with Nigeria, Niger, Burkina Faso, and Mali being the largest producers Proso millet India, China, Japan, Russia, Afghanistan, Iran, Iraq, Syria, Turkey, Mongolia, Romania, and USA (Nebraska, South Dakota, and Colorado)

Prasad Rao et al. 1993

Yadav 1996a; afriprod.org.uk/ paper02obilana.pdf

http://hort.purdue.edu/ newcrop/proceedings1997/ v3-182html; Wanous 1990 (continued )

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S. DWIVEDI ET AL.

Table 5.6 (Continued) Major geographical regions and countries with substantial production Tef Eastern and southern Africa: Ethiopia the major grain producer and the highlands of Eritrea; South Africa (both forage and grain), northern Kenya Europe and North America (small-scale grain production): USA, Canada, and the Netherlands Oceania: Australia (both grain and forage) Other countries: tef as forage in Morocco, India, and Pakistan

Reference database.prota.org

per unit of water than other cereals (Briggs and Shantz 1914; Felter et al. 2006). Millets grains are nutritious (see Section II) and commonly used for food in Asia and Africa, while in Europe and on the American continent, they are predominantly used as poultry feed. However, proso millet is a common ingredient in high-priced artisan breads sold in the United States, where there is a new ‘‘ancient grains’’ marketing niche. Millets straws are important sources of fodder in developing countries. Millets are also grown on the American continent as forage crops on light-textured or acidic soils throughout the tropical and subtropical lowlands and increasingly as a mulch component in no-till soybean production on the acidic soil savannahs of Latin America (http://www.cgiar.org/impact/research/millet.html). Millets are an underresearched crop commodity, especially compared with maize, which continues to push into previous millet cropping systems. Pearl millet, and to a lesser extent proso millet, finger millet, foxtail millet, and tef, have received greater attention from the research community to developing genetic and genomic resources for use in breeding, while in others only limited progress has been realized to date. This chapter is focused primarily on domestication and evolution of millets vis-
a-vis other cereals; nutritional quality to diversify food uses; germplasm resources; sources of resistance to biotic and abiotic stresses and of agronomic and seed quality traits; diversity pattern in germplasm collections and formation of reduced subsets representing diversity present in entire germplasm collection of a given species to identifying new sources of variation; promoting use of male sterility to exploit heterosis; and genomic resources as an aid to marker-aided

267

Japanese barnyard millet (Echinocloa crus-galli), Indian barnyard millet (E. Colona), cockspur grass, Korean native millet, prickly millet, sawa millet, and watergrass Ragi in Hindi; tailaban in Arabic; petit mil and coracan in French; fingerhirse in German; wimbi and ulleji in Swahili; dagussa in Ethiopia; telebun in Sudan; bulo in Uganda; African millet, birdsfoot, hansa ragi, koracan, maduwa Hungry rice in English, fonio in French; acha in Nigeria, eboniaye in Senegal, findo in Gambia, podgi in Benin; crabgrass, fundi, and raishan. Italian millet; German millet; Russian millet; Hungarian millet; awa in Japanese; Siberian millet, dawa in Indonesia, shao-mi, su and kou wei tsao in China; mohar in Russia; millet des oiseaux and millet d’Italie in French; panico, milho panico, and milho panico de Italica in Portaguese; kimanga in Swahili Hortus, magharu, shoriew, mim (arora), trigo tropical (Joyal), attabi (Bodner), walln€ ofer adlay in the Philippines; hatomugi, mayuen, or Chinese pearl barley in China kodo in Hindi, khoddi in Urdu, arugu in Telugu, and varagu in Tamil, all Indian languages; African bastard millet grass, arika, haraka, ditch millet in New Zealand, and mandal in Pakistan Samai in Tamil (India); sama (little or slender) (India)

Bajra, bajri, bulrush millet, cattail millet, babala, bulrush, seno, spiked millet, cumbu, gero, munga; dukhun in Arabic; mil a chandelles in French; mijo perla in Spanish Broomcorn millet, common millet, hog millet, Hershey millet, white millet, creeping paspalum, ditch millet, Indian paspalum, water couch, brown corn, Russian millet; huang mi, mi tzu, and shu in Chinese Tef, t’ef, teff grass, and/or Williams lovegrass in English, French and Portuguese; tahf in Arabic

Barnyard millet

Pearl millet

Tef

Proso millet

Little millet

Kodo millet

Job’s tears

Foxtail millet

Fonio

Finger millet

Other vernacular names

Common name

Arunachalam et al. 2005; Wanous 1990 Yadav 1996a; Wanous 1990; http://www.sik.se/traditional grains/review/ Prasad Rao et al. 1993; Wanous 1990; http://www.sik. se/traditional grains/review/ http://database.prota.org; NRC 1996; Wanous 1990

http://plantsforuse.com; http:// iat.sut.ac.th/food/FIA2007/ FIA2007/paper/P1-07-CP.pdf Prasad Rao et al. 1993; de Wet et al. 1983; Wanous 1990

http://database.prota.org; Wanous 1990; Austin 2006

NRC 1996; Wanous 1990

Wanyera 2007; NRC 1996; Wanous 1990

Prasad Rao et al. 1993; Wanous 1990

Reference

Table 5.7. Vernacular names of barnyard millet, finger millet, fonio, foxtail millet, Job’s tears, kodo millet, little millet, proso millet, and tef as known in different regions.

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Table 5.8. Major biotic constraints reported in barnyard millet, finger millet, fonio, foxtail millet, Job’s tears, kodo millet, little millet, pearl millet, proso millet, and tef. Biotic stress Barnyard millet Grain smut (Ustilago panici-frumentacei Brefeld) Finger millet Leaf, neck and finger blast (Pyricularia grisea); leaf blight (Heliminthosporium nodulosum); shoot fly (Atherigona milliaceae) and pink stem borer (Sesamia inferens) Fonio Insect causing severe leaf and stem damage Foxtail millet Blast (Pyricularia setariae); downy mildew (Sclerospora graminicola); rust (Uromyces setariae-italiae); smut (Ustilago crameri); leaf spot (Helminthosporium spp.); shoot fly (Atherigona spp.); seed smut (Sorosporium bullatum), kernel smut (Ustilago paradoxa); and wheat curl mite (Eriophyes tullipae Keifer) and wheat streak mosaic virus reported from USA Job’s tears Leaf blight (Pseudocochlibolus nisikadoi)

Kodo millet Head smut (Sorosporium paspali); rust (Puccinia substriata Ellis and Barht); smut (Ustilago crus-galli, U. paradoxa and U. panici-frumentacei) Little millet Rust (Uromyces linearis) Pearl millet Downy mildew (Sclerospora graminicola); smut (Moeszimyoces penicillariae); ergot (Clavisceps fusiformis); leaf blight (Pyricularia grisea and Bipolaris setariae); rust (Puccinia substriata); head caterpillar (Heliothis albipunctella); scarab beetle (Pachnoda interrupta (Olivier)), stem borer (Acigona ignefusalis (Hamps.), and striga (Striga hermonthica) Proso millet Head smut (Sphacelotheca destruens); bacterial spot (Pseudomonas syringae), smut (Sphacelotheca panici milliacei), wheat curl mite (Eriophyes tullipae) and wheat streak mosaic virus reported from USA

Reference Gupta et al. 2009a Sreenivasaprasad et al. 2007; cropgene bank.sgrp.cgiar.org

Adoukonou-Sagbadja et al. 2006 Brink 2006; Siles et al. 2004; http://www.hort.purdue.edu; http://database.prota.org

http://www.nilgs.affrc.go.jp/db/ diseases/contents/de40. htm#cm%20leaf%20blight Viswanath and Seetharam 1989

Viswanath and Seetharam 1989 crop.sgrp.cgiar.org; de

ianpubs.unl.edu/live/ec137/ build/ec137.pdf; Ilyin et al. 1993; Baltensperger 1996

5. MILLETS: GENETIC AND GENOMIC RESOURCES Table 5.8

269

(Continued)

Biotic stress Tef Diseases: Rust (Uromyces eragrostidis); head smudge (Heliminthosporium miyakei); damping off (Drechslera spp., and (Epicoccum nigrum) Pest: Wollo bush-cricket (Decticoides brevipennis); red tef worm (Mentaxya ignicollis); black tef beetle (Erlangerius niger); grasshoppers, ants, and termites

Reference database.prota.org

gene introgression of food, feed, and bioenergy traits for product development.

II. NUTRITIONAL QUALITY AND FOOD, FEED, MEDICINAL, AND OTHER USES Millets grains are nutritionally equivalent or superior to other cereals (Mengesha 1965; FAO 1972). The grains contain high amounts of carbohydrates, proteins, minerals, and vitamins. For example, high levels of protein, calcium, iron, and zinc are found in finger millet, foxtail millet, and fonio; methionine, iron and zinc in pearl millet; methionine and/or cysteine in finger millet and fonio; iron in tef; tryptophan, lysine, methionine, phenylalanine, threonine, valine, leucine, and isoleucine in foxtail millet (Ode et al. 1993; de Lumen et al. 1993; NRC 1996; Malleshi and Klopfenstein 1998; Fernandez et al. 2003; Khairwal et al. 2004; Alaunyte et al. 2010; database.prota.org; http://www. underutilized-species.org/documents/millet_mssrf.pdf). Millets gains are therefore recommended for lactating women and for diabetic (non-insulin-dependent) and sick people (Kumari and Sumathi 2002). Diets containing proso millet protein concentrate raise plasma levels of high-density lipoprotein (HDL) cholesterol without causing an increase in low-density lipoprotein (LDL) cholesterol levels in rats and mice (Nishizawa et al. 1990; Nishizawa and Fudamoto 1995; Shimanuki et al. 2006; Park et al. 2008). Furthermore, Nishizawa et al. (2009) reported the beneficial effects of dietary Japanese barnyard millet protein on plasma levels of adiponectin, high-density lipoprotein (HDL) cholesterol, glucose, and triglycerides in obese diabetic mice. Foxtail millet grain has high protein and iron contents compared to rice, wheat, and maize. Not only is the biological value of digestible

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protein higher than in rice and wheat, seven of the eight essential amino acids, which cannot be synthesized by the human body, are higher in foxtail millet (Zhang et al. 2007a). Edible fiber is important for intestine and stomach health. Foxtail millet grain contains 2.5 times the edible fiber found in rice and thus is a promising source for edible fiber (Liang et al. 2010). Foxtail millet bran contains 9.4% crude oil and is rich in linoleic (66.5%) and oleic (13.0%) acids (Liang et al. 2010). Millets fodders are highly nutritious and palatable and are fed to animals in Asia, Africa, and the American continent. From ancient times (>7000 years BP), foxtail millet has been in use for grain (for use by human) and hay production (for cattle and horse feeding) in China (Diao 2007). Some of the foxtail millet cultivars specifically bred for hay production in China contain as high as 15% protein (Zhi et al. 2011). Some brown-midrib (bmr) mutants in pearl millet have shown increased in vitro dry matter digestibility compared to normal cultivars (Cherney et al. 1988; Akin and Rigsby 1991), and have potential as sources of improved forage quality. Millets being C4 plants have great potential for biomass production; for example, biomass of pearl millet can yield 6 to 12 t ha1 on a dry-weight basis in less than 100 days (Khairwal et al. 2004). Hall et al. (2004) reported substantial genetic variation for stover quality and quantity without detrimental effect on grain yield in pearl millet. Millets are also considered sacred crops in some communities/ regions, where they play a central role in social events and celebrations. Because of its long cultivation history and great contribution to Chinese ancient civilization, foxtail millet was named ‘‘first’’ among the ‘‘Five Grains of China’’ (Austin 2006), which also include proso millet, rice, soybean, and wheat. Foxtail millet is used even today in ancestor worship ceremonies. In developing countries, in both Africa and Asia, the dry stalks of millets are used for fuel, thatching houses, constructing fences, and making mats. Job’s tears seeds are used as decorative beads to make necklaces and rosaries (Table 5.9). Substantial variations in seed composition of proso millet, finger millet, and foxtail millet cultivars have been reported. Ravindran (1991) reported higher seed protein (14% to 16%) and crude fat (5% to 8%) in proso millet and foxtail millet than in finger millet (protein 10% and crude fat 1.6%). Finger millet, however, had higher carbohydrate (81%) levels than those reported for proso millet and foxtail millet (70% to 74%), while all three millets had similar (4%) fiber contents. Ravindran (1991) also reported high calcium and potassium contents in finger millet grains, while other minerals, such sodium, magnesium, and phosphorous, were similar across these three millets. Regarding the

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Finger millet Flour to make bread (chapatti); porridge; popped grains as snacks; whole grains cooked as khichadi; sprouted grains; dosa, a thin fermented pancake containing blackgram

Barnyard millet Flour to make bread (chapatti); porridge; popped grains as snacks

Food

Both grain and/or stover used for animal feed including caged birds and poultry

Straw superior to rice and oat straw because of high protein and Ca content (Yabuno 1987)

Feed

Highly recommended diet for lactating women, diabetic people, and sick people

Unknown

Medicinal uses

Grains brewed for beer

Unknown

Beverage

Unknown

Unknown

Other uses

(continued )

Taylor and Emmambux 2008

Reference

Table 5.9. Food, feed, medicinal and industrial uses of barnyard millet, finger millet, fonio, foxtail millet, Job’s tears, kodo millet, little millet, pearl millet, proso millet and tef grains, and stover.

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Foxtail millet Dehusked grain for steamed food and porridge or gruel; flour to make bread (chapatti); porridge; popped grains as snacks

Fonio Porridge; tuwo; fonio-beans prepared on special occasions; couscous; both black fonio and white fonio used to make couscous ‘‘wusu-wusu’’; bread; popped

Food

Table 5.9 (Continued)

Both grain and/or stover used for animal feed including caged birds and poultry; hay production

Straw and chaff used a fodder; hay

Feed

Pregnant and lactating women; prevention of diabetics; bran oil for skin diseases; dietary fiber for prevention of stomach and intestinal diseases

Grain is regarded as medicinal (i.e., antithyroid, chronic diarrhea, dysentery, chickenpox, stomachache, asthma) and healing properties; highly recommended diet for lactating women, diabetic people, and sick people

Medicinal uses

Huangjiu or yellow wine—-alcoholic drink; xiaomiyin— nonalcoholic drink

Grains brewed for beer, named locally as tchapalo, tchoukoutou, pito and burukuto

Beverage

Decoration; thatching houses

Straw and chaff mixed with clay to build houses; sacred crop that plays central role in social events/ celebrations; grains used as an important part of dowry in Sahelian communities

Other uses

Sema and Sarita 2002; Li 2005; Austin 2006; Diao 2007; Zhang et al. 2007a

http://www. underutilizedspecies.org; NRC 1996; AdoukonousSagbadia et al. 2006

Reference

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Little millet Flour to make bread (chapatti); porridge; popped grains as snacks

Kodo millet Flour used to make chapatti or flat cake/bread

Job’s tears Porridge

Both grain and/or stover used for animal feed including caged birds and poultry

Straw as fodder

Foliage as green fodder to animals

Not known

Not known

Anodyne; anthelmintic, antiinflammatory; antipyretic; antirheumatic; antispasmodic; cancer; hypoglycemic; diuretic; pectoral; sedative; tonic; warts; appendicitis; rheumatoid arthritis; menstrual disorders

Not known

Not known

Tea from boiled seed as drink to cure warts; soup; grains for brewing beer ‘‘dzu’’; vines; coffee made from roasted grains

Not known

Not known

Seeds as decorative beads to make necklaces and rosaries; stems to make matting

(continued )

http://www.pfaf. org/database/ plants.php? Coix þ lacrymajobi; http://www. waynesword. palomar.edu/ plapr99.htm

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Tef A flat, spongy, and slightly sour bread, injera; porridge; gruel (muk)

Proso millet Flour to make bread (chapatti); porridge; popped grains as snacks

Pearl millet Flour to make bread (chapatti); porridge; boiled and/or roasted grains; baked food; weaning mixture; diabetic product; couscous or arraw (steamed product)

Food

Table 5.9 (Continued)

Tef straw as animal feed

Both grain and/or stover used for animal feed including caged birds and poultry

Both grain and/or stover used for animal feed including caged birds and poultry

Feed

Gluten-free grains for health food

Birdseed

Gluten-free grains to use in health food

Medicinal uses

Grains brewed to make alcohol

A popular alcoholic beer, bosa, in Balkans, Egypt, and Turkey

Nonalcoholic— oshikundu in Namibia and kunun zaki in Nigeria Alcoholic— ndlovo beer in Bulawayo and Zimbabwe

Beverage

Hay

Hay

Dry stalks used for firewood, thatching houses, constructing fences, and making mats

Other uses

http://database. prota.org; Stallknecht et al. 1993

Baltensperger 1996; Lyon et al. 2008

Andrews and Kumar 1992; Khairwal et al. 2004; Taylor and Emmambux 2008

Reference

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trace elements, both proso millet and foxtail millet had high manganese, zinc, and iron contents, while all the three millets had similar copper contents. Most millets grains contain some antinutrients in their seeds. The major antinutrients include polyphenols, phytic acid, and oxalic acid. Phytates decrease the bioavailability of minerals such as calcium, iron, and zinc, while oxalic acid reduces calcium availability (Reddy et al. 1982). Ravindran (1991) found that finger millet grains have less phytic acid than that present in proso millet and foxtail millet, while foxtail millet grains contain high amounts of oxalate. To date, no antinutrients from barnyard millet and kodo millet have been reported. Among all millets, Kodo millet has the highest free radical quenching potential, thus possessing good antioxidant property (Taylor and Emmambux 2008). Some people are allergic to gluten present in cereals; for example, gluten in wheat causes severe allergies. Unlike foxtail millet (Sakamoto 1987), pearl millet, tef, some proso millet, fonio, and barnyard millet grains are gluten-free and therefore offer good opportunities for their use as health foods (NRC 1996; Gulia et al. 2007b; Hoshino et al. 2010). The association of a mycotoxin with ‘‘kodua poisoining’’ was reported when kodo millet (Paspalum scorbiculatum) grains infected with Aspergillus flavus or A. tamarii were used as food or feed. Both fungi produce cyclopiazonic acid, which results in kodua poisoning in man (Rao and Husain 1985), which result sleepiness, tremors and guiddiness (Bhide 1962). Grain from millets has also shown high potential for milling, popping, and malting. Malleshi and Desikachar (1985) demonstrated that millets could be milled to remove the outer bran (husk) and such milled grains could be easily cooked for consumption. The popped products have potential for use in development of breakfast and specialty foods (Srivastava and Batra 1998; Srivastava et al. 2001; Singh and Sehgal 2008). The millets grains, especially pearl millet, finger millet, foxtail millet, proso millet, and Job’s tears, are locally brewed, both in Africa and Asia, to produce alcoholic and nonalcoholic beverages (Table 5.9). Malting and fermentation processes result in malted and brewed alcoholic or nonalcoholic products. Huangjiu, an alcoholic drink made from brewing foxtail millet or proso millet grain, was very popular in ancient China and is still popular in some parts of northern China. Malted pearl millet and finger millet are used in brewing of the traditional opaque African beer in southern and eastern Africa. Finger millet provides the best-quality malt, which is used in the brewing industry in southern and eastern Africa as well as in south and southeast Asia and for making highly digestible nutritious foods.

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Foods prepared from millets are of several types that differ between countries and regions (Table 5.9). Because of their long cultivation and use as food, a number of different methods of consumption have been developed using foxtail millet and proso millet in China. The most popular dish from these millets are dehusked grain (referred to as miaomi) steamed or used to make gruel and porridge. Flour from foxtail millet and proso millet is used to make bread, pancakes, chapattis, and snacks. Steamed bread made from composite flour containing foxtail millet, wheat, and soybean has gained prominence in northern China; it not only tastes good but is also nutritious (Diao 2007). Food dishes from pearl millet in western Africa vary by countries: thick porridge (tuwo) is most popular in Sahelian countries while thin porridge and steamed products (couscous) are also consumed in Francophone countries. Tef and fonio are mostly used for porridges and flat breads. For example, injera, the soft, spongy, thin pancakelike bread with a sour taste made from tef flour, is the major staple food in Ethiopia. This traditional milletbased food has recently gained ground in Europe, North America, and Israel. Traditional foods made from pearl millet in India include chapatti or roti, porridges, and roasted/boiled grains eaten as snacks (Khairwal et al. 2004). European and American multigrain breads frequently use dehulled proso millet. Grain color is an important seed quality trait that influences the overall grain quality that determines the end use pattern of millets. Grain color in pearl millet ranges from ivory, to cream, to gray and brown. The major grain colors in other millets include white and black in fonio; white, red, and brown in tef; white and brown in finger millet; yellow, red, gray, black, and white in foxtail millet; white, cream, straw, olive, red, black, and brown in proso millet; and straw, olive, brown, and gray in little millet. Moreover, variation in grain color is associated with variation in quality traits and trade value. For example, tef grains with dark color are rich in flavor (NRC 1996); white-colored finger millet grains contain higher protein and iron contents but are lower in fiber and tannins (Seetharam et al. 1984; Rao 1994); black-colored finger millet grains contain only half as much iron and one-tenth as much molybdenum as reported for white-colored finger millet grains (Fernandez et al. 2003; Glew et al. 2008); dark-colored proso millet grains have higher tannin contents than those with light color (Lorenz 1983). White-grained finger millet and foxtail millet grains get high premiums in trade (C. R. Ravishanker, pers. commun.). Red- and brown-seeded tef are harvested from plants that are hardier, faster maturing, and easier to grow (NRC 1996).

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Millets have medicinal values for treating complex diseases (Table 5.9). Foxtail millet is widely used not only as an energy source for pregnant and lactating woman but also for sick people and children and especially for diabetics. It is reported to reduce blood sugar concentration in female diabetics (Sema and Sarita 2002). Job’s tears grains are most popularly used in Chinese traditional medicine because of their anti tumor and anti-allergenic, probiotic, and hypolipidomic properties while fonio reportedly has healing properties. It is suggested that the low incidence of anemia in the Ethiopian population can be attributed to the high consumption levels of tef, which has high iron content (NRC 1996). Utilization of whole-meal cereals including the seed coat in food formulations is increasing worldwide, since these are rich sources of phytochemicals and dietary fiber, which offer several health benefits. Regular consumption of finger millet is known to reduce the risk of diabetes (Gopalan 1981) and gastrointestinal tract disorders (Tovey 1994), which could be attributed to polyphenols and dietary fiber present in its grains. In China, foxtail millet is used to cure rheumatism. Proso millet protein concentrate, when fed for 21 days to rats, was shown to increase plasma levels of HDL cholesterol without an increase in lowdensity lipoprotein (LDL) cholesterol compared with a casein diet, which (HDL) may have a beneficial effect against the risk of coronary heart disease (Shimanuki et al. 2006). Furthermore, finger millet and proso millet may prevent cardiovascular disease by reducing plasma triglycerides in hyperlipidemic rats; in contrast, sorghum increases total cholesterol and HDL and LDL cholesterol concentrations (Lee et al. 2010). Inhabitants of southeast Asia and eastern Asia prefer sticky food. Amylose is an important starch in cereals including millets. Foods made from waxy grains are much stickier than those obtained from nonwaxy grains due to differences in amylose content. Large variations in the waxy phenotype has been reported in several cereals including foxtail millet, proso millet, and Job’s tears. This presents opportunities to diversify food uses of millets using allelic variation at the waxy locus (see Section VIII.E).

III. DOMESTICATION, PHYLOGENETIC, AND GENOMIC RELATIONSHIPS The comprehensive overview of grass phylogenetic relationships stems from the Grass Phylogeny Working Group (GPWG 2001). A simplified representation of one of the combined analyses, using morphological

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BEP clade

Bambusoideae

bamboos

Ehrhartoideae

Rice (cultivated and wild)

(Brachypodieae)

brachypodium

(Aveneae) Pooideae (Poeae)

oat

(Triticeae)

wheat, barley, and rye

ryegrass and fescue

© 60-80 mya Aristoideae

Danthonieae Arundinoideae

PACCAD clade

Chloridoideae

finger millet and tef

Centothecoideae (Paniceae) Panicoideae

foxtail millet, pearl millet, and common millet (Proso millet)

(Andropogoneae)

maize, sorghum, sugarcane, and Job’s tears

Fig. 5.1. Phylogenetic relationships of the crown group of grasses. Taxon terminal names are subfamilies, with tribes in parentheses. (Source: Adapted from Doust 2007).

and molecular data sets, revealed that the earliest diverging lineages of basal grasses were from a few species and that cereal and forage crops were domesticated from many different grass groups (Fig. 5.1). The members of ‘‘crown’’ (C) group of grasses, which have two large clades, the BEP and PACCAD (acronyms composed of the initial letters of the included subfamilies), diverged from one another 60 to 80 million years ago (Crepet and Feldman 1991; Prasad et al. 2005). The BEP clade is comprised of the basal subfamily Bambusoideae (bamboos) sister to Ehrhartoideae (wild and cultivated rice) and Pooideae (wheat, oats, barley, etc.). This large group of
4200 species is sister to another clade (PACCAD clade) comprised of the Panicoideae, Arundinoideae, Chloridoideae, Centothecoideae, Aristidoideae, and Danthonioideae subfamilies. The Panicoideae has two tribes, the Paniceae, containing

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the foxtail millet, pearl millet, and proso millet, and the Andropogoneae, containing sorghum, maize, sugarcane, and Job’s tears. The Chloridoideae subfamily includes finger millet and tef (Doust 2007). In the first 15 to 20 million years of the 60 to 80 million years of evolution, when the main cereal grass lineage separated from other flowering plants, there was little molecular divergence among grass genomes. However, marked genomic divergence has occurred in the last two-thirds (45–60 million years) of this period (Paterson et al. 2004), resulting in genome size differences that range from rice at 420 Mb to wheat at 16,000 Mb (Goff et al. 2002). Genomic evolution in grasses has been complex, with a number of rounds of genome duplications followed by gene deletions (Kellogg 2003; Malcomber et al. 2006). Cereal genomes have shown a high level of macrocollinearity (Gale and Davos 1998), while microcollinearity was disrupted or incomplete at sequence level (Xu and Zhang 2004). Finger millet, foxtail millet, and pearl millet among the millets were the only species studied for collinearity with other cereal genomes. The rice genome has shown a high degree of conserved macrocollinearity against that of foxtail millet and finger millet (Devos et al. 1998; Srinivasachary et al. 2007), while the pearl millet genome has undergone many rearrangements compared to foxtail millet and rice (Devos et al. 2000; Gale et al. 2005). Pearl millet (Pennisetum glaucum) belongs to the genus Pennisetum, which has five sections: Penicillaria, Brevivalvula, Gymnothrix, Heterostachya, and Eu-Pennisetum (Stapf and Hubbard 1934) and 80 to 140 species (Donadıo et al. 2009), with haploid chromosome numbers of 5, 7, 8, or 9 (Jauhar 1981) and ploidy levels ranging from diploid to hexaploid. Phylogenetic analyses revealed that Pennisetum (excluding P. lanatum) is paraphyletic as it is nested with the closely related genus Cenchrus. Sections Pennisetum and Gymnothrix are polyphyletic. The domesticated species P. glaucum, P. purpureum (napiergrass), P. squamulatum, P. nervosum, and P. sieberianum are closely related, suggesting potential use of these species in crop improvement (Martel et al. 2004; Donadıo et al. 2009). The wild progenitor of pearl millet is Pennisetum glaucum ssp. monodii (Harlan 1975; Brunken 1977). Some believe that pearl millet is the product of multiple domestications (Harlan 1975; Port
eres 1976) while others propose a single domestication (Marchais and Tostain 1993). Evidence suggests that pearl millet domestication took place in Africa, although different geographical origins have been proposed along the Sahelian zone from Mauritania to Sudan (Harlan 1975; Port
eres 1976; Marchais and Tostain 1993). The earliest archaeological evidence for pearl millet domestication is from northern Ghana, some 3,500 years BP (D’Andrea and Casey 2002). Studies on

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isozyme and simple sequence repeat (SSR) markers have further confirmed a monophyletic origin of pearl millet in West Africa (Ibrahima et al. 2005; Mariac et al. 2006a,b; Oumar et al. 2008; Kapila et al. 2009). Using microsatellite data from wild and cultivated accessions from Africa and Asia, Oumar et al. (2008) detected significantly higher diversity in the wild pearl millet group. The phylogenetic relationship among accessions not showing introgressions support a monophyletic origin of cultivated pearl millet in West Africa, with eastern Mali and western Niger as the most likely region of pearl millet domestication. Introgression has played a major role in evolution of pearl millet (Brunken et al. 1977; Ibrahima et al. 2005; Miura and Terauchi 2005; Mariac et al. 2006a,b; Oumar et al. 2008). There seems to be a putative supergene or gene complex involved in the domestication syndrome that differentiates weedy and cultivated types (Miura and Terauchi 2005). Quantitative trait loci (QTL) analyses involving F2 populations derived from crosses of cultivated pearl millet and Pennisetum glaucum ssp. monodii revealed two genomic regions on linkage groups (LGs) 6 and 7, which controlled most of the key morphological differences (Poncet et al. 1998, 2000, 2002). The importance of these two LGs reveals their central role both in the developmental control of spikelet structure and in the domestication process of pearl millet, and these genomic regions may correspond with quantitative trait loci (QTL) involved in domestication of other cereals, such as maize and rice (Poncet et al. 2000, 2002). Foxtail millet (Setaria italica) is a diploid species, and its wild ancestor is S. virdis (Kihara and Kishimoto 1942; Li et al. 1945; Wang et al. 1995; Le Thierry d’Ennequin et al. 2000). Vavilov (1926) suggested east Asia, including China and Japan, to be the principal center of diversity for foxtail millet, while other views suggest independent domestication in China and Europe based on archaeological, isozyme, 5S rDNA, and morphological evidence (Harlan 1975; de Wet et al. 1979; Jusuf and Pernes 1985; Li et al. 1995a,b, 1998; Benabdelmouna et al. 2001a). However, diversity studies using different DNA marker systems do not support the hypothesis of two domestication centers. Using 16 restriction fragment length polymorphism (RFLP) probes, Fukunaga et al. (2002a) classified 62 landraces into five groups, with no clear geographical structure. Le Thierry d’Ennequin et al. (2000) used 160 polymorphic amplified fragment length polymorphism (AFLP) loci data on 39 S. italica (foxtail millet) and 22 S. virdis (green foxtail millet) accessions. Neither cultivated nor wild accessions showed a clear differentiation of population structure, but both domesticated and wild accessions from China were the most genetically diverse, which supports the monophyletic origin of foxtail millet in China. Previous studies

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involving rapid amplified polymorphic DNA (RAPD) and restriction fragment length polymorphism (RFLP) markers (Schontz and Rether 1998, 1999) or the analysis of either waxy or prolamine genes (Nakayama et al. 1999; Fukunaga et al. 2002b) were also not conclusive in supporting hypotheses of two domestication centers of foxtail millet. QTL mapping of candidate genes revealed that tillering and panicle shape were involved in domestication (Doust et al. 2004, 2005), while human selection contributed to the origin of waxy phenotype in foxtail millet (see Section VIII.D). The genus Setaria, which also includes foxtail millet, has approximately 125 species widely distributed in warm and temperate parts of the world. The genome of foxtail millet and S. viridis is designated as AA genome (Li et al. 1945). Weedy tetraploid species S. faberii and S. verticillata have AABB genome, probably originated from a natural cross between S. viridis and another diploid species, S. adhaerans (Benabdelmouna et al. 2001a,b). S. grisebachii from Mexico has been identified as CC genome diploid species (Wang et al. 2009). S. queenslandica is the only autotetraploid (AAAA genome) species in genus Setaria (Wang et al. 2009) whereas other polyploid species such as S. pumila and S. pallide-fusca do not contain the AA genome (Willweber-Kishimoto 1962; Benabdelmouna et al. 2001a,b; Benabdelmouna and Darmency 2003). Cultivated finger millet, E. coracana subsp. coracana, was domesticated some 5,000 years ago from the wild E. coracana subsp. africana (2n ¼ 4x ¼ 36) in the highland that stretches from Ethiopia to Uganda (Hilu and de Wet 1976; Hilu et al. 1979; Werth et al. 1994). Subsp. africana is the result of a spontaneous hybridization event between the diploid E. indica (AA genome) and an unknown B-genome donor (Hilu and Johnson 1992; Hiremaths and Salimaths 1992; Salimaths et al. 1995; Neves et al. 1998; Bishit and Mukai 2000). Neves et al. (2005) assessed the phylogenetic relationships in finger millet, a tetraploid species, using nuclear (internal transcribed spacer [ITS] region of the 18S-26S ribosomal DNA repeat and the 5.8S RNA gene) and plastid (trnT-trnF) DNA sequences, which strongly support a monophyletic origin, but basal relationships in the genus remain uncertain, with either E. jaegeri or E. multiflora the first diverging lineage. Further, two putative ITS homologues loci (A and B loci) were identified in finger millet. E. coracana and its putative ‘‘A’’ genome donor, the diploid E. indica, are close allies, while the sequence data contradict the hypothesis that E. floccifolia is its second genome (B) donor. Thus, the ‘‘B’’ genome donor remains unidentified and may be extinct. More recently, Dida et al. (2008) analyzed phylogeny of finger millet landraces from Africa

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and India and their wild ancestor with microsatellite markers. They confirmed that finger millet was domesticated in East Africa and dispersed into India, which became the secondary center of diversity for this crop. Proso millet (Panicum miliaceum) and little millet (P. sumatrense) are tetraploid species (Sakamoto 1988) that belong to the genus Panicum, a cosmopolitan genus with approximately 450 species. Panicum is a remarkably uniform genus in terms of its floral characters but exhibits considerable variation in anatomical, physiological, and cytological features. Proso millet probably originated from a weedy variety, Panicum miliaceum var. ruderale, distributed from northeast China to eastern Europe (Sakamoto 1987). Vavilov (1926) suggested that China is the center of diversity for proso millet, while Harlan (1975) opined that proso millet probably was domesticated in China and Europe together with foxtail millet. Further study revealed that proso millet was domesticated somewhere in the region ranging from central Asia to northwestern India together with foxtail millet (Sakamoto 1987). Current evidence suggests that proso millet was the first millet domesticated, some 10,000 years BP in Neolithic China, where it appears to have been the earliest dry-farming crop (Lu et al. 2009). Using molecular data of the chloroplast ndhF gene, Aliscioni et al. (2003) assessed infrageneric classifications and proposed a robust phylogenetic tree of Panicum; however, genome origin of proso millet and little millet has not been analyzed. RAPD analysis differentiated North American wild proso and cultivated species (Colosi and Schaal 1997). Barnyard millets Echinochloa crus-galli (Japanese) and E. colona (Indian), both hexaploid species, are from eastern Asia and India. E. crus-galli originated from the hybridization between tetraploid E. oryzicola and an unknown diploid species. The genetic relationship between E. crus-galli and E. oryzicola using nuclear DNA (nrDNA) ITS and the chloroplast DNA (cpDNA) trnT-L, trnL intron, and trnL-F regions clearly separated the New World E. crus-galli from Eurasian E. crus-galli and showed a close relationship to the American taxa, E. crus-pavonis and E. walteri. The nuclear DNA ITS sequences further indicated no differentiation between the Eurasian E. crus-galli and E. oryzicola, in contrast to their clear divergence in the cpDNA sequence, suggesting that E. oryzicola is the male donor of E. crus-galli (Aoki and Yamaguchi 2008). Further, phylogenetic analysis of the homologous copy sequences of Oryza sh4 gene (controlling shattering nature of the spikelets) in Echinocloa showed genomic relationship between the Asian Echinocloa species, which supports the theory that the allohexaploid E. crus-galli shares two genomes with its parental donor, E. oryzicola. The Asian

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perennial tetraploid species, E. stagnina, shares one genome with E. oryzicola and possesses an unknown genome. E. crus-pavonis, from the New World, shows a close affinity of two genomes with E. crus-galli and E. oryzicola, while E. colona sows distinct affinities in all homologous copies (Aoki and Yamaguchi 2009). Ethiopia is the center of origin and diversity for tef (Eragotis tef ) (Vavilov 1951), and farmers in Ethiopia have greatly contributed to domesticating this unique cereal as a food crop. Tef is an allotetraploid cereal crop whose origin within the large genus Eragrostis was investigated by Ingram and Doyle (2003). Phylogenetic analysis of sequence data from the nuclear gene waxy and the plastid locus rps16 strongly supports the widely held hypothesis of a close relationship between tef and E. pilosa, a wild allotetraploid. Eragrostis heteromera, another previously proposed progenitor, is shown by the waxy data to be a close relative of one of the tef genomes. Other putative progenitors included in the taxon sample were not supported as closely related to tef. The waxy phylogeny also resolves the relationships among other allopolyploids, supporting a close relationship between the morphologically similar disomic tetraploid species E. macilenta, E. minor, and E. mexicana. Eragrostis cilianensis, another morphologically similar disomic polyploid, appears to have shared one diploid progenitor with these species but derived its other genome from an unrelated diploid. Both E. tef and E. pilosa are disomic tetraploid species, cross compatible, and have similarity in karyotype and morphological traits; however, the two differ in spikelet shattering. The multifloreted spikelets of E. pillosa readily break apart at maturity as a natural mechanism of seed dispersal, whereas they remain attached to the rachis at maturity in E. tef (Phillips 1995). Job’s tears (Coix lacryma-jobi), a native to tropical Asia, belongs to the Andropogoneae tribe. The genus Coix consists of four species, Coix aquatica, C. gigantea, C. lacryma-jobi, and C. puellarum. C. lacryma-jobi is further divided into four taxa, var. mayuen, var. lacryma-jobi, var. monilifer, and var. sternocarpa. C. lacryma-jobi is widely distributed in Africa, Oceania, east Asia, and America (Bor 1960; Koyama 1987). Var. mayuen is cultivated as a cereal or medicinal plant in east Asia, southeast Asia, and south Asia, whereas other taxa are wild and some are used as medicine or beads. Murakami and Harada (1958) reported that mayuen is cultivated as a cereal and domesticated from lacryma-jobi, but the two differ in hardness of seed coats; mayuen is softer than lacrymajobi. Job’s tears probably were domesticated as a cereal in the continental parts of southeast Asia (Arora 1977; Sakamoto 1988). Enomoto et al. (1985) used restriction endonuclease of cpDNAs to study the phylogenetic relationship among crops in tribe Gramineae and

284

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showed that the phylogenetic tree is in complete agreement with that reported by Tateoka (1957) except that the genetic distance between the chloroplast genomes of sorghum (Sorghum bicolor) and maize (Zea mays)/Job’s tears (Coix Lacryma-jabi), is closer than that between maize and Job’s tears despite sorghum belongs to different tribe from maize and Job’s tears. Thus, the two genera, Zea and Coix, should be placed in separate tribes. More recently, Leseberg and Duvall (2009) also demonstrated that the position of Job’s tears in a phylogenetic tree coincides with the broadly delimited Andropogoneae (GPWG 2001) but contradicts earlier studies that classified Job’s tears in a putative sister tribe, Maydeae, with Zea mays (Kellogg and Birchler 1993). The genus Digitaria has 230 species, widely distributed in the tropics and subtropics (Clayton and Renvoze 1986). Of these species, D. exilis (white-seeded fonio) and D. iburua (black-seeded fonio) are domesticated and cultivated in West Africa (Port
eres 1976), with the former being most diverse and widely cultivated, while the latter is restricted to northern Nigeria, Benin, and Togo (Murdock 1959; NRC 1996). The putative wild relatives of cultivated fonio are probably D. horizontalis and D. longiflora; the latter has many interesting agronomic traits (erect habit, resistant to lodging, long panicle full of grains and large-size seeds) and appears useful for improving cultivated fonio (Dansi et al. 2010).

IV. ASSESSING PATTERNS OF DIVERSITY IN GERMPLASM COLLECTIONS Ex situ seed storage is the most widely used method to conserve millets genetic resources. To date, 161,708 accessions of millets species are preserved in gene banks across the globe, 98.1% cultivated and 1.9% wild types (Table 5.10). Finger millet, foxtail millet, pearl millet, and proso millet form the largest collection of cultivated millets germplasm, while fonio and Job’s tears form the smallest (Tables 5.11–13). In addition, the U.S.-based GRIN database contains 306 accessions of 18 Echinocloa species from 33 countries housed at the National Center for Genetic Resources Conservation (Fort Collins, Colorado; NSSL); 1,468 accessions of eight Eleusine species from 20 countries housed at NSSL and Southern Regional PI Station (Griffin, Georgia; S9); 1,014 accessions of 36 Setaria species from 52 countries housed at the North Central Regional PI Station (Ames, Iowa; NC 7); 1,616 accessions of 38 Panicum species from 52 countries housed at NC 7, NSSL, the Plant Germplasm Quarantine Program (Beltsville, Maryland; PGQP), S9, and the Western

5. MILLETS: GENETIC AND GENOMIC RESOURCES

285

Table 5.10. List of cultivated and wild relatives of barnyard millet, finger millet, fonio, foxtail millet, Job’s tears, kodo millet, little millet, proso millet, and tef germplasm preserved worldwide in national and international gene banks in Africa, America, Asia, Europe, and Oceania. Crop

Africa

Cultivated germplasm Barnyard millet Finger millet 7,766 Fonio 285 Foxtail millet 985 Kodo millet Job’s tears Little millet Pearl millet 11,105 Proso millet Tef 4,747 Total 24,888 Wild relatives Barnyard millet 27 Finger millet 930 Foxtail millet 143 Job’s tears Pearl millet 286 Tef 1 Total 1,387

America

Asia

1,453

749 24,308

1,368 1 13,213 1,134 768 1,7937

19 21 57 5 102

38,429 4,025 154 1,017 13,252 8,547 420 90,901

Europe

48 4,643

Oceania 67 21 336 227

4 4,088 14,918 46 23,747

130 388 8 1,025 1 1,552

252 245 20 1,168

1 1 24 25

1

Total 816 33,596 285 45,761 4,252 159 1,017 41,910 24,844 6,001 158,641 27 1,079 552 9 1,369 31 3,067

Source: http://apps3.fao.org/wiews/germplasm_query.htm.

Regional PI Station (Pullman, Washington; W6); and 1,401 accessions of 69 Paspalum species from 44 countries housed at NSSL, PGQP, and S9 gene banks (http://www.ars-grin.gov/npgs/stats/). The largest collections of finger millet can be found in India in Asia and in Ethiopia, Kenya, and Uganda in Africa; China, France, India, and Japan have the largest collections of foxtail millet; China, Russia, and Ukraine have the largest collections of proso millet; India has the largest collections of kodo millet and little millet; India and Japan have the largest collections of barnyard millet; Benin has the largest collection of fonio; Japan has the largest collection of Job’s tears; Brazil, Canada, China, France, India, Namibia, Niger, Nigeria, and Pakistan have the largest collections of pearl millet; and Ethiopia has the largest collections of tef germplasm. Evidence suggests that some of the fonio germplasm has already been lost. The main reason for fonio genetic erosion is due to difficulties in its harvesting and postharvest processing (Adoukonou-Sagbadja et al. 2004). Likewise, diversity in barnyard millet has fast eroded due

286

Nepal

Japan

India

Asia Bangladesh China

Country

Bangladesh Agr. Res. Inst., Joydebpur, Gazipur Institute of Crop Germplasm Resources, Chinese Academy of Agricultural Sciences (ICGR-CAAS), Beijing All India Coordinated Small Millet Project, UAS, Bangalore CSK HP Krishi Vishvavidyalaya, Palampur, Himachal Pradesh CCS Haryana Agricultural University, Hisar, Haryana Indian Grassland and Fodder Research Institute(IGFRI), Jhansi, Uttar Pradesh International Crop Research Institute for the Semi-Arid Tropics, Patancheru Indian Grass and Fodder Research Institute National Bureau of Plant Genetic Resources (NBPGR), New Delhi Regional Station Akola, NBPGR, Maharashtra Regional Research Center, Jodhpur Department of Genetic Resources I, National Institute of Agrobiological Sciences (NIAS), Tsukuba-shi National Grassland Research Institute (NGRI), Nasu-gun, Tochigi-ken Plant Germplasm Institute, Faculty of Agriculture, Kyoto University (KYOPGI), Mozume-cho - Muko-shi, Kyoto Central Plant Breed. & Biotechnol. Division, Nepal Agric. Res. Council (CPBBD), Khumaltar, Kathmandu

Institute

4,330 349

9,522 455

869

58

74

30

274

2,450

1,488

5,852

565

2,512

515 26,233

Foxtail millet

6,257 30

300

Finger millet

5,772 133

568 3,294

875 734

103

Pearl millet

No. accessions

Table 5.11. Number of cultivated germplasm accessions of finger millet, foxtail millet, pearl millet and proso millet preserved globally in national and international gene banks.

16

62

296

849

577

209 6,517

Proso millet

287

Senegal

Nigeria Namibia

Niger

Malawi Mali

Ethiopia Kenya

Burkina Faso

Benin Botswana

Africa Angola

Thailand

Sri Lanka

Pakistan

Centre National des Resources Phytogenetiques, Minist
ere de l’agriculture et du D
eveloppement Rural (CNRF), Luanda Centre de Recherches Agricoles Sud (CRAS), Attogon Department of Agricultural Research, Sebele Agricultural Research Station, Gaborone Centre de Recherches Agricoles de Farako-Ba (CRA), Bobo-Dioulasso Inst. Biodiversity Conserv (IBC). Addis Ababa Natl. Gene Bank of Kenya, Crop Plant Genet. Resour. Centre (KARI-NGBK), Muguga Chitedze Agr. Research Station Station de Recherche Agronomique de Cinzana (SRAC), Cinzana, Segou Institut National de la Recherche agronomique du Niger (INRAN), Niamey ICRISAT, Niamey Nat. Centre Genet. Resour. Biotechnol., Moor Plantation—Ibadan National Plant Genetic Resources Center, National Botanical Research (NPGRC) Institute Unite de Recherche en Diversite G
en
etique et Culture In-vitro (URCI), Dakar

Plant Genetic Resources Institute, Natl. Agric. Res. Centre, Islamabad Fodder Research Institute, Sargodha Seed Conservation Unit, Plant Genetic Resources Centre, Gannoruwa, Peradeniya Dry Zone Agricultural Research Institute, Maha-Illuppallma National Corn and Sorghum Research Center, Kasetsart University, Pak Chong - Nakhon Ratchasima

2,156 2,875

31

295

45 5

772

110

138

44

2,817 46 1,416

2,052

47 243

166 499

112

27 61

135

63

333

1,377

(continued )

21

288

USA

Mexico

Canada

Americas Brazil

Embrapa Milho e Sorgo (CNPMS), Sete Lagoas Embrapa Recursos Geneticos e Biotechnologia (CENARGEN), Brasilia Plant Genet. Resour. of Canada, Saskatoon Research Centre, Agr. & Agri-Food Canada, Saskatoon, Saskatchewan Estacio´n de Iguala, Instituto Nacional de Investigaciones Agrıcolas, (INIA), Iguala North Central Reg. Plant Introd. Station, USDA-ARS, NCRPIS, Iowa State Univ. Ames, IA National Center for Genetic Resources Preservation, Fort Collins Colorado Plant Genetic Resources Conservation Unit, Southern Regional Plant Introduction Station, University of Georgia, USDA-ARS, Griffin, GA

Division of Plant and Seed Control, Dept. Agriculture, Pretoria National Plant Genetic Resources Centre (NPGRC), Arusha Serere Agric. & Animal Prod. Res. Inst.,(SAARI) Soroti Mt. Makulu Central Res. Station, Chilanga SADC Plant Genet. Resour. Centre, Lusaka Zambia Agriculture Research Institute (ZARI), Chilanga Genetic Resources and Biotechnology Institute, Ministry of Agriculture, Mechanization and Irrigation Development (GRBI), Causeway—Harare

South Africa Tanzania Uganda Zambia

Zimbabwe

Institute

Country

Table 5.11 (Continued)

748

702

3

3 74 1,231 390 1,037

Finger millet

1,000

350

18

122

41

Foxtail millet

2,063

3,764

7,225 161

785 323 73

69 48 2,142

Pearl millet

No. accessions

713

400

21

Proso millet

289

Australian Medicago Genetic Resources Centre, South Australian Research and Development Institute (AMGRC), SARDI, PRC GPO Box 397, Adelaide Australian Tropical Crops & Forages Collection, Australian Plant Genetic Resource Information Service, Biloela

AGES Linz—Austrian Agency for Health and Food Safety/Seed Collection, Wieningerstrasse 8, Linz Inst. Plant Genet. Resour. ‘‘K.Malkov’’ (IPGR), Sadovo, Plovdiv Res. Inst. Crop Production, Praga Biologie Vegetale Appliquee, Institut Louis Pasteur (IUT), 3 rue de l’Argonne-Strasbourg ORSTOM-MONTP, Montpellier Cedex Gene Bank, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, Gatersleben Institute for Agrobotany (RCA), Kulsomezo 15, Tapio´szele Bot. Garden of Plant. Breed. & Acclimatization Inst., Bydgoszcz Res. Inst. Cereals and Technical Plants Fundulea, Fundulea, Calarasi N.I. Vavilov All-Russian Scientific Res. Inst. of Plant Industry, St. Petersburg Res. Inst. Plant Production, Piestany Inst. Plant Prod. V.Y. Yurjev of UAAS, Kharkiv Ustymivka Experimental Station of Plant Production, S. Ustymivka Institute of Biological, Environmental & Rural Sciences, Aberystwyth University (IBERS-GRU), Ceredigion, Wales

Source: http://apps3.fao.org/wiews/germplasm_query.htm.

Total

Oceania Australia

United Kingdom

Russian Federation Slovakia Ukraine

Hungary Poland Romania

Germany

Bulgaria Czech Republic France

Europe Austria

33,596

13

8

11

27

10

46,070

336

12

14

27 82

3,500 124

34 850

41,910

252

4,059 29

24,844

245

53 1,046 3,976

8,778

20 721 65

97 162

290

S. DWIVEDI ET AL.

Table 5.12. Number of cultivated germplasm accessions of barnyard millet, kodo millet, and little millet preserved globally in national and international gene banks. No. accessions Country Asia India

Oceania Australia

Total

Institute All India Coordinated Minor Millet Project, UAS, Bangalore ICRISAT, Patancheru NBPGR, New Delhi NBPGR Regional Station, Akola, Maharashtra Tropical Crops & Forages Collection, Australian Plant Genetic Resource Information Service, Biloela

Barnyard millet

Kodo millet

Little millet

1,111

544

749

665 2,170 79

473

67

227

816

4,252

1,017

Source: http://apps3.fao.org/wiews/germplasm_query.htm.

to considerable reduction in acreage and changing sociocultural and economic dimensions of the farming community in India (Maikhuri et al. 2001). Foxtail millet, finger millet, and pearl millet have extensive collections of their wild relatives preserved in ex situ seed gene banks. No wild relatives are reported for fonio, kodo millet, and little millet (Table 5.14). In addition, some of the pearl millet wild relatives are maintained by the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) in an ex situ field gene bank at Patancheru, India, as they do not set seed. Among global gene banks, China has the largest collection of wild relatives of foxtail and proso millet; India has the largest collection of finger millet; and France and India have largest collections of pearl millet. A German gene bank contains the largest number of the few accessions of tef’s wild relatives available. Descriptor lists were developed and used to characterize barnyard millet (IPGRI 1983), finger millet (IBPGR 1985a), foxtail millet (IBPGR 1985b), kodo millet (IBPGR 1983), proso and little millets (IBPGR 1985c), pearl millet (IBPGR/ICRISAT 1993), and tef (Ketema 1997) germplasm for sets of morphological and agronomic traits. This information, along with passport data, was used to assess patterns of diversity in millets germplasm collections and has revealed many interesting facts about the utility of such germplasm in millets breeding and

5. MILLETS: GENETIC AND GENOMIC RESOURCES

291

Table 5.13. Number of cultivated germplasm accessions of fonio, Job’s tears, and tef millets preserved globally in national and international gene banks. No. accessions Country Asia China

India

Japan

Africa Ethiopia Benin Ghana Kenya South Africa Americas Brazil USA

Europe Germany

UK

Hungary Oceania Australia

Institute

Fonio

National Key Laboratory of Crop Genetic Improvement, Huazhong Agr. Univ., Wuha National Bureaue Plant Genetic Resources, New Delhi CCS Haryana Agr. Univ., Hissar Department of Genetic Resources I, National Institute of Agrobiological Sciences (NIAS) National Inst. Crop Sci., Tsubuka Institute of Biodiversity Conservation, P.O.Box 30726 Laboratory of Genetics and Biotechnology, Univ, Aboney-Calvi, Cotonou Sabana Agr. Res. Inst., Tamale National Gene Bank of Kenya, Crop Plant Genetic Resources Centre, Muguga Division of Plant and Seed Control, Dept. Agr, Technical Service

Job’s tears 14

253

140

4,741 261 24 3 3

400 368 1

Gene Bank, Leibniz Institute of Plant Genetics and Crop Plant Research Federal Center for Breeding Researcg on cultivated plants (BAZ), Braunschweig Welsh Plant Breeding Station, Genetic Resources Unit, Institute of Grassland and Environmental Research Institute for Agrobotany

12 30 2

2

2

2

Australian Tropical Crops & Forages Genetic Resources Centre

Source: http://apps3.fao.org/wiews/germplasm_query.htm.

137

30

Centro de Pesquisa Agropecuaria dos Cerrados (CPAC), Planaltina Western Regional Plant Introduction Sta., USDA-ARS, Washington State Univ. North Central Regional Plant Introduction Station, USDA-ARS, NCRPIS

Total

Tef

20 285

159

6,001

292

Malawi South Africa Tanzania Zambia

Kenya

Pakistan Yemen Africa Ethiopia

Japan

India

China

Asia Armenia

Country

Int. Livestock Res. Inst. (ILRI), Addis Ababa Institute of Biodiversity Conservation (IBC), Addis Ababa Agricultural Research Centre (KARI), Kitale National Gene Bank of Kenya, Crop Plant Genetic Resources Centre(KARI-NGBK), Muguga Chitedze Agricultural Research Station, Lilongwe RSA Plant Genetic Resources Centre, Pretoria National Plant Genetic Resources Centre (NPGRC), Arusha SADC Plant Genet. Resour. Centre, Lusaka Zambia Agriculture Research Institute, Chilanga

Laboratory of Plant Gene Pool and Breeding(LPGPB), Yerevan Scientific Center of Agrobiotechnology (SCAPP), Echimiadzin Institute of Crop Germplasm Resources, Chinese Academy of Agricultural Sciences, Beijing National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuha International Crops Research Institute for the Semi Arid Tropics, Patancheru National Bureaue Plant Genetic Resources, New Delhi CCS Haryana Agric. University, Hissar Department of Genetic Resources I, National Institute of Agrobiological Sciences (NIAS), Tsukuba-shi Plant Genet. Resour. Inst., Natl. Agric. Res. Centre, Islamabad Agricultural Research and Extension Authority (AREA), Dhamar

Institute

27

Barnyard millet

383

156 21 286

56

11 17

25

105

Finger millet

119 6 13 5

18

81

62

54

173

Foxtail millet

1

7

Job’s tears

No. accessions

8 10

59

203

78 875

42 30

Pearl millet

Table 5.14. Number of wild relative accessions of barnyard millet, finger millet, foxtail millet, Job’s tears, pearl millet, and tef preserved globally in national and international gene banks.

1

1

Tef

293

Source: http://apps3.fao.org/wiews/germplasm_query.htm.

American continent Canada Plant Genetic Resources of Canada, Saskatoon Res. Center, Agric., and Agri-Food Colombia CIAT, Cali, Valle del Cauca USA Western Regional Plant Introduction Station, USDA-ARS, Washington State University Plant Genetic Resources Conservation Unit, Southern Regional Plant Introduction Station, University of Georgia, USDA-ARS, Griffin Uruguay INIA La Estanzuela Europe Germany Gene Bank, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, Gatersleben Austria AGES Linz—Austrian Agency for Health and Food Safety/Seed Collection, Wieningerstrasse 8, Linz France Biologie Vegetale Appliquee, Institut Louis Pasteur (IUT), Strasbourg ORSTOM-MONTP, Montpellier Cedex Hungary Institute for Agrobotany (RCA), Kulsomezo 15, Tapio´szele Slovakia Botanical Garden, University of Agriculture, Nitra United Kingdom Seed Conservation Department, Royal Botanic Gardens (RBG), Kew, Wakehurst Place Oceania Australia Australian Medicago Genetic Resources Centre, South Australian Research and Development Institute (AMGRC), SARDI, PRC GPO Box 397, Adelaide Australian Tropical Crops & Forages Genetic Resources Centre (ATCFC), Biloela Total 27

2

18

906

57

23

1,133

15

250

30

21

4

9

16

3

9

1 1,781

7

250

131

31

5

27

25

32

1

1

1

22

2

3

294

S. DWIVEDI ET AL.

genetics (Table 5.15). For example, accessions belonging to laxa race of barnyard millet, endemic to Sikkim state of India, are not represented in the ex situ collections preserved at the ICRISAT gene bank in Patancheru, India. Thus, there is an urgent need to collect this race before it becomes extinct. Likewise, the germplasm accessions from tef-growing regions of Hararghe, Arsi, Wellega, and Bale in Ethiopia are not represented in the gene bank of the Institute of Biodiversity Conservation in Ethiopia (Demissie 2001). Fonio landraces collected from Ghana and Togo have immense diversity with respect to agroecological adaptation and preferences of the tribes that maintain and cultivate these landraces: for example, landraces from the northern zone of Togo are better adapted to dry conditions; those from the Kara region in the north had the most landrace diversity, with greatest landrace diversity being maintained by the Lamba tribe. The later-maturing fonio landraces from Ghana have lighter seeds (1,000-seed weight) while early-maturing types have heavier seeds. Furthermore, earliness, ease in processing, and long shelf life (e.g., seeds of ‘‘Saranu’’ landrace could be stored up to eight years without loss of quality or viability) were the basis for farmer selection of landrace variability in fonio. More recently, Dansi et al. (2010) grouped 15 farmernamed landraces collected from the fonio production zones of Benin into five morphotypes, of which four belong to D. exilis (white fonio) and one to D. iburua (black fonio), and identified eight preference criteria of farmer-preferred fonio varieties: earliness, culinary characteristics, ease of harvesting and processing, productivity, grain size, storability, and drought tolerance. This study further revealed that farmers preferred the early-maturing landrace ‘‘Tintinga’’ as it help them to bridge the food shortage period when no other crops are ready for harvest and consumption. Likewise, the preference for the ‘‘S embr e’’ landrace was mainly due to its ease in processing (husking) of the grains, while most farmers disliked landraces ‘‘Tamaou’’ and ‘‘Foˆloˆm’’ because of their long growth period and difficulties in husking their grains. Foxtail millet (Setaria italica) accessions from Afghanistan, Iran, and Lebanon, one of the three possible (putative) centers of domestication and diversity in foxtail millet, resemble green foxtail millet (S. virdis), the wild progenitor species of cultivated S. italica. In pearl millet, landraces from Yemen are a source of variation for early maturity, cold tolerance, short stature, and large seeds. Landraces from western and central Africa show exceptional buffering against environmental variability, and landraces from Cameroon, Togo, and Ghana are good sources for earliness and/or large seeds. Early flowering, profuse tillering, more panicles plant1, and larger seed size are the characteristics of some landraces from northwestern India. Some of the landraces from this Indian region exhibit no trade-off

295

11 landraces from farmers barns in Ghana

Fonio 13 landraces from Ghana and 5 traits

Finger millet 909 germplasm from southern and eastern Africa and 7 traits

Barnyard millet 194 accessions from India and 14 traits

Accessions/traits studied

Phenology—a major determinant of diversity among landraces: those from Nyankpala matured earlier than those from eastern part of northern region; late-maturing types had lighter 1000-seed weight while early-maturing types heavier seeds Earliness, ease of processing and storage quality the basis for farmers’ selection of landrace variability, i.e., Nomba, Fefeka, and Kiyo landraces selected for early maturity; Yadema for ease in processing; Sarannu for long shelf life (8 years without loss of quality and viability); and Nankapando for drought resistance

Early-flowering accessions from Kenya while later-flowering types from Tanzania and Zaire; accessions with narrowest inflorescence width from Kenya and Zimbabwe while those with the widest inflorescence width from Nepal, Ethiopia, and Tanzania; accessions with no panicle exertion can be found in Kenya, Nepal, and Zimbabwe while those with full panicle exertion from Tanzania and Zaire

Assessing pattern of phenotypic diversity among accessions collected from different ecogeographical regions of India revealed no accession represented race laxa, endemic to Sikkim in India

Pattern of diversity discerned

(continued )

Clottey et al. 2006b

Clottey et al. 2006a

Upadhyaya et al. 2007a

Gupta et al. 2009

Reference

Table 5.15. Summary of the pattern of diversity as assessed in barnyard millet, finger millet, fonio, foxtail millet, pearl millet, proso millet, and tef germplasm.

296

20,844 germplasm from 51 countries and 23 traits

169 landraces from India evaluated for grain and stover yield

Pearl millet 145 inbreds derived from 122 WCA landraces

2907 accessions from 16 provinces of China þ 22 countries and 9 traits

Flowering, relative response to photoperiod and panicle length significantly impacted, population structure differentiation but not the environmental factors such as latitude, temperature, or precipation Significant differences among landraces for biomass, grain, and stover yield; several landraces outperformed controls in both grain and stover yields; no trade-off between stover and grain yields under arid zone conditions Diversity in flowering ranges from 33 to 159 days; plant height from 30 cm to 490 cm; tillers from 1 to 35; 100-seed weight from 1.5 to 21.3 g; forage type 141 accessions; 9 panicle shapes, 5 seed shapes, and 10 seed colors

Greater diversity for flowering in Sri Lankan germplasm, while narrowest in Russian germplasm; accessions from China dwarf while those from India tall; accessions with maximum panicle exertion from Russia; accessions with longest and widest inflorescence from India Accessions of Chinese origin highly diverse, while those from Afghanistan, Iran, and Lebanon less diverse and characterized by short plant height with more tillers and smaller panicles, resembling green foxtail millet (wild type)

Landraces from the northern zone better adapted to dry conditions than those cultivated in the south, which are adapted to a relatively wet climate; landraces from Kara region in the north have the most diversity followed by Plateaux in the south and Savanes in the north; at ethnic level, the Lamba tribe maintained maximum landrace diversity followed by the Akposso, LossoNwada, and Tamberma

95 accessions representing 34 landraces collected from 7 ethnic groups in Togo

Foxtail millet 1535 accessions from 26 countries and 6 traits

Pattern of diversity discerned

Accessions/traits studied

Table 5.15 (Continued)

Upadhyaya et al. 2007b

Yadav and Bidinger 2008

Stich et al. 2010

Li et al. 1995a

Reddy et al. 2006

Adoukonou-Sagbadja et al. 2004

Reference

297

227 landrace populations from Ghana and 18 traits

918 accessions including wild relatives from Cameroon and 8 traits

105 landraces from northwestern India and 8 traits

229 germplasm from Yemen and 12 traits

424 landraces from West and Central Africa (WCA) evaluated for flowering

5197 germplasm from India and 8 traits

Climate variables impacted pattern of diversity: arid zone as the promising source of early flowering, short height, and large seeds; semiarid zone for thick panicles and high panicle exertion; subhumid zone for tall and long panicles Exceptional buffering capacity (both at individual and population level) against environmental variability, due to variation in photoperiod sensitivity and intravarietal heterogeneity for flowering, confer adaptive advantages under variable climatic conditions, thus, a good resource to enhance adaptation of pearl millet under similar scenarios in other agroecological zones as found in WCA Yemen has extreme variation in elevation, temperature, and rainfall, which significantly impacted variability in pearl millet: germplasm from high elevation good source for early maturity, cold tolerance, short plant height, and large seeds; accessions from lower elevation have longer panicle while increasing elevation have accessions with thinner panicle Large variation in flowering, plant height, panicle length and panicles plant1 among landraces; more than 2-fold difference in grain and stover yield; phenotypic diversity spread into 9 clusters, some with specific attributes: i.e., landraces from cluster 9 were highest yielding due to early flowering, more panicle plant1, and larger seed size while cluster 4 landraces provided highest stover yield but flowered late and produced less grain A good source for more reproductive tillers, large compact spikes, and larger ivory- and cream-colored grain besides its potential for forage; early-maturing types (Mouri) adapted to low rainfall, while late-maturing types (Yadiri) in high rainfall regions Mixtures of various morphological types were the common features of landrace populations grown by the farmers and good source of genes for earliness and large grain size (continued )

Rao et al. 1985

Rao et al. 1996

Yadav et al. 2004b

Reddy et al. 2004

Haussman et al. 2007

Upadhyaya et al. 2007c

298

1080 germplasm (36 populations) from 6 central/northern regions of Ethiopia and 14 traits

60 germplasm and 6 traits

3000 panicle derived lines from 60 germplasm of Ethiopia and 17 traits

Tef 144 heterogeneous germplasm from Ethiopia and 18 traits

Proso millet 842 germplasm from 27 countries and 9 traits

Accessions/traits studied

Table 5.15 (Continued)

Regions and altitudes have had no substantial effect on genetic diversity; higher intraregional genetic diversity (between tef germplasm from the same region and altitude) than interregional diversity Detected regional and clinal (altitude zone) diversity patterns in tef germplasm; all the 6 regions remain separate and unclustered at 75% similarity, while at 50% level of similarity Shewa, Wellega, and Keffa clustered together and the remaining 3 regions remained distinct and ungrouped Germplasm from high altitudes (>2400 m.a.s.l.) differed significantly from those either lowland (<1800 m.a.s.l.) or midaltitude (1800–2400 m.a.s.l) Large variations within populations as well among populations within regions and altitude zones providing immense potential for the genetic improvement through breeding

Early-flowering accessions from Syria while late-flowering from India; dwarf accessions from Mexico and tall from Sri Lanka; accessions with good panicle exertion from Australia and China while those with shorter panicle from former USSR and of longer panicle from Nepal

Pattern of diversity discerned

Assefa et al. 2001

Assefa et al. 2002

Assefa et al. 2003a

Adnew et al. 2005

Reddy et al. 2007

Reference

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299

between stover and grain yields and thus provide potential resource for producing dual-purpose hybrids adapted to arid-zone environments. Tef landraces from Ethiopia have revealed greater intraregional diversity than interregional diversity, clearly indicating that regions and altitudes have had no substantial effect on genetic diversity in tef populations. Unlike other cereals, there are very limited collections of millets wild relatives in gene banks. Wild relatives are not utilized in crop improvement programs, probably because sufficient variability already is present in the cultivated gene pool and there is a lack of resources for introgression work to eliminate weedy characteristics. However, some wild relatives have been reported to contribute beneficial traits to the cultivated gene pool. For example, resistance to herbicides (triazine, sethoxydim, dinitroaniline, and trifluralin) from Setaria virdis (green foxtail millet), controlled by one to two major genes with some modifier effects, has been successfully transferred into S. italica (the cultivated type) (Darmency and Pernes 1985; Jasieniuk et al. 1994; Wang et al. 1996; Wang and Darmency 1997). Likewise, Pennisetum glaucum subsp. monodii accessions (PS# 202, 637, 639, and 727) are good sources of resistance to Striga hermonthica, a serious cereal parasitic weed in sub-Saharan West Africa. PS 202 is also resistant to downy mildew, a devastating disease of pearl millet (Wilson et al. 2004). Other wild pearl millet accessions have been used as sources of rust resistance (Hanna et al. 1985) and alternative cytoplasmic male sterility systems (Hanna 1989). Clearly, more research is needed to find useful traits locked into the genetic backgrounds of wild relatives of millets to expand their cultivated gene pools. Targeting induced local lesions in genomics (TILLING) is a novel nontransgenic PCR-based technology that uses chemically mutated populations. It has been successfully implemented to improve crops and identify gene function in maize, barley, and wheat (reviewed in Dwivedi et al. 2007). Lodging is a serious constraint to tef production, and there is no genetic variation reported for this trait in germplasm collections. Recently, an Ethiopian researcher at the University of Bern, Switzerland, has developed a tef-based TILLING assay. The assay will be transferred to the technology platform of the Biosciences Eastern and Central Africa in Nairobi, Kenya, for use in tef with the initial objective of developing dwarf tef plants resistant to lodging (http://www.syngentafoundation.org). Ecotilling has also been applied on 500 nonmutanized accessions to detect useful genetic variations in natural populations of tef (Assefa et al. 2010). Likewise, researchers at ICRISAT have developed a TILLING population in pearl millet that can be studied to identify mutants with beneficial traits or identify specific genes contributing substantially to variation in specific traits (e.g., downy mildew and rust resistance) for use in pearl millet improvement (ICRISAT 2009).

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V. IDENTIFYING GERMPLASM WITH BENEFICIAL TRAITS A. Resistance to Biotic Stresses Like other cereals, the millets are also affected by several fungal diseases. The most prominent among these are blast in finger millet, foxtail millet, and pearl millet; downy mildew in pearl millet and foxtail millet; ergot in pearl millet; rust in pearl millet, foxtail millet, and tef; smut in barnyard millet, foxtail millet, Job’s tears, pearl millet, and proso millet; and wheat curl mite (Eriophyes tullipae), the carrier for wheat streak mosaic virus, and the virus itself in proso millet (Table 5.8). Their effects range from mild symptoms to catastrophes when large areas are destroyed. For example, India harvested a record grain production of 8.2 million t of pearl millet during the 1970–1971 season, but production declined to 4.6 million t in 1971–1972 season due to a severe epidemic of downy mildew on a popular single-cross hybrid, HB3, grown on a large scale in India at the time. Tift 23A (which had no resistance to downy mildew) was the only cytoplasmic male sterile (CMS) line used as a female parent to develop the first commercialized pearl millet hybrids in India including HB3 (Singh 1995). Subsequent studies (Yadav 1996b) have clearly demonstrated that the male-sterile cytoplasm itself is not associated with increased susceptibility to downy mildew; instead, the nuclear genotype controls downy mildew reaction in pearl millet. The deployment of genetic resistance is the most sustainable way to minimize losses in grain yield and quality due to pest and diseases. Precise phenotyping, presence of natural variation in crop germplasm (including wild relatives), pathogen variability, and understanding the mechanism and genetics of resistance are very important to finding and using new genes for host plant resistance to biotic stresses. 1. Phenotypic Screening. Researchers at ICRISAT and elsewhere have developed phenotypic screens (field and/or greenhouse) for resistance to downy mildew (Williams et al. 1981; Singh and Gopinath 1985; Singh et al. 1997; Jones et al. 2002; Thakur et al. 2008), ergot (Thakur and Williams 1980; Thakur et al. 1982), rust (Singh et al. 1997), and smut (Thakur et al. 1983; Thakur and King 1988c) in pearl millet; to blast (neck and finger) in finger millet, foxtail millet, and pearl millet (R. P. Thakur, pers. commun., ICRISAT); and to grain smut in barnyard millet (Gupta et al. 2009a). These screenings allow identification of millet diseaseresistant germplasm.

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2. Natural Genetic Variation. Pearl millet, finger millet, foxtail millet, and probably proso millet germplasm collections have been most extensively evaluated for resistance to major diseases. There are several sources of resistance to downy mildew, ergot, rust, blast, and smut in pearl millet; to blast in finger millet; to blast, downy mildew, rust, and smut in foxtail millet; to smut in proso millet and barnyard millet. These resistances in many cases have been transferred into improved genetic backgrounds (Table 5.16). Clearly, more research input is needed to identify sources of resistance to rust in tef and smut in barnyard millet and Job’s tears. 3. Pathogen Variability, Mechanism, and Genetics of Resistance. Downy mildew (Sclerospora graminicola) is the major pathogen of pearl millet in Asia and Africa. It is heterothallic and reproduces both sexually and asexually, with pathogen populations from West Africa earlier reported to be highly virulent compared to those from south Asia and eastern and southern Africa. This disease has demonstrated potential to shorten the useful life of genetically uniform single-cross hybrids (Singh 1995; Thakur et al. 2002, 2004). Host plant resistance to downy mildew can be dominant over susceptibility, additive, recessive, or even exhibit (pseudo-) overdominance. Partial host plant resistance to the causal pathogen of downy mildew is controlled by one or more major genes with some modifiers (Singh et al. 1993; Jones et al. 1995, 2002; Hash and Witcombe 2001; Breese et al. 2002). Six major putative pathotypes, based on disease incidence across a set of differential lines, have been reported on pearl millet in India (Thakur et al. 2006), while additional pathogenic variation is present in sub-Saharan Africa (Jones et al. 1995). Inter-simple sequence repeats (ISSR) primers have been used to characterize variability among 22 S. graminicola isolates. The 19 intersimple sequence repeats (ISSR) primers were able to distinguish all these isolates, which formed four major clusters, accounting for 70% of the marker-based variation among isolates (Sudisha et al. 2009), while Jogaiah et al. (2008), based on RAPD and ISSR marker profiling data, grouped the 27 downy mildew isolates into six distinct pathotypes. However, clustering of six pathotypes within groups was not similar when RAPD and ISSR-based dendograms were compared. More recently, Sharma et al. (2010) reported a high level of variation among 46 downy mildew isolates from India for disease incidence, latent period, and virulence index. Based on reaction on a set of nine pearl millet lines, they classified 46 isolates into 21 pathotypes, with pathotype P11 the most virulent, infecting all the nine host differentials. Furthermore, there was little correspondence between the two dendograms generated by the average linkage cluster analysis: The virulence index-based dendogram

302

Foxtail millet Downy mildew (Setosphaeria graminicola) Meera (SR 16), Longgu 28, Jingu 16, Jingu 11, Lugu No 7, Yugu No 3, Lujin 3, Beihuang, Zhenggu 2 Blast (Pyricularia setariae) K74-10-4-4, 73-10-24-15, 72-12-6-3, 77-10-7-9, 77-10-7-24, 7-6-22-21 Nenxian 13, Jigu 1, Jingu 16, Jingu 11, Jinggu 1, Lugu No 7, Yugu No 3, Minquanginggu Smut (Ustilago crameri) Jingu 16, Lugu No 7, K8763 (P.1, gene donor for smut resistance), Saratovskoye 2, Saratovskoye 3, Saratovskoye 6, Veselepodolyanskoye 632, Barnaulskoye 80, Gorlinka Rust (Uromyces setariae-italicae) Lugu No 7, Yugu No 2, Yugu No 3 Job’s tears Leaf blight Akisizuku Smut (Ustilago coicis) Mayuen

Barnyard millet Grain smut (Ustilago panici-frumentacei Brefeld) Large range variation, from highly resistant, to moderately resistant to highly susceptible category, were reported among 257 accessions tested for grain smut spores at anthesis Finger millet Blast (Magnaporthe grisea) GE# 281, 568, 669, 705, 1044, 1293, 1409, 1546, 1855, 3022, 3024, 3058, 3060 and MR 6; IE 287 and IE 976; IC 43335; MR 33, KMR 9 and KMR 3; Gulu E, Seremi 1, Seremi 2, Pese 1, SX8, SEC915; KNE# 620, 629, 688, 814, 1034, and 1149; VL 149, VL 146, Gautami, GPU 28,

Sources of resistance to major diseases in millets crops

Chang and Tzeng 1999

Tetsuka et al. 2008

Jiyaju and Yuzhi 1993

Jiyaju and Yuzhi 1993

Nakayama et al. 2005 Jiyaju and Yuzhi 1993

Jiyaju 1989; Jiyaju and Yuzhi 1993; Maloo et al. 2001

Seetharam 1989, 1998; Gowda et al. 1999; Jain and Yadav 2004; Madhukeshwara et al. 2004; Wanyera 2007; Sreenivasaprasad et al. 2007

Gupta et al. 2009

Reference

Table 5.16. Germplasm and cultivars reported resistance to major diseases in barnyard millet, finger millet, foxtail millet, Job’s tears, pearl millet, proso millet, and tef.

303

Smut (Moesziomyces penicillariae) SSC 46-2-2-1, SC 77-7-2-3-1, SSC 18-7-3-1; ICMV 8282, ICMV8283; ICMA 88006A and ICMA 88006B (resistant to smut and downy mildew); ICMA #91333, 91444 and 91555; 44 accessions selected from the screening of 1747 germplasm; ICML #5–10; ICMPS #100-5-1, 700-1-5-4, 900-1-4-1, 900-3-1, 900-9-3, 1300-2-1-2, 1400-1-6-2, 1600-2-4, 1500-7-3-2, 1800-3-1-2, and 2000-5-2; SSC FS 252-S-4, ICI 7517-S-1, ExB 132-2-S-5-2-DM-1, ExB 46-1-2-S-2, ExB 112-1-S-1-1, and P-489-S-3 Proso millet Smut (Sphacelotheca panici milliacei pers (Bubak)) K8763 (P.1, gene donor for smut resistance), Saratovskoye 2, Saratovskoye 3, Saratovskoye 6, Veselepodolyanskoye 632, Barnaulskoye 80, Gorlinka; ‘II’Inovskoe’ (having Sph2-resistant gene) Tef Rust (Uromyces eragrostidis) Lower levels of rust severity reported in 22 landraces

Ergot (Claviceps fusiformis) ICML #1, 2, 3, 4, 5, 6, 7, 8, 9, 10; ICMA 92666 and ICMB 92666 (resistant to ergot, smut, and downy mildew); ICMA #91333, 91444, and 91555; ICMPE #13-6-30, 134-6-9, 134-6-34, 13-6-27, 37, and 71

Pearl millet Downy mildew (Sclerospora graminicola) ICML #12, 13, 14, 15, 16, and 22; IP #16438 and 16762; P 310-17 and P 1449-3; IP18292; IP18293; 700651; ICMP #312, 423, and 85410; 7042S; 841A; IP #9, 55, 104, 253, 262, 336, 346, 498, 545, and 558; landrace such as Ardi-Beniya Ka Bas, Dhodsar local and Desi Bajri-Chomu Rust (Puccinia sps.) ICML #5, 6, 7, 8, 9, and 10; ICML #17, 18, 19, 20 and 21; Tift 3 (PI 547035) and Tift 4 (PI 547036); Tift 65 (resistant to rust and leaf spot); Tifleaf 3

Dawit and Andnew 20005

Ilyin et al. 1993; Zolotukhin et al. 1998

Thakur et al. 1986; Thakur and King 1988c; Yadav and Duhan 1996; Rai et al. 1998b; Khairwal and Yadav 2005

Thakur et al. 1982; Willingale et al. 1986; Thakur and King 1988a,b; Thakur et al. 1992; Rai et al. 1998a; Khairwal and Yadav 2005

Bourland 1987; Thakur and King 1988a; Wilson and Burton 1991; Burton and Wilson 1995; Hanna et al. 1997

Singh et al. 1997; Khairwal and Yadav 2005; Thakur et al. 2006; Sharma et al. 2007

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grouped the isolates into eight clusters while the AFLP-based dendogram formed seven clusters; four isolates could not be clustered into any of these groups. Ergot (Claviceps fusiformis) infection in pearl millet occurs mainly through the stigmas, and stigma receptivity influences the infection of pearl millet florets by C. fusiformis conidia (Thakur and Williams 1980). For infection to occur, it is essential that the stigmas remain fresh long enough to enable ergot conidia to germinate and for penetrating hyphae to pass down through the stigma to the ovary. The period required for a stigma to be infected by C. fusiformis is approximately between 36 and 48 hours in the tropics. Stigmas that remain fresh for 48 hours or more in the absence of cross- or self-pollination are potentially at risk from ergot. However, escape from ergot becomes likely if the stigma remains receptive for a few hours only (Willingale et al. 1986). Further, postpollination stigmatic constriction, ubiquitous among pearl millets, provides a mechanical barrier to invasion of the fertilized ovary by the fungal pathogen. Pollination thus provides protection against ergot infection as it induces rapid withering of stigmas. Pollen-based escape mechanisms must be avoided while screening for other forms of resistance to ergot. To do that, plants at the boot-leaf stage should be bagged so that the inflorescences emerge into a pollen-free and inoculum-free environment. Such panicles should be inoculated with a conidial suspension containing 1  106 conidia milliliter1 and bagged immediately after inoculation. Very low levels of resistance to ergot have been reported in pearl millet; however, when such germplasms were intermated and the progenies evaluated for ergot resistance during succeeding generations, from F2 to F6, using an improved screening technique, the resistance level increased steadily when individual inoculated inflorescences with little or no ergot were selected to provide selfed seed for the next generation (Thakur et al. 1982, 1985). No major genes for ergot resistance have been reported in pearl millet. Resistance is recessive and polygenic (Thakur et al. 1983). To the authors’ knowledge, there has been no pathogenic variability reported in C. fusiformis. Likewise, resistance to smut (Moesziomyces penicillariae) in most of the ergot susceptible lines is independent of the timing of flowering events, while in ergot-resistant lines, it could be closely related to flowering events (Thakur 1989). Resistance to smut is controlled by a few dominant genes with additive effects (Chavan et al. 1988), although the recessively inherited trichomeless mutation (tr), which removes most aerial trichomes, including stigmatic hairs, is reported to confer partial resistance to smut (Wells et al. 1987; Wilson and Hanna 1998). To our best knowledge, there are no

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definite indications of any pathogenic variation in M. penicillariae populations. Blast (Magnaporthe grisea) is the major disease of finger millet and foxtail millet and damages the leaf, neck, and finger or panicles. This fungus can also be an important disease of pearl millet grain and forage crops and cause disease on many other grasses, including rice. Using a PCR-based method and marker profiling of 328 M. grisea isolates, Srinivasaprasad et al. (2007) demonstrated that M. grisea isolates from East Africa were genetically distinct from those of Asia, and identified 243 haplotypes from 328 M. grisea isolates. Cluster analysis of these haplotypes showed continuous genetic variation and lack of clonal lineage among the blast pathogen populations from East Africa. Some of the shared haplotypes identified were common between countries while others were restricted to one country. Likewise, some of the shared haplotypes represented M. grisea isolates from different parts of the finger millet plant, indicating genetic similarity of isolates capable of causing different types of blast. Furthermore, some of the shared haplotypes also represented M. grisea isolates both from cultivated and wild finger millet, suggesting their genetic similarity; thus, wild finger millets could serve as an alternate host in the field. Pathogenicity tests have further confirmed that all M. grisea isolates caused susceptible blast reactions on finger millet varieties, with variation in aggressiveness. Preliminary genetic analysis of blast resistance to four Japanese fungus isolates suggests that resistance to blast is controlled by more than two dominant genes in foxtail millet (Nakayama et al. 2005). B. Tolerance to Abiotic Stresses All crops are affected by abiotic stresses, and millets are no exception. However, these crops are generally considered well adapted (at least compared to most other cereals) to drought, salinity, high temperature, water logging, soil Al þþþ saturation, and poor soil fertility stresses (Zegada-Lizarazu and Iijima 2005). In addition, the thinner-stemmed millets, such as finger millet, foxtail millet, proso millet, and fonio, are often affected by lodging, especially under conditions of high soil fertility. Lodging is often less problematic in pearl millet, especially in improved cultivars, although some commercialized single-cross hybrids and their parental lines are highly prone to lodging. In addition, the parasitic weed Striga has become a major constraint to finger millet production in Africa (N. Wanyera, NASARRI, Soroti, Uganda, pers. comm.).

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Identification and utilization of undiscovered variation for abiotic stress tolerance could enhance the adaptation of cereal crops. Worldwide, over 161,708 gene bank accessions of the ten millets species preserved in national and international gene banks (see Section IV) provide researchers a unique resource for the discovery and characterization of genetic variation for abiotic stress tolerance that can eventually be harnessed in crop improvement programs. Precise phenotyping is the key to finding and exploiting new genes for abiotic stress tolerance. Phenotypic screens for drought, salinity, and high temperature stresses have been developed by ICRISAT to identify tolerant germplasm (Krishnamurthy et al. 2007; ICRISAT 2009). Further, improved understanding of the physiological and molecular basis of tolerance mechanisms will contribute toward developing more stress-tolerant crops. Unlike other cereals, these millets have received limited research attention to identify sources of resistance to abiotic stresses. More of the research priority was on identifying drought and salinity tolerance in pearl millet, which as a species is also reasonably tolerant to Al toxicity (Flores et al. 1991); drought tolerance in fonio; drought, salinity, low temperature, lodging, and water-logging tolerance in foxtail millet; and drought and salinity tolerance in proso millet (Table 5.17). In a limited way, there have been some gains in understanding the physiological basis of abiotic stress tolerances and the genomic regions associated with control to some of these abiotic stresses (see Section VIII.A); for example, research teams have started developing more drought-tolerant pearl millet inbred lines and hybrids using marker-assisted backcrossing (MABC) (Serraj et al. 2005). 1. Drought. Using seedling survival following repeated drought stress, Li (1991, 1997) grouped 17,799 foxtail millet accessions (17,313 landraces and 486 elite cultivars) into five grades of drought tolerance, with grade 1 accessions being the most drought tolerant and including more elite cultivars than landraces. Using a similar screening procedure, Wen et al. (2005) identified several drought-tolerant landraces and cultivars from Shanxi Province in China. Researchers in China developed a quick and simple screen for drought tolerance using mannitol or polyethylene glycol (PEG-6000) tests and identified relative water content and germination rate under osmotic stress as indicators of drought tolerance at the seedling stage in foxtail millet (Zhang et al. 2005; Zhu et al. 2008). Foxtail millet is most sensitive to drought at the inflorescence and spikelet development stage (about 35 to 50 days after sowing). When comparing water use efficiency (WUE) of the six millet species under waterlogging, well-watered (control), and drought conditions,

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Table 5.17. Germplasm/cultivars reported resistant/tolerant to abiotic stresses in finger millet, foxtail millet, Job’s tears, pearl millet, proso millet, and tef. Abiotic stress and sources of resistance/tolerance DROUGHT Finger millet MR-2 (high-yielding dual-purpose cultivar), AK132-1 Foxtail millet Longgu 28, Nenxian 13, Chingu No 4, Jingu 11; Longgu 25, Longfu 92170, Nuanxuan 8, Chigu 4, Yugu 1, Yugu 2, Zheng 173, Jigu 11, Chengu 7, Jingu 9, Jingu 10, Jingu 16, Yapoche, Dongfangliang, Liutiaoqing, Paosima, Yintianhan, Liutiaoqing, Kaoshanhuang, Shengzitou Pearl millet CZP 9802; 863B, ICMP 83720, ICMV 9413, ICMV 94472, and PRLT 2/89-33 Tef DZ-Cr-37, 237186, 237131 and 212928; Ada and DZ-01-99; Kaye Murri and Ada (35% longer maximum root length under drought stress); Fesho had largest osmotic adjustment SALINITY Finger millet TRY1 Foxtail millet Prasad; Honggu, Xiaohuanggu, and Sanbianchou (tolerant at germination and seedling stage) Pearl millet 10876 and 10878 (Sudan), 18406 and 18570 (Namibia), and ICMV93753 and ICMV 94474 (India); 863-B, CZI 98-11, CZI 9621, HTP 94/54, ICMB 02111, ICMB 94555, ICMB 95333, ICMB 00888, ICMB 01222, ICMP 451, IP 3732, IP 3757, IP8210, and PRLT 2/89-33 Proso millet 008211, 008214, 008215, 0080220, and 008226 (tolerant at seedling stage) LODGING Foxtail millet Longgu 28, Nenxian 13, Jingu 11, Yugu No. 1, Yugu No 2, Yegu 5, Yanggu, Liuyuexian 2, Cang 155, Gufeng 1, An 4844, Heng 8735, Ji 9409, Pin 324, Zheng 9188, Pin 540, Cang 409, An 7169, An 9217, Bao 182 Job’s tears Akisizuku

Reference

Gowda et al. 1998; Seetharam 1998 Chen and Qi 1993; Li 1997

Yadav 2004; Dwivedi et al. 2010 Ayele et al. 2001; Degu et al. 2008; Asfaw and Itanna 2009

Seetharam 1998 Sreenivasulu et al. 1999; Tian et al. 2008 Ali et al. 2004; Dwivedi et al. 2010

Sabir and Ashraf 2007, 2008

Chen 1989; Chen and Qi 1993; Tian et al. 2010

Tetsuka et al. 2008 (continued )

308 Table 5.17

S. DWIVEDI ET AL. (Continued)

Abiotic stress and sources of resistance/tolerance

Reference

WATERLOGGING Foxtail millet Lugu No. 7

Chen and Qi 1993

LOW TEMPERATURE Foxtail millet Liggu No. 26 (adapted to very cold region, which extended foxtail millet cultivation some 385 km farther north to 54 ; normally, the northern limit of foxtail millet cultivation in China was 50 N)

Chen and Qi 1993

Zegada-Lizarazu and Iijima (2005) found that waterlogging significantly reduced WUE in all millets species but drought did not. The ratio of WUE under stress to that under the control conditions indicated that pearl millet had the highest and lowest tolerances to drought and waterlogging conditions, respectively, while barnyard millet was tolerant to both stresses. Postflowering drought (also termed as terminal drought) is the major form of drought that causes substantial reduction in grain and stover yields in pearl millet (Mahalakshmi et al. 1987; Winkel et al. 1997; Bidinger and Hash 2004). Genotypes that flower early, have few but effective basal tillers, are low in biomass, and have a high harvest index (including panicle harvest index) perform better under terminal drought stress (Yadav et al. 2003b; Bidinger et al. 2005). Landraces or traditional cultivars provide a rich source of diversity for tolerance to abiotic stresses in pearl millet (see Section IV.D). Farmers of the drought-prone arid zone of northwestern India (Rajasthan, Gujarat, and Haryana) prefer sowing these traditional landraces or landrace-based materials because of their grain and stover yield advantages over conventionally bred materials (Bidinger et al. 2009). For example, CZP9802, the first open-pollinated variety of pearl millet derived from the landraces of Rajasthan, combines a high level of adaptation to drought stress and outyielded controls—Pusa 266 (grain yield 0.98 t ha1; stover yield 2.1 t ha1) and ICTP 8203 (grain yield 1.14 t ha1; stover yield 2.7 t ha1)—by producing 14% to 33% higher grain and 18% to 36% higher stover yield in arid zone environment (<400 mm of seasonal rainfall) of northwestern India (Yadav 2004). It flowers within 48 days of sowing and matures in 75 days, and thus has the ability to escape terminal droughts that are very frequent in these arid zone environments. Okashana 1, another early-maturing pearl millet variety, selected by the farmers in Namibia from ICRISAT-bred populations, is cultivated on about 50% of the pearl millet area in Namibia (Daisuke 2005). The Iniadi

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landrace from West Africa is early maturing (70 to 85 days), relatively photoperiod insensitive, and productive with lustrous, bold grain and well-exerted, compact, conical panicles. It has contributed to development of large numbers of pearl millet cultivars worldwide (Andrews and Kumar 1996), including ICMV 88904 (released as ICMV 221) (Witcombe et al. 1997), which was bred by recurrent selection for a combination of improved grain yield potential, terminal drought tolerance, and downy mildew resistance, and has been released for cultivation in India, Kenya, Uganda, Eritrea, and Ethiopia. More recently, preliminary results from the screening of finger millet and foxtail millet core collection accessions, using mini lysimeter (cylinders 25 cm diameter and 200 cm long, containing 124 kg of wellfertilized Alfisol) in a partly controlled environment, revealed genotypic differences in response to drought tolerance, with several accessions performing well under drought stress conditions (L Krishnamurthy, ICRISAT, pers. comm.). The genus Eragrostis is widely distributed in dry habitats of tropical, subtropical, and temperate zones of both hemispheres (Boechat and Longhi-Wagner 2000). One of the well-known adaptive features of plants established in dry habitats is the ability to form slime-producing (mycospermatic, mucilaginous) diaspores (e.g., fruits or seeds), which are involved in plant dispersal (Huang et al. 2000; Penfield et al. 2001). Recently, Kreitschitz et al. (2009) reported the presence of slime cells, a type of modified epidermal cell, covering the fruit of tef, which is exclusively composed of pectins. The pectin forms uniform layers on the cell wall inner surface, which in the presence of water quickly hydrate and cause swelling of the slime cells. The ability of the slime to absorb and maintain moisture around the grain is probably an adaptive feature for tef, which may create conditions suitable for rapid germination in dry habitats. Furthermore, grain-filling is the most sensitive growth stage to water stress, and severe water stress has caused significant reduction in physiological performance of tef (Mengistu 2009). Species within the genus Eragrostis differ greatly in their ability to tolerate water stress and had a positive correlation between leaf tensile strength and drought tolerance. Leaf tensile strength strongly correlated with differences in leaf architecture and cell wall chemistry. Leaf tensile properties differed according to the measured position along the lamina (Balsamo et al. 2006). More recently, Degu et al. (2008) found that tef cultivars ‘Kaye Murri’ and ‘Ada’ under drought stress conditions had about 35% longer maximum root length (MRL) compared with that under irrigated conditions, while cultivar ‘Fesho’ had the largest osmotic adjustment (OA) value 1.38 Mpa under similar conditions. In contrast,

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‘Balami’ and ‘Alba’ had decreased MRL and low OA under drought stress conditions, which reveals that the ability to increase MRL and increased OA contributes to better performance under drought conditions (Degu et al. 2008). Baltensperger, working in Nebraska on proso and foxtail millets, developed several proso millet cultivars. Baltensperger, working in nebraska on proso millet and foxtail millet, developed several proso millet cultivars (Baltensperger et al. 1995a,b, 1997, 2004a,b) and foxtail millet germplasm (Siles et al. 2004). Much of this was attributed to early maturity avoidance. 2. Salinity. There has been only limited research reported on response to soil salinity in finger millet, foxtail millet, pearl millet, and proso millet germplasms/cultivars, unlike other cereals (Table 5.18). Wholeplant tolerance to salinity in pearl millet is associated with reduced shoot N content and increased K þ and Na þ contents, while K þ /Na þ and Ca þ þ /Na þ ratios are of lesser importance. Genetic variation exists for shoot biomass ratio (shoot biomass under salinity/shoot biomass from nonsaline control), associated with salt tolerance, and shoot Na þ concentration could be considered as a potential nondestructive selection criterion for vegetative-stage screening (Krishnamurthy et al. 2007). Salt-tolerant proso millet accessions produced high biomass but accumulated low amount of Na þ in their shoots and roots under saline conditions, while salt-sensitive accessions accumulated a high amount of Na þ under saline conditions. The salt-tolerant accessions also maintained higher K þ /Na þ ratios than the salt-sensitive accessions (Sabir and Ashraf 2007). Using relative germination rate at 1.0% and 1.5% NaCl concentration, Zhi et al. (2004) screened 260 foxtail millet landraces and cultivars and detected a large range of variation: 0% to 20% in 29 accessions; 21% to 50% in 45 accessions; 51% to 90% in 153 accessions; and over 90% in 33 accessions. Glutamine synthetase (GS) and pyrroline-5-carboxylate (P5C) reductase are important for proline synthesis. Veeranagamallaiah et al. (2007) studied the changed expression profile of glutamine synthetase and pyrroline-5-carboxylate (P5C) reductase under saline conditions using salt-sensitive (Lepakshi) and salt-tolerant (Prasad) foxtail millet cultivars. Salt stress resulted in significant accumulation of proline in seedlings of both the cultivars; however, proline accumulation was more in the tolerant than in the sensitive cultivar and was positively correlated with increased glutamine synthetase and P5C reductase activities. More recently, preliminary results from the screening of finger millet and foxtail millet core collections accessions in pot (23 cm diameter) culture using Alfisol (11 kg well-fertilized soil) in a partly controlled

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Table 5.18. Summary of DNA-based markers available in barnyard millet, finger millet, foxtail millet, pearl millet, proso millet, and tef from 2002 to 2010. Summary of DNA markers reported Barnyard millet 3 of 5 SSR loci isolated from Echinocloa colona Finger millet 3 EST-derived SSR 9 of 31 EST-derived SSRs polymorphic in finger millet producing 2 alleles, while 11 EST-SSRs polymorphic in pearl millet Foxtail millet
1000 SNPs by sequencing pools of RILs (S. italica acc. B100  S. virdis acc. A10)

12 EST-derived SSR 100 polymorphic SSRs developed from 2 genomic DNA libraries Job’s tears 17 polymorphic SSRs isolated from a microsatelliteenriched library of Job’s tears Pearl millet >100 polymorphic EST-SSR markers mapped in 1 or more of 4 pearl millet RIL populations
250-280 DArT markers polymorphic in each of 3 pearl millet RIL populations 11 of 31 finger millet EST-derived SSR primer pairs detected polymorpism in pearl millet 4 EST-SSRs and 9 CISPs detecting polymorphism in 1 or more of 4 pearl millet biparental mapping populations A set of 21 polymorphic EST-SSRs and 6 genomic SSRs 19 EST-derived SSR primer pairs, of which 11 gave amplification products and 4 detected polymorphism on agarose gels 16 EST-derived polymorphic SSRs SSCP–SNP primer pairs developed by comparison of rice and pearl millet EST sequences 36 SSRs derived from from genomic library 18 SSRs derived from genomic library

Proso millet 46 polymorphic SSRs from rice, wheat, oat, and barley

Reference Danquah et al. 2002; Nozawa et al. 2006 Nnaemeka 2009 Arya et al. 2009

http://www.plantbio.uga. edu/media/ 2010_grad_symposium (1).pdf Nnaemeka 2009 Jia et al. 2009b

Ma et al. 2006

Rajaram et al. 2010 Senthilvel et al. 2010 Arya et al. 2009 Yadav et al. 2008

Senthilvel et al. 2008 Yadav et al. 2007

Mariac et al. 2006b Bertin et al. 2005 Qi et al. 2004 Budak et al. 2003; Allouis et al. 2001; Qi et al. 2001 Hu et al. 2009 (continued )

312 Table 5.18

S. DWIVEDI ET AL. (Continued)

Summary of DNA markers reported Tef 262 polymorphic SSR markers 80 EST-derived SSRs 8 MSeI- and 8 EcoRI-based AFLP primers; 8 ISSR markers; 22 EST-derived SSRs and 10 SSRs from rice 8 polymorphic ISRs

Reference Zeid et al. 2010 Yu et al. 2006b Chanyalew et al. 2005

Assefa et al. 2003b

environment revealed genotypic differences for salt (100 mM concentration saturating the soil to field capacity) tolerance, with several accessions outyielding the contols (L. Krishnamurthy, ICRISAT, pers. comm.). 3. Low Temperature. The northern limit of the foxtail millet cultivation in China was 50o N. However, researchers in China have developed a foxtail millet cultivar (Table 5.17) that is tolerant to extreme cold and thus extended the cultivation of foxtail millet 385 km farther north to 54 (Chen and Qi 1993). 4. Lodging. Lodging is a constraint in many crops, including millets, causing substantial losses in grain yield and quality. Both crop management and environmental factors impact lodging (Berry et al. 2005). Finger millet, foxtail millet, proso millet, tef, and the fonio are reported to suffer from lodging. The use of lodging-resistant cultivars along with good crop husbandry is the most effective way to minimize losses due to lodging. Knowledge of traits associated with lodging and identifying a suitable method to assess lodging are essential steps to select for lodging resistance and to predict the risk of lodging in a cultivar. A lodging coefficient based on stem and root traits associated with lodging is found to be a suitable indicator of field selection for lodging resistance in foxtail millet (Tian et al. 2010). Further, the study revealed that mechanical strength of the stem and plant height were the most important contributors to lodging coefficient in the landraces, whereas the weights of the aboveground and underground tissues in combination with mechanical strength of the stem were most important in the improved cultivars. A number of landraces and improved cultivars that resist lodging have been reported in foxtail millet from China (Table 5.17), which could be used as a resource of this trait to transfer into new breeding lines. Most recent proso millet lines developed in

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the United States have had strong selection for lodging resistance (Baltensperger et al. 1995a,b, 2004a). 5. Waterlogging. There are relatively few reports on waterlogging in millets. Based on the changes in dry-matter production and transpiration coefficient under varying soil moisture conditions, Kono et al. (1987) classified cereal crops into four groups: rice and Job’s tears are susceptible to drought but tolerant to waterlogging; finger millet and Japanese barnyard millet are relatively tolerant to both drought and waterlogging; proso millet, pearl millet, sorghum, and maize are relatively susceptible to waterlogging but tolerant to drought; and foxtail millet is highly susceptible to waterlogging but tolerant to drought. Further studies under prolonged waterlogging stress detected substantial reduction in number of roots in foxtail millet and slight reductions in proso millet and pearl millet. However, total root numbers increased in rice, finger millet, Job’s tears, Japanese barnyard millet, sorghum, and maize (Kono et al. 1988). No systematic study on waterlogging has been reported on other millet crops, but ‘Lugu 7’ foxtail millet has been found tolerant to waterlogging (Chen and Qi 1993). C. Seed Quality Seed size, seed color, protein and fat contents, and minerals and vitamins are important traits that influence grain quality in cereals including millets, and various procedures have been developed to measure these effectively (Gomez et al. 1997). Variations in amino acid composition influence the protein quality. Various reports indicate sufficient genetic variation for seed quality traits, which has been exploited to develop cultivars with high protein or fat content in some millet crops. For example, Chinese cultivars of foxtail millet ‘Anzhenhuanggu’, ‘Baocaohonggu’, ‘Gouweisu’, ‘Huangshugu 01724’, ‘Huiningdaheigu’, ‘Lazhutaigu 013611’, ‘Pin114’, ‘Pingliangmaocaogu’, and ‘Xiaohonggu 015147’ have high seed protein (15%–18%) and fat (5%) (He et al. 2002; Dong and Cao 2003; Zhu et al. 2004). Finger millet germplasm accessions with high seed protein include GE 2500, 1168, MS 174 and MS 2869, while those with high seed calcium are Malawi 1915 and CO 11 (Vadivoo et al. 1998). More recently, researchers at ICRISAT identified finger millet germplasm accessions with relatively high seed protein (8.5%–12.7%), calcium (3.2–5.2 g kg1 seed), iron (41–56 mg kg1 seed), and zinc (26–31 mg kg1 seed) contents, which were higher than the best controls (protein 8.2%; Ca 3.1 g kg1 seed; Fe 40.3 mg kg1 seed; and Zn 22.9 mg kg1). Likewise, some foxtail millet accessions had higher seed protein (17.8%), calcium

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(288 mg kg1 seed), iron (59 mg kg1 seed), and zinc (74 mg kg1 seed) contents than the controls (protein 13.4%, Ca 152.8 mg kg1 seed, Fe 48.6 mg kg1 seed, and Zn 52 mg ka1 seed) (ICRISAT 2009). An earlymaturing foxtail millet germplasm, Super Early Maturation No. 2, has been developed that has high protein (14.4%), fat (6.2%), and iron (54.1 mg kg1) contents and requires 1650oC heat units to mature at approximately 1,400 m altitude in Bashang, China (Liu et al. 2006). Chinese researchers have also reported large variation in vitamin E content (2.74 mg g1–90.97 mg g1) among foxtail millet landraces Huangbangtou, Huangtenggu, Xiaohuanggu, and Yazuinian (Li et al. 2009). Pearl millet grain contains 17.4% protein, 6.3% fat, 2.8% fiber, and 2.2% ash (Sawaya et al. 1984). Pearl millet landraces of diverse origin differ in fatty acid composition, with linoleic acid (45%), oleic acid (23%), and palmitic acid (22%) being the dominant fatty acids (Jellum and Powell 1971). More recently, pearl millet germplasm and advanced lines with high iron and zinc contents, which are positively correlated, have been identified (http://www.harvestplus.org). Some newly developed hybrids had more than 70 ppm grain Fe and in excess of 50 ppm Zn contents, with two hybrids showing 80 to 85 ppm Fe and 70 ppm Zn, which are higher than those reported in improved cultivars of other cereal crops (ICRISAT 2009). Chinese proso millet accessions Dabairuanmi 0673, Taianhuangmi 2657 and Yongchanghuangmi 2659 showed high protein content (17%–19%), whereas 80-4064, Dahuangshu 2643 and Heimizi 4392 had high fat (
5.5%); and Edanbai 0885, Hongmizi, and Ziganhong had both high protein and fat contents (Wang et al. 2007a). Proso millet cultivar ‘Tololanskoe’ is reported to contain high protein content (13.6%) (Kalinova and Moudry 2006). The protein content of Japanese barnyard millet ranged from 11.1% to 13.9% (Monteiro et al. 1987). Significant work at utilization of the waxy trait has been conducted in the United States to improve specific food quality in proso (Heyduck et al. 2008; Graybosch and Baltensperger 2009). Millets and other cereals are deficient in some of the essential amino acids, such as lysine (Geervani and Eggum 1989). The lysine content in foxtail millet germplasm ranges from 0.20% to 0.30% (Zhu et al. 2004; Tian et al. 2009); however, there are some high-lysine foxtail millet cultivars (e.g., ‘Gouweisu 27531’, ‘Gouweisu 27510’, and ‘Xiaomi 27516’) (Zhu et al. 2004). Compared to other millets, proso millet grains are richer in essential amino acids (leucine, isoleucine, and methionine) and contain about 3.3 g kg1 of the limiting amino acid lysine (Vadivoo et al. 1998). High lysine content has been reported in proso millet

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cultivar ‘Belgorodskoe’ (Kalinova and Moudry 2006). Black and grey seeded foxtail millet germplasm often have higher lysine contents (He et al. 2002). Pearl millet seeds are relatively larger than other millets, with 1,000seed mass ranging from 1.5 g to 21.3 g and averaging 8 g to 12 g among germplasm accessions (Upadhyaya et al. 2007b; Loumerem et al. 2008). Foxtail millet grains are relatively small compared with other cereals, with 1,000-seed mass ranging from 1.9 g to 3.6 g (Liang and Quan 1997). Finger millet 1,000-seed mass averaged 2.6 g (Vadivoo et al. 1998). Proso millet seeds are larger (3–10 g 1,000-seed mass, average
7.0 g) than foxtail millet but smaller than pearl millet. Nonwaxy proso millet cultivars usually have larger seed than waxy types (Wang 2006). Much of the selection for proso millet and foxtail millet in the United States has been based on large seed size (Baltensperger et al. 1995a,b). Variation in seed color can influence seed quality. For example, white-seeded finger millet accessions had higher protein content than brown-seeded types, while white-grained types had higher prolamin and lower glutelin levels than those with brown-grain types (Vadivoo et al. 1998). Black- and grey-seeded foxtail millet germplasm have high protein content (He et al. 2002). Ethiopian farmers overwhelmingly selected a very white-seeded tef variety, DZ-01-196 (Magna), which gets a premium price in the market, although variation in seed color has no effect on agronomic or nutritional traits (Belay et al. 2006). Foxtail millet has been cultivated in China for a very long time, with ancient farmers selecting landraces with better taste and cooking quality. Foxtail millet landraces with superior cooking characteristics are Jinmin, Jiugenqi, Qinzhouhuang, and Taohuami (Dong et al. 2003). Most foxtail millet landraces and cultivars in China are yellowseeded, the preferred seed color. More recently, however, whiteseeded cultivars have been bred to meet diversified market demands (Diao 2007). Grains of pearl millet, finger millet, fonio, proso millet, foxtail millet, and tef are brewed to produce beer. Genotypic differences in brewing quality have been reported. For example, a preponderance of ß-amylase as the major starch-degrading enzyme has been found in fonio millet cultivars ‘Nock 2’, ‘KN 3’, and ‘Chori 1’, which is similar to the enzyme profile in barley (Nzelibe et al. 2000). Further, malt of ‘Chori 1’ has a-amylase content similar to that in barley (Nzelibe and Nwasike 1995; Nzelibe et al. 2000). Finger millet malt is prized for its high diastatic power and is second only to that of barley in its ability to hydrolyze starches (NRC 1996).

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VI. GENOMIC RESOURCES A. Markers and Genetic Linkage Maps The discovery of DNA markers and construction of genetic linkage maps in millets lagged behind other cereals such as rice, wheat and maize (reviewed in Dwivedi et al. 2007). Pearl millet, foxtail millet, finger millet, Job’s tears and tef among the millets have been investigated for development of PCR-based markers (Table 5.18) and construction of genetic linkage maps (Table 5.19). The foxtail millet has the largest collection of single-nucleotide polymorphisms (SNPs) and a high-density SNP-based genetic map, with
1,000 SNP markers evenly mapped to all nine chromosomes (http://www.plantbio.uga.edu/media/2010_grad_symposium(1).pdf). An consensus genetic map (418 cM) of pearl millet, based on four crosses, mapped 353 RFLP and 65 SSRs into seven linkage groups, with
85% of the markers occupying less than a third of the total map length (Qi et al. 2004). Recently, an array of about 6,900 Diversity Array Technology (DArT) clones was developed using PstI/BanII complexity reduction and is now available for mapping lowcost, high-throughput DArT markers in pearl millet (Senthilvel et al. 2010). Further, Senthilvel et al. (2010) also identified 256 to 277 polymorphic DArT markers in three pearl millet recombinant inbred lines (RIL) populations, which they have integrated with simple sequence repeat (SSR) data to construct individual genetic maps, each with >300 marker loci. Over 200 DArT markers were mapped in more than one population, and their mapping positions were reasonably consistent across maps. Among these, 32 DArT markers representing all seven pearl millet linkage groups were mapped in all three RIL populations, permitting the development of a well-saturated pearl millet consensus linkage map combining DArT and SSR markers. Recently some DNA markers from rice, wheat, oat, and barley have shown polymorphism in proso millet (Hu et al. 2009). More recently, Reddy et al. (2010) isolated 41 resistant gene homologues from a popular finger millet cultivar, ‘UR762’, which showed strong homology to NBSLRR type R-genes of other crop species. The molecular cloning of these resistant gene homologues may provide new ways to deploy these genes against biotic stresses. Clearly, more directed efforts are needed to develop markers in other millets. One way to overcome the paucity of DNA markers in these millets is to try markers from other cereals, as both macro- and micro-synteny have been reported among cereals (Devos et al. 2000; Srinivasachary et al. 2007; Yadav et al. 2008; also see Section VIII.D). Recent work on switchgrass (Panicum virgatum) has shown

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Table 5.19. Summary of genetic linkage maps reported in finger millet, foxtail millet, pearl millet, and tef from 1994 to 2007. Summary of linkage maps reported Finger millet 131 markers mapped to 16 LGs on A genome, with a total map distance 721.4 cM, while 196 markers to 9 LGs on B genome covering 786.8 cM map distance 332 loci from 266 primers mapped into 26 LGs. 13 on A-genome and 9 on B-genome LGs assembled into 9 homologous groups, 6 six of these corresponding to a single rice chromosome each, while remaining 3 were orthologous to 2 rice chromosomes; gene orders between rice and finger millet highly conserved Foxtail millet A high-density genetic map with
1000 SNPs evenly mapped to all 9 chromosomes; a number of chromosomal rearrangements, including several previously unknown rearrangements, relative to sorghum and rice genomes

81 SSR and 20 RFLP markers mapped to 9 LGs, with a total map length of 1654 cM, and marker density of 16.4 cM 160 RFLP loci mapped to 9 LGs, with a total map distance of 964 cM Job’s tears 80 AFLP and 10 RFLP markers mapped to 10 LGs, with a total map length of 1339.5 cM, average marker density 14.88 cM Pearl millet A map with 55 RFLP and 32 genomic SSR and 17 EST-SSR loci spanning 675 cM An integrated genetic map, based on 4 crosses, mapped 353 RFLP and 65 SSRs into 7 linkage groups (LGs),
85% of the markers occupying less than a third of the total map length A map with 61 RFLP and 30 SSR loci spanning 476 cM 181 RFLP loci mapped to 7 LGs, with a total map length of 303 cM and
2 cM marker density A map with 38 RFLP markers covering 280 cM Tef 252 SSR loci mapped to 30 LGs, with a total map length of 1277.4 cM (78.7% genome coverage), averaged marker density 5.7 cM 156 loci from 121 markers (RFLP, SSR, SNP/INDEL, IFLP, ISSR) mapped to 21 LGs, with a total map length of 2081.5 cM and 12.3 cM marker density 166 markers (AFLP, ISSR, and SSR) mapped to 20 LGs, covering 2112.3 cM and marker density of 12.7 cM.

Reference Dida et al. 2007

Srinivasachary et al. 2007

http://www. plantbio.uga. edu/media/ 2010_grad_ symposium(1). pdf Jia et al. 2009b Wang et al. 1998

Qin et al. 2005

Senthilvel et al. 2008 Qi et al. 2004

Yadav et al. 2004a Liu et al. 1994 Jones et al. 1995 Zeid et al. 2010

Yu et al. 2006a

Chanyalew et al. 2005 (continued )

318 Table 5.19

S. DWIVEDI ET AL. (Continued)

Summary of linkage maps reported

Reference

149 RFLP loci mapped to 20 LGs, with a total map distance of 1489 cM and marker density of 9.99 cM; alignment of tef RFLP map with the rice RFLP map shows synteny and collinear gene order between the 2 genomes 211 AFLP loci mapped to 25 LGs, with a total map distance of 2149 cM, marker density of 10.4 cM

Zhang et al. 2001

Bai et al. 1999

many common expressed sequence tag (EST) markers with proso millet (Tobias et al. 2008). B. Characterization and Functional Validation of Genes Associated with Important Traits A number of QTLs have been identified and mapped for resistance to downy mildew, drought tolerance, grain yield and yield components, and for stover quality in pearl millet and for agronomic traits in foxtail millet and tef (see Section VIII.A). Linkage analysis in most of these studies allowed identification of genes/QTLs at a distance as large as 10 to 40 cM from the nearest markers, which may not be suitable for either marker-assisted breeding or for identification/cloning of candidate genes. Unlike other cereals such as rice, maize, and barley (Table 5.20), the only studies reported on functional validation of genes associated with agronomic traits in millets are for the tb1 and ba1 genes associated with branching (basal and axillary) in foxtail millet (Doust and Kellogg 2006); PHYC gene associated with flowering time and morphological variation (spike length and stem diameter) (Sa€ıdou et al. 2009); a major drought-tolerance QTL on linkage group 2 (Sehgal et al. 2009) in pearl millet; and the SiOPRI gene associated with osmotic adjustment and improved drought tolerance in foxtail millet (Zhang et al. 2007b). Further, toward identifying candidate genes for salt tolerance in foxtail millet, Jayaraman et al. (2008) used the cDNA–AFLP technique to compare gene expression profiles of salt-tolerant and salt-sensitive cultivars in foxtail millet, and identified 27 nonredundant differentially expressed cDNAs unique to genes involved in metabolism, cellular transport, cell signaling, transcriptional regulation, messenger ribonucleic acid splicing, seed development and storage in the salttolerant cultivar ‘Prasad’. The expression patterns of seven such genes showed a significant increase in ‘Prasad’ after 1 hour of salt stress in comparison to the salt-sensitive cultivar ‘Lepakshi’. More recently,

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Table 5.20. Summary of quantitative trait loci (QTL) or gene association with important traits and their validation in barley, foxtail millet, maize, pearl millet, and rice from 1995 to 2009. Trait Barley Flowering time Foxtail millet Drought (osmotic adjustment) Vegetative branching (basal and axillary) Maize Plant architecture Yield Pearl millet Flowering time, plant and spike morphology Rice Heading time Grain number Seed shattering Salt tolerance UV resistance Submergence tolerance

QTL/gene

Validation

References

Ppd-H1

Association

Stracke et al. 2009

SiOPR1

Zhang et al. 2007b

tb1 and ba1

Doust and Kellogg 2006

Tb1 lcyE

Complementation Mutagenesis

Doebley et al. 1995, 1997 Harjes et al. 2008

PHYC

Association

Sa€ıdou et al. 2009

Hd1/Se1 Hd3a Gn1/CKX2 qSH-1/RPL sh4 SKC1 qUVR-10 Sub1

Transformation Transformation Transformation Complementation Transformation Transformation Transformation Transformation

Yano et al. 2000 Kojima et al. 2002 Ashikari et al. 2005 Konishi et al. 2006 Li et al. 2006 Ren et al. 2005 Ueda et al. 2005 Xu et al. 2006

Lata et al. (2010) detected above 2.5-fold variation in nine up-regulated transcripts between drought-tolerant and susceptible cultivars upon dehydration stress. The induction of these genes suggests their function in regulation of dehydration tolerance in foxtail millet. These researchers therefore initiated cloning of full-length copies of some of the known and unknown up-regulated genes and will analyze their functions to identify candidate genes for drought tolerance in foxtail millet. In summary, the limited published research on QTL mapping and validation among millets has been restricted only to foxtail millet, pearl millet, and tef and research on gene expression for abiotic stresses tolerance has been limited to pearl millet and foxtail millet, largely because of the nonavailability of DNA markers or sequences in most of the other millets. Clearly, more efforts should be directed toward the development of large numbers of genic and genomic markers to conduct

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association genetics for identification and validation of candidate genes associated with important traits. C. Genomic and Genetic Tools to Sequence the Foxtail Millet Genome Foxtail millet has a highly conserved genome structure relative to the ancestral grass lineage (Devos et al. 1998). It is a diploid grass with a relatively small genome (490 Mb) and is closely related to bioenergy grasses, such as switchgrass (Panicum virgatum), napiergrass (Pennisetum purpureum), and pearl millet. It is an ideal model crop to investigate plant architecture, genome evolution, and physiology in the bioenergy grasses (Doust et al. 2009). In 2008, the Joint Genome Institute of the U.S. Department of Energy announced support for developing genomic and genetic tools to complement sequencing of the foxtail millet genome and for the improvement of biomass production for bioenergy crops (http:// GenomicScience.energy.gov/research/DOEUSDA). Four U.S. universities along with the Hudson Alpha Institute for Biotechnology of Huntsville, Albama, and the Joint Genome Institute of Walnut Creek, California, are involved in sequencing of the foxtail millet genome and development of the complementary tool sets. The latest report from this group revealed that draft genome sequencing of foxtail millet has been completed to 8.3  coverage, with the aligned sequence showing a high degree of synteny to rice and sorghum, even though these lineages last shared a common ancestor more than 50 million years ago (Mitros et al. 2010). The ongoing genetic and genomic research on foxtail millet includes annotation and mining of the full genome sequence, development of foxtail millet bacterial artificial chromosome (BAC) and expressed sequence tag (EST) resources, comparative analysis with sorghum and rice, characterization of orthologous copies of genes controlling biomass in other grass groups, establishment of efficient transformation protocols, creation of new mapping populations, and QTL analyses to identify new candidate genes for plant architectural variation. In addition, resequencing of several diverse green foxtail millet accessions will provide a data set that allows measurement of the overall genetic variability present within the wild and cultivated crop and will a source of markers for mapping and biodiversity studies (Doust et al. 2009, 2010; see Section VII.A). Other genomic tools available for foxtail millet research include the availability of >100 SSRs and the genetic map (see Section VI.A),
1,500 SNPs, the genome sequences from other cereals (see Section VIII.D), the QTL associated with agronomic traits (see Section VIII.A), and candidate genes

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associated with agronomic traits (see Section VI.B). All of these resources are expected to support molecular breeding in foxtail millet. VII. ENHANCING USE OF GERMPLASM IN CULTIVAR DEVELOPMENT A. Core, Mini-Core and Reference Sets for Mining Allelic Diversity and Identifying New Sources of Variation Core (
10% accessions of the entire collection) and mini-core (
10% accessions of the core collection or
1% of entire collection) collections are cost-effective sources to identify accessions with desirable agronomic traits, including resistance to biotic and abiotic stresses. To date, core and mini-core collections (based on phenotypic characterization and evaluation data) are reported in finger millet, foxtail millet, little millet, pearl millet, and tef (Table 5.21). Limited evaluation of finger millet and foxtail millet core collections has resulted in identification of germplasm accessions that mature early, produce more grain or fodder in comparison to control cultivars, or differ in panicle shape and size and seed color and of a few accessions tolerant to drought or salinity. Many of accessions with grains having high seed protein, calcium (Ca), iron (Fe), and/or zinc (Zn) contents were also identified (ICRISAT 2009). Moreover, the core or mini-core collections are dynamic in nature, and these must be augmented, as recently done in pearl millet. Researchers at ICRISAT have developed a global composite collection in pearl millet, finger millet, and foxtail millet, which were genotyped (using SSRs and high-throughput assay, ABI3700) to determine population structure and diversity prior to formation of reference germplasm sets. This reference set captured between 87% to 95% allelic diversity of the composite collections (www.generationcp.org; ICRISAT 2009). Clearly, more research is needed to develop these subsets in other millets or to augment the existing subsets to make them more relevant to the changing needs of crop breeding. B. Assessing Population Structure and Diversity in Germplasm Collections Vast collections of millets germplasm are maintained worldwide in gene banks (see Section IV), and in many cases core or mini-core collections have been formed (see Section VII.A), representing diversity present in the entire collection of a given species. Such reduced subsets are ideal resources to dissect population structure and diversity (both at

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Table 5.21. Core collection, mini-core subset, and genotype-based reference set reported in finger millet, foxtail millet, little millet, pearl millet, and tef. Crop Core collection Finger millet Foxtail millet Little millet Pearl millet Tef Mini-core collection Finger millet Foxtail millet Pearl millet Genotype-based reference set Finger millet Foxtail millet Pearl millet

No. accessions 622 551 155 55 1600 2094 (revised core) 320

Reference Upadhyaya et al. 2006 Gowda et al. 2007 Upadhyaya et al. 2008 Gowda 2008 Bhattacharjee et al. 1997 Upadhyaya et al. 2009 http://www.database.prota.org

80 35 238

Upadhyaya et al. 2010 ICRISAT unpublished data Upadhyaya et al. 2011

300 200 300

ICRISAT unpublished data ICRISAT unpublished data ICRISAT unpublished data

phenotypic and molecular level), to identify new sources of variation, and to conduct association mapping, which provides insights to markertrait association. In the last few years, there have been greater efforts to develop PCR-based markers, especially microsatellites and SNPs, and/ or DArT markers (see Section VI.A), which were employed to assess population structure and diversity in barnyard millet, common millet, finger millet, foxtail millet, Job’s tears, pearl millet, and tef germplasm collections (Table 5.22). For example, barnyard millet accessions belonging to var. esculenta were less diverse than those of var. crus-galli or var. formosensis (Nozawa et al. 2006), and the molecular profile of tetraploid E. oryzicola is different from that of hexaploid E. crus-galli var. formosensis (Nozawa et al. 2004). Microsatellites differentiated finger millet subsp. africana accessions from those of subsp. coracana originating either from Africa or Asia (Dida et al. 2008). Wang et al. (2010) detected a low level of genetic diversity in Setaria virdis (green foxtail millet) in comparison to its cultivated form, Setaria italica. In addition, they also found that despite a 55% loss of its wild diversity, S. italica still harbors a considerable level of diversity when compared to rice and sorghum. Likewise, the level of linkage disequilibrium in S. italica extends to 1 kb; it decayed rapidly to a negligible level within 150 bp in S. virdis. The 17 SSRs differentiated most of the Chinese Job’s tears accessions from those of Korean accessions, and the Chinese accessions

323

Foxtail millet 77 S. italica and 40 S. virdis accessions, rDNA IGS

Finger millet 109 accessions including wild types and 45 SSRs

170 accessions and 13 SSRs

Barnyard millet 155 accessions and 3 SSRs

Accessions and markers

PCR-based length polymorphism and sequence polymorphism of rDNA intergenic spacer (IGS) clearly demonstrated genetic differentiation between cultivated and wild forms from northern Pakistan and Afghanistan; cultivated forms to some extent showed genetic differentiation between diffient areas, while wild forms clearly showed differentiation between regions in northern Pakistan.

E. coracana germplasm grouped into 3 distinct clusters: subsp. africana, subsp. coracana originating from Africa, and subsp. coracana originating from Asia, with few accessions showing introgression between the African and Asian cultivated germplasm pools, and lower diversity in Asian subpopulation probably due to small number of founder plants involved in its origin.

The 155 accessions included 49 from var. esculenta, 94 from var. crusagalli, and 12 from var. formosensis. SSR markers clustered the var. esculenta accessions into 2 groups (either from central and northeastern Japan or northern and southern Japan), crusa-galli accessions into 12 groups, and formosensis accessions into 6 groups. E. esculenta were less diverse than either of crusa-galli or formosensis accessions. The var. esculenta accessions grouped into 2 classes, while those from var. crus-galli into 11 classes. Marker EC1 discriminated E. oryzicola (a tetraploid species) from the hexaplopid species E. crus-galli var. formosensis.

Pattern of population structure and diversity

(continued )

Fukunaga et al. 2010

Dida et al. 2008

Nozawa et al. 2004

Nozawa et al. 2006

Reference

Table 5.22. Assessment of population structure and diversity as reported in barnyard millet, common millet, finger millet, foxtail millet, and tef germplasm.

324

Job’s tears 79 accessions (Korea and Japan) and 17 SSRs

39 Setaria species and 19 RAPD markers

81 accessions and AFLP markers

Most Chinese accessions genetically distinct from Korean accessions; genetic relatedness and place of collection not related; greater within population polymorphism in Chinese accessions, potentialy a reservoir of novel alleles for crop improvement.

DNA sequence variation at 9 loci revealed low level of genetic diversity in wild green foxtail (q ¼ 0.0059). Despite of a 55% loss of its wild diversity, the cultivated foxtail millet still harbored a considerable level of diversity (q ¼ 0.0027) compared to rice (q ¼ 0.0024) and sorghum (q ¼ 0.0034). LD in domesticated foxtail millet extends to 1 kb, while it decayed rapidly to a negligible level within 150 bp in wild green foxtail millet. Landraces grouped into 5 major clusters: cluster I and II and to some extent cluster IV contain landraces from East Asia including China; cluster III from subtropical and tropical regions in Asia; cluster V from central and western regions of Eurasia; Chinese landraces highly variable among the germplasm studied. Chinese accessions were highly diverse, consistent with the hypothesis of a center of domestication in China, while accessions from eastern Europe and Africa form 2 distinct clusters. The genetic relatedness within S. virdis or between S. virdis and S. italica is probably due to consequence of geneflow between the two subspecies. RAPD analysis revealed that S. italica more closely related to S. virdis, supporting idea that the former originated from the latter. Setaria italica and S. glauca differ considerably. S. glauca and S. sphacelata distinct from S. italica, implying that it will be difficult to transfer some of the beneficial traits from S. glauca and S. sphacelata to S. italica.

50 S. italica and 43 S.virdis accessions, sequence variation at 9 loci

62 landraces and 16 RFLP markers

Pattern of population structure and diversity

Accessions and markers

Table 5.22 (Continued)

Ma et al. 2010

Li et al. 1998

Le Thierry d’Ennequin et al. 2000

Fukunaga et al. 2002b

Wang et al. 2010

Reference

325

72 inbreds (70 B-lines and 2 R-lines) and 34 SSR primer pairs

22 inbreds and 627 markers

2000 lines and 24 SSRs

Pearl millet 145 WCA inbreds and 20 SSRs

STRUCTURE analysis detected 5 subgroups and 1 admixed group. Plotting the STRUCTURE results on the geographic map revealed no obvious association either of country of origin or agroecological zone of origin. Established a diversity panel of 288 genotypes, 4 maturity groups representing the whole breadth of genetic variation in the pearl millet germplasm pool from Africa and Asia. 267 of the 627 markers (100 pearl millet genomic SSRs, 60 pearl millet EST SSRs, 410 intron sequence haplotypes, and 57 exon sequence haplotypes) were polymorphic among the 22 inbred lines, which were grouped into 3 clusters with most of the inbreds derived from landrace Iniadi in cluster I; high correlation (r >0.97, P <0.05) between the patterns of diversity exposed by different marker systems. The 72 hybrid parental lines included 70 phenotypically diverse B-lines developed at ICRISAT-Patancheru from diverse germplasm and breeding materials of African, Asian, and American origin, and 2 elite R-lines. Genetic similarity estimates among these inbreds varied from 0.05 (ICMR 356 and ICMB 01666) to 0.73 (ICMB 97444 and ICMB 95555), with a mean of 0.29. Five major clusters were detected, with the smallest comprised of R-line ICMR 356, 2 older B-lines (81B and ICMB 841) and 2 more recent B-lines (ICMB 95333 and ICMB 98777). The second cluster included 30 B-lines, including 843B, arranged in 4 major subclusters. The third cluster appeared to contain elite R-line ICMP 451 and 5 B-lines including 863B and ICMB 88004. The fourth and fifth cluster included 17 B-lines each, arranged in 3 subclusters.

(continued )

Kapila et al. 2009

Thudi et al. 2010

Yadav et al. 2010

Stich et al. 2010

326

Proso millet 118 accessions and 46 SSRs

10 landraces and 16 RFLP markers

53 accessions and 30 SSRs

118 accessions grouped into 5 clusters that parallel with their known geographical distribution; accessions from the Loess Plateau ecotype were more genetically diverse than other 5 ecotypes reported from China.

The cultivated accessions showed significantly lower number of alleles and lower gene diversity than wild types. Wild accessions from the central region of Niger showed introgression of cultivated alleles, while cultivated accessions from the western, central, and eastern Niger showed introgressions of wild alleles, wild populations thus interesting source of new alleles and new allele combinations, which could be useful to broaden the genetic base of cultivated pearl millet. The material included 14 and 13 landraces from western and eastern Rajasthan and 12 control cultivars. The diversity analysis revealed much higher variation within landrace population than between regional samples. Variation between landrace groups bearing a specific name from eastern Rajasthan was higher than intragroup variation. Greater gene flow among landrace populations of western Rajasthan due to frequent exchange of seed materials among farmers. Two major and 8 minor clusters formed involving 53 lines, the genetic distance ranged from 0.28 to 0.92, and few unique lines with potentially important new sources of alleles identified for enhancing trait value. High within accession (30.9%) and between accessions (69.1%) variability among 10 landraces of Indian origin, selected from the pearl millet landrace core collection (504 accessions).

467 accessions including 46 wild species and 25 SSRs

39 landraces þ 12 controls; AFLP markers

Pattern of population structure and diversity

Accessions and markers

Table 5.22 (Continued)

Hu et al. 2009

Bhattacharjee et al. 2002

Budak et al. 2003

vom Brocke et al. 2003

Mariac et al. 2006a

Reference

327

3 species and AFLP markers

59 cultivated, wild types and RAPD markers

Tef 92 lines and 8 ISSR markers

Cultivated/wild and weedy types (12) and AFLP markers

38 accessions and 3 intron splice junction (ISJ) primers

UPGMA resulted formation of 6 major clusters of 2 to 37 lines with further 8 lines remained ungrouped, and all the improved cultivars grouped in cluster 1. High polymorphism among wild relatives but low polymorphism among cultivated accessions. The RAPD primers differentiated E. pillosa from E. curvula, both wild relatives, with former more closely related to cultivated tef. AFLP analysis differentiated the species, E. tef, E. pilosa and E. curvula, from one another, with E. pilosa being the most diverse followed by E. curvula and E. tef; however, E pilosa more closely related with E. tef than E. curvula. Within tef germplasm, Rubicunda and DZ-01-1093 were distantly related to the rest of the tef accessions.

Geographical origin and glutinous vs. nonglutinous trait associated with the pattern of clustering of 38 accessions, with majority of the landraces forming 5 clusters while cultivars or breeding lines from Inner Mongolia 3 clusters. Cultivated and weedy biotypes formed 2 distinct clusters without any geographic association: a group formed only by weedy biotypes and another composed of domesticated and weedy biotypes displaying domesticated traits, while the typical wild types clustered separately. The most distinct biotypes were Colorado-Weld county black-seeded and Wyoming-Platte county type. Differences in aggressiveness and nutrient accumulation were also noticed: Canada-Rosemount biotype being more aggressive than Colorado biotype while Canada Rosemount and Colorado tan seeded biotypes showed differences in nutrient accumulation.

Ayele and Nguyen 2000

Bai et al. 2000

Assefa et al. 2003b

Karam et al. 2004

Hu et al. 2008

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exhibited greater within-population polymorphism, thus they form a potential reservoir of novel alleles for crop improvement (Ma et al. 2010). Pearl millet cultivars and landraces in Niger had a significantly lower number of microsatellite alleles and lower gene diversity than that of their wild relatives, with wild populations from western and central Niger showing introgression of cultivated alleles; thus the wild relatives provide an interesting source for new alleles and new allelic combinations to broaden the genetic base of cultivated pearl millet (Mariac et al. 2006a). RFLP and AFLP markers detect high within-accessions and between-accessions variability among pearl millet landraces from India (Bhattacharjee et al. 2002; vom Brocke et al. 2003) or substantial gene flow among pearl millet landrace populations due to frequent exchange of seed materials among farmers in western Rajasthan, India (vom Brocke et al. 2003). More recently, Yadav et al. (2010) used 24 SSRs distributed over seven pearl millet linkage groups to identify a ‘‘diversity panel’’ of 288 genotypes of four maturity groups from a composite collection of 2,000 diverse pearl millet breeding lines and accessions from Africa and Asia. This diversity panel of accessions represented the whole breadth of genetic variation in the pearl millet germplasm pool; the researchers are further studying it to identify gene-based markers tightly linked to the drought-tolerant QTL on LG2. In order to elucidate the relationship between foxtail millet and its wild ancestor green foxtail, d’Ennequin (2000) used AFLP markers. They indicated that both foxtail millet and green foxtail accessions originating in China were much more diverse than those from eastern Europe and Africa. Their results provide evidence that China is the center of foxtail millet domestication. More recently, with the development of microsatellites, the population structure of foxtail millet germplasm collections has been further detailed. For example, Jia et al. (2009a) reported close relationships among newly released cultivars except those from Shanxi Province in China, while Zhu et al. (2010) classified 120 landraces into four clusters coincident with their geographical origin: Northwest Inland group, Loess Plateau and Inner Mongolia group, North China Plain Landrace group, and North China Plain Cultivar group. Furthermore, Li et al. (2011) used ISSRs to demonstrate that foxtail millet landraces from China are not only highly diverse but also that they, along with landraces from Europe, are closely related with a group of green foxtail millet accessions originating in the central and western region of the Yellow River basin in China, where substantial archaeological evidence for ancient cultivation has been recovered (Lee et al. 2007). Wang et al. (2010) used nine genomic DNA fragment sequences to study relationships among 50 foxtail millet and 34 green

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foxtail millet accessions collected worldwide and found a relatively low level of genetic diversity in wild green foxtail millet (q ¼ 0.0059). They further reported that despite 55% loss of diversity as compared to green foxtail millet, the cultivated foxtail millet (S. italica) germplasm still harbors considerable diversity (q ¼ 0.0027) comparable to that reported in rice (q ¼ 0.0024) and sorghum (q0.0034). Wang et al. (2010) also observed linkage disequilibrium extending to 1 kb in foxtail millet, while it decayed rapidly to a negligible level at 150bp in the wild green millet. C. Promoting Use of Male Sterility as an Aid in Crossing Most of the millet crops, except for pearl millet, are self-pollinated, and all possess small flowers that are difficult to emasculate for crossing and hybrid seed production (Siles et al. 2001). In the case of pearl millet, protogyny can be exploited for manual crossing without emasculation, small-scale seed production of experimental hybrids, or production of chance hybrids. Male sterility thus becomes an important genetic tool to facilitate crossing and to facilitate production of sufficient hybrid seed to permit exploitation of hybrid vigor. Although male sterility is a common phenomenon in the plant kingdom (Kaul 1988), so far among millets, it is routinely used to produce seed of hybrid cultivars in only pearl millet and to some extent experimented in foxtail millet and finger millet. The CMS in pearl millet has been widely exploited for grain-producing hybrids in India and for forage (and to a lesser extent grain) hybrid production in the United States. Several sources of male-sterility-inducing cytoplasms—for example, A1 (Burton 1965), A2 and A3 (Burton and Athwal 1967), Av (Marchais and Tostain 1985), A4 (Hanna 1989), Ex-bornu ¼ Ag (Aken’ova 1985), A5 (Rai et al. 1998c), and Aegp (Delorme et al. 1997)—have been identified in pearl millet. Most of the pearl millet hybrids in India are based on the A1 CMS source, which has been clearly shown as not increasing the vulnerability of these hybrids to downy mildew (Yadav 1996b; Rai et al. 1998a,b), despite earlier concerns that this might be the case. Further studies have shown that A4, once a commercially unexploited CMS source, is not associated with downy mildew susceptibility and can safely be used as an alternative to the A1 cytoplasm (Yadav 1996a). Unfortunately, the A2, A3, and Ag CMS systems do not reliably maintain male sterility in seed production environments, so they cannot be exploited for commercial hybrid seed production. CMS is a maternally inherited phenotype characterized by an ability to produce sterile pollen, while female fertility and vegetative

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development are unaffected. Cytological observation indicates that pollen mother cell/microspore/pollen degeneration in A-lines occurred at different stages of anther development in pearl millet CMS lines. Each cytoplasm had its unique influence on microsporogenesis and anther development, as evidenced by different developmental pathways leading to pollen abortion. The cause of pollen abortion differed from line to line, from floret to floret within a spikelet, from anther to anther within a floret, and in some cases even from locule to locule within an anther. This could be one of the reasons for greater instability of male sterility in the A2 and A3 systems and greater stability of male sterility in the A1 and A4 systems (Chhabra et al. 1997). More recently, Rai et al. (2009) compared stability of male sterility among A1, A4, and A5 CMS lines, which revealed that the A5 CMS source is the most stable, followed by A4 and A1. Hybrids based on A1 and A5 CMS sources had no significant difference in grain yield, which implies that seed parents’ breeding efficiency will be the greatest with the A5 CMS system. The previous work also revealed that grain yield of hybrids based on A2, A3, and A4 cytoplasms was either similar to or significantly higher than that of their counterpart hybrids with A1 cytoplasm (Yadav 1996b). Hybrids based on A3 and A4 cytoplasms produced, on average, 8% more grain compared with those based on A1 cytoplasm. These studies indicate that the A4 and A5 CMS sources can be used as alternatives to A1 cytoplasm to widen the cytoplasmic base (and thereby the nuclear genetic base) of pearl millet hybrids. The CMS phenotype is associated with mutations in the mitochondrial genome (Hanson 1991) and rearranged mitochondrial genes are frequently co-transcribed with standard mitochondrial genes (Dewey et al. 1986; Laver et al. 1991; Bonhomme et al. 1992). Delorme et al. (1997) characterized cytoplasmic diversity, using mitochondrial gene-specific DNA probes in combination with eight restriction endonucleases, among five pearl millet isonuclear CMS lines as compared to the isonuclear fertile cytoplasm; their study revealed that five CMS cytoplasms (81A1, 81Av, 81A4, 81Aegp, and 81A5) can be distinguished from each other and from the isonuclear fertile cytoplasm (81B). Further, based on cox1, cox3, apt6, and apt9 polymorphisms, these lines can be classified into two major groups: one corresponds to A5, Aegp, Av and A1 cytoplasms, and the other consists of the A4 cytoplasm. The rearrangement involving the cox1 gene might be related to CMS in the former group, whereas rearrangement within the atp6/cox3 cluster region might be related to CMS in the latter group. ChandraShekara et al. (2005) used mitochondrial DNA polymorphism to differentiate A1, A2, and A3 CMS lines from A4 and A5 CMS lines. Spontaneous fertility reversion in the

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CMS A1 line of pearl millet occurs rarely (0.01% frequency), observed as a single pollen-shedding panicle surrounded by fully male-sterile panicles in a CMS plant (Smith et al. 1987). More recently, Feng et al. (2009) compared mitochondrial genome configurations between the male-sterile A1 line and the fertile revertants to demonstrate that this low frequency might be controlled by the substoichiometric nature of junction molecule CoxI-3-2, which appears to be essential to initiate the reversion phenomenon. Genetic male sterility in foxtail millet is controlled either by single recessive or dominant genes (Cui et al. 1979; Hu et al. 1986, 1993; Diao et al. 1991) and used to develop hybrid cultivars, such as ‘Suanxi 28Zhangnong 10’ and ‘Jigu 16’ (Cui et al. 1979; Du and Wang 1997). Herbicide resistance in foxtail millet (Darmency and Pernes 1985), which is dominant in nature (Wang and Darmency 1997), has been used to identify true hybrids while pseudo- (false) hybrids could be easily removed by spraying herbicide. Using this system, a few foxtail millet hybrid cultivars (F1), such as ‘Zhangzagu 8’ and ‘Zhangzagu 10’, were bred that showed grain yield up to 9 t ha1 in China (Diao and Cheng 2008). Researchers in China have used both physical and chemical mutagens as well as wide hybridization to discover a CMS system in foxtail millet (Hu et al. 1986; Zhou et al. 1988; Luo et al. 1993; Zhu and Wu 1997; Wu and Bai 2000). However, to date, no successful CMS line has been developed for commercial exploitation of hybrid vigor in foxtail millet. More recently, Zhi et al. (2007) reported a CMS material in a cross involving green foxtail and foxtail millet; the hybrid and BC1 plants were all male sterile. Further work is in progress to perfect this CMS system for the exploitation of hybrid vigor in foxtail millet. Heterosis for grain yield up to 68% has been reported, which reveals that heterozygosity could provide a significant yield benefit over nonhybrid cultivars in foxtail millet (Siles et al. 2004). Gupta (1999) developed a genetic male-sterile line, INFM 95001 (PI 595204), from the finger millet germplasm line IE 3318, using ethyl methanesulfonate. Genetic study involving INFM 95001 with its sister male-fertile line (IE 3318) and three unrelated male-fertile lines (FMV 1, FM 2, and SDFM 957) revealed that male sterility in INFM 95001 is controlled by a major recessive gene (Gupta 1999). Exploitation of the male-sterility gene present in INFM 95001 would facilitate crossing for the production of finger millet hybrid progenies to generate new segregants, to enhance genetic recombination in recurrent selection programs, and to facilitate exploitation of background selection in marker-assisted backcrossing programs.

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So far male-sterility systems in other millets have not been reported. Clearly, more research is needed to discover a CMS-based system because of the problems associated with the use of nuclear gene-based male sterility systems in hybrid seed production. However, genetic male-sterility systems still would be useful as breeding tools to facilitate production of segregating populations derived from controlled crosses, particularly in small-flowered self-pollinated species such as most millets, where it is otherwise difficult to produce large numbers of seeds from crosses required for efficient recurrent selection or backcrossing programs.

VIII. FROM TRAIT GENETICS TO ASSOCIATION MAPPING TO CULTIVAR DEVELOPMENT USING GENOMICS A. Markers/QTL Associated with Agronomic Traits, Abiotic Stress Tolerance, Biotic Stress Resistance, and Product Quality Pearl millet, finger millet, foxtail millet., and tef have sufficient genetic and genomic resources (see Section VI.A) to identify QTL associated with beneficial traits. Of these, pearl millet has been extensively investigated to identify QTL associated with agronomic traits, including resistance to biotic (Jones et al. 1995, 2002; Morgan et al. 1998; Hash and Witcombe 2001; Breese et al. 2002; Gulia et al. 2007a) and abiotic stresses (Yadav et al. 2002, 2004a; Bidinger et al. 2005, 2007; Sharma et al. 2010) as well as the association of QTL for flowering time with genotype  environment interaction of grain and stover yield in favorable production environments (Yadav et al. 2003a). More recently, Kholova et al. (2009) investigated whether the control of water loss under nonlimiting conditions is involved in terminal drought tolerance in pearl millet. Using test crosses of drought-tolerant and sensitive inbred lines together with QTL–near-isogenic line (NIL) introgression lines containing a terminal drought-tolerance QTL, they demonstrated that upon exposure to water deficit, transpiration began to decline at lower fraction of transpirable soil water in the tolerant than in the sensitive genotypes, while the transpiration rate (Tr) under well-watered conditions was lower in test crosses of the tolerant than in those of the sensitive parental genotypes. The fraction of transpirable soil water and Tr of the QTL near-isogenic line (QTL-NIL) test crosses followed patterns similar to their drought-tolerant parent. Further, Tr measured in detached leaves from the field-grown plants of the parental test crosses showed lower Tr values in test crosses of tolerant parents and the

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differences in Tr between genotypes were not related to the stomatal density, which further demonstrates that constitutive traits controlling leaf water loss under well-watered conditions correlate with expression of this terminal drought-tolerance QTL in pearl millet, which may lead to more water being available for grain filling under terminal drought conditions. Furthermore, Kholova et al. (2010) investigated whether this pearl millet terminal drought-tolerance QTL confers high leaf abscisic acid (ABA), limiting transpiration at high vapor pressure deficit (VPD), thus leading to transpiration efficiency differences. ABA levels under well-watered conditions were higher in drought tolerant testcross genotypes, including those of the QTL-NILs, than in test crosses of sensitive genotypes. ABA levels did not increase significantly under water stress in any of the test crosses, while well-watered Tr was lower in tolerant than in sensitive genotypes at all vapor pressure deficit (VPD) levels. This finding supports the hypothesis that water-saving (avoidance) mechanisms (i.e., a low Tr even at low VPD), which may relate to leaf ABA or sensitivity to higher VPD that further restricts Tr, may operate under well-watered conditions in drought-tolerant pearl millet. Both constitutive traits (higher leaf ABA levels and lower Tr), which did not lead to transpiration efficiency differences, could contribute to absolute water saving, which would become critical for grain filling under conditions of limited total water availability and deserve consideration in breeding for pearl millet genotypes tolerant to terminal drought stress when grown on soils capable of retaining water for use during grain filling. Interestingly, this same major drought-tolerant QTL from PRLT 2/89-33 also confers a positive effect under salinity stress by limiting Na þ accumulation in pearl millet leaves (Sharma et al. 2010). Variation in grain mineral contents (Fe and Zn) has been reported in pearl millet germplasm, improved cultivars, and elite hybrid parental lines (ICRISAT 2009). Genetic mapping using an existing RIL population recently identified five putative QTLs for grain Fe density and two for grain Zn density in this crop, with favorable alleles for grain densities of both minerals from 863B-P2 (high Fe and Zn) at a major QTL mapped on LG3, while LG6 alleles from ICMB 841-P3 (moderate Fe and Zn) were favorable for both minerals (Kumar et al. 2010). Ruminant nutritional value of pearl millet straw (i.e., stover quality) is a genetically complex trait (Hash et al. 2003). Marker-aided identification of genomic regions would facilitate identification of progenies with better stover quality. Bl€ ummel et al. (2003) reported sufficient genetic variation in cell wall digestibility and stover yield in pearl millet germplasm/parental lines. The stover quality on dry matter basis is determined by its gas volume (mL) produced after 24 h of in vitro digestion of dry matter (GAS24), in

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vivo organic matter digestibility, nitrogen content, metabolic energy content, and sugar content. Nepolean et al. (2006) identified two genomic regions on LG2 and LG6 associated with stover quality and three genomic regions on LG3, LG5, and LG6 associated with stover yield in a set of mapping population progeny test crosses. Further, the genomic region on LG2 also contains another major QTL associated with terminal drought tolerance (Yadav et al. 2004a) and thus is a good candidate region to improve terminal drought tolerance and better stover quality. More recently, the researchers at ICRISAT have validated a stover quality QTL in LG4, and found that this QTL cosegregates with dominantly inherited host plant resistance to the foliar disease blast caused by Pyricularia grisea. The donor parent for this stover quality/blast resistance QTL is 863B-P2. Further, an improved version of the previously released hybrid HHB 146 containing this QTL is now being tested by the All India Coordinated Pearl Millet Improvement Project (AICPMIP) for its adaptation in India (Nepolean et al. 2010). The domesticated foxtail millet (Setaria italica) has fewer branches than its wild progenitor (Setaria virdis), a phenomenon similar to maize (Zea mays) when it domesticated from its wild ancestor, teonsite (Doebley and Stec 1993). The basal branching (four QTL, one each on chromosomes I and V and two on chromosome III, together contributed 66%–73% phenotypic variation) and axillary branching (four QTL, one each on chromosomes VI and IX and two on chromosome V, together contributed 65%–99% phenotypic variation) is partially controlled by separate loci, and the orthologue of teosinte branched1, the major gene controlling branching phenotype in maize, has only a minor and variable effect. Other candidate genes for control of branching were a number of hormone biosynthesis pathway genes (Doust et al. 2004). They also detected that some of the variation in basal branching is controlled by loci separate from those controlling axillary branching, which is similar to what is reported in pearl millet (Poncet et al. 2000), a species more closely related to foxtail millet (Doust and Kellogg 2002) than either is to maize. Doust and Kellogg (2006) further found that branch number in F2:3 progenies of a cross between two species varies with genotype, planting density, and other environmental variables, with significant genotype  environment interactions, and the likely candidate genes underlying the QTL include teosinte branched1 and barren stalk1; however, much variation in branching is explained by QTL that do not have obvious candidate genes from maize or rice. QTL analysis in tef detected several genomic regions associated with yield and yield components, with majority of the QTL concentrated in 4 to 6 clusters on a few linkage groups, suggesting pleotropic effects of a

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few major genes (Chanyalew et al. 2005; Yu et al. 2007). Tef suffer from lodging that reduces grain yield and quality. Using F9-generation derived RIL from an interspecific cross (Eragrostis tef  E. pilosa), Zeid et al. (2010) mapped 83 QTL (phenotypic variation ranged from 4.8% to 33.0%) on 20 LGs for lodging, grain yield, and 15 other related traits. They detected two major clusters of QTL on LG6 and LG7, with LG7 harboring the largest number of QTL for eight traits. Furthermore, seven QTL for grain yield on five LGs together explained 64.7% variance. QTL for panicle length, panicle weight, and panicle seed weight were colocated with QTL for grain yield on LG7 and LG23. B. Marker-Aided Introgressions of Disease Resistance Downy mildew (DM) is one of the most important diseases of pearl millet, with diverse virulent pathogen populations reported from Africa and Asia (Singh et al. 1993). HHB 67 was a highly popular (<65 days from sowing to grain maturity) and widely grown (
500,000 ha) pearl millet hybrid in northwestern India following its release in 1989. However, like all popular single-cross hybrids before it, this hybrid became susceptible to DM (up to 30% incidence in farmers’ fields), with potential to cause substantial grain and stover yield losses to farmers in the state of Haryana. Resistance to DM is multigenic in nature and controlled by both major and minor QTL. All pearl millet DM-resistance QTL detected to date confer partial resistance that is pathogen-population specific, although in rare cases only a single major QTL of large effect can be detected in screens of a particular host mapping population against a particular pathogen isolate. Researchers at ICRISAT, in collaboration with partners from Haryana Agricultural University (which had bred and released the orginal HHB 67) and U.K.-based teams at the University of Wales used both marker-aided backcross and conventional backcross systems to incorporate additional DM resistance into the parental lines of HHB 67. Toward this end, they employed marker-assisted bacrkcross transfer of DM resistance (two major QTL) from donor parent ICMP 451 to male parent H 77/833-2 (Breese et al. 2002), while they used conventional backcross to transfer DM resistance in female parent 843A/B from the donor parent ICML 22. Using these improved parental sources, an improved version of HHB 67 was developed, tested, and released as ‘‘HHB 67 Improved.’’ Not only does it show substantially improved resistance to DM, but it also produced higher grain and stover yields (5%–10%) than the original hybrid HHB 67. After 3 years (2002–2004) of rigorous testing under AICPMIP, ‘‘HHB 67 Improved’’ was released in 2005 for cultivation in Haryana. It can be easily recognized from the

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original HHB 67 because of its long, thin panicles with short bristles. It was the first public sector–bred marker-assisted breeding product to be commercialized in India (Hash et al. 2006) and has been widely and rapidly adopted by the seed industry and pearl millet producers in that country. Furthermore, introgression lines containing downy mildew resistance QTL in other elite hybrid parent genetic backgrounds, such as J 2340, will soon be available for evaluation in India. C. Marker-Aided Introgressions to Enhance Drought Tolerance Pearl millet research at ICRISAT led to identification of a major QTL on LG2 associated with increased grain yield and harvest index under terminal drought stress in PRLT 2/89-33 (Yadav et al. 2002). The QTL marker-assisted selection–derived topcross hybrids moderately but significantly outyielded the field-based topcross hybrids under varying moisture stress conditions. However, this advantage under stress was at the cost of lower yield of the same hybrids under nonstressed environment. The hybrids flowered earlier and had limited effective basal tillers, low biomass, and high harvest index, similar to that of PRLT 2/89-33 (Bidinger et al. 2005). More recently, Serraj et al. (2005) and Witcombe et al. (2008) reported results of marker-assisted backcrossing by ICRISAT and its U.K.- and India-based partners to produce a set of near-isogenic version of elite pollinator H 77/833-2 (drought sensitive but widely used source for producing hybrids in India, including HHB 67 referred to earlier) with and without the LG2 drought-tolerance QTL from the donor parent PRLT 2/89-33. Field screening in carefully managed field environments revealed that hybrids produced on QTL introgression lines with the QTL yielded up to 21% more grain under postflowering drought stress conditions with no adverse effect on grain yield under nonstressed conditions. Furthermore, several of these introgression lines had a significant positive general combining ability for grain yield under terminal stress due to high panicle harvest index. Thus, these markerassisted breeding products have greater value for both water-limited and assured moisture conditions than either parental line. More recently, it has been shown that the drought-tolerance QTL contributed by PRLT 2/ 89-33 exerted favorable effects on growth and productivity traits under salt stress by limiting Na þ accumulation in leaves (Sharma et al. 2010) and that the mechanism of this terminal drought-tolerance QTL appears to be constitutively higher leaf ABA levels that reduce transpiration rate, altering the dynamics of crop water use so that there is still moisture left deep in the soil profile to support grain filling, at least under the managed terminal drought stress conditions in which this QTL was originally

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detected (Kholova et al. 2009, 2010). Thus, breeding line PRLT2/89-33 and its backcross derivatives provide important genetic resources for improving drought and salinity tolerance in pearl millet. Testing of products of the pyramiding of LG2 terminal droughttolerance QTL from PRLT 2/89-33 with two downy mildew resistance QTL (on LG1 and LG2) from donor parent ICMP 451-P6 in the genetic background of elite pollinator H 77/833-2 (male parent of released pearl millet hybrids HHB 60, HHB 67, and HHB 68) has recently been initiated (C. T. Hash, pers. commun.). D. Use of Rice, Maize, Sorghum, and Foxtail Millet Genome Sequences to Strengthen Molecular Breeding Tools In the last 25 years, most of the genomic and molecular breeding research of cereals concentrated on major crops such as maize, rice, sorghum, and wheat because of their significance in world food production. Similar genomic research on millets has been very limited during the same period. Therefore, availability of genomic resources is very limited in the millets except for pearl millet, finger millet, foxtail millet, and tef. In recent years, genomic research has intensified in these millets due to their potential in sustainable farming in the era of climate change and global warming. Nevertheless, comparative genomics have great potential to speed up development of genomic tools in these millets to support molecular breeding using genome sequences of rice, maize, sorghum, and foxtail millet. The earliest evidence of conservation of map position and order of DNA markers between chromosomal regions across different genomes in plants were reported between tomato and potato (Bonierbale et al. 1988). Soon after, comparative studies in grasses revealed a high degree of synteny of many DNA markers between chromosomal regions of different grass genomes, which had differences of 60 million years in evolutionary divergence times and up to 40-fold variation in genome sizes (Devos and Gale 1997; Gale and Devos 1998; Keller and Feuillet 2000). As a result, a series of early studies on genomic comparisons between members of grass family (Poaceae) were reported between rice and maize (Ahn and Tanksley 1993); rice and wheat (Kurata et al. 1994); rice, maize, wheat, and oat (Van Deynze et al. 1995); foxtail millet and rice (Devos et al. 1998); foxtail millet and maize (Doust et al. 20004); and pearl millet, rice, and foxtail millet (Devos et al. 2000). The comparative genomics approach was successful for map-based prediction of genes underlying the QTL that determine key traits for genetic improvement of the crops (Paterson et al. 1995; Doust and Kellogg 2006). Moore et al. (1995)

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published the first comparative genome map of seven different grass species using rice as reference map; their map subsequently was further refined (Gale and Devos 1998; Devos and Gale 2000). Although divergence of rice from other grass species occurred about 60 to 80 million years ago, fewer than 30 rice linkage blocks would be enough to represent all these genomes (Moore et al. 1997). Comparative mapping in grasses has resulted in the most comprehensive data set of comparative genomics in a plant family to date. Genome conservation is not limited only to a large region of chromosome, which is called macrocolinearity. Similar conservation was also observed at DNA sequence level (called microcolinearity) within orthologous regions in different members of the grass family. Ramakrishna et al. (2002) reported one such microcolinearity of orthologous regions in barley, rice, sorghum, and wheat based on bacterial artificial chromosome sequence analysis. However, within microcolinear regions, different types of sequence rearrangements (small inversions, gene duplications, deletions, and translocations) occurred during grass genome evolution (Paterson et al. 2010). For example, comparative analysis of finger millet and rice genomes reveals that six of the nine finger millet homologous groups correspond to a single rice chromosome each, while each of the remaining three finger millet groups are orthologous to two rice chromosomes, and in all three cases one rice chromosome was inserted into the centromeric region of a second rice chromosome to give the finger millet chromosomal configuration. Gene orders between rice and finger millet were highly conserved, with rearrangements being limited to single marker transpositions and small putative inversions encompassing at most three markers (Srinivasachary et al. 2007). Although these regions will appear as collinear at the genetic map level, some microrearrangements, such as deletions and translocations, can greatly complicate genome analysis at small regions. Although collinearity at the map level can be used in taxonomy and as a predictive tool, comparative map-based gene isolation requires highly conserved gene orders at the 100-kb to 1-Mb level (Devos and Gale 2000). Thus, the use of rice, maize, sorghum, finger millet, and foxtail millet for the map-based isolation of genes from other millet genomes often may be complicated by such local genome rearrangements. Consequently, approaches based on collinearity between grass genomes must also be performed using more closely related species (e.g., within tribes or subtribes). Finger millet is an excellent source of seed calcium (376–515 mg per 100 g), with a level far above that of the other cereals and millets (Barbeau and Hilu 1993). More recently, Nath et al. (2010) cloned the CaM gene, a calcium sensor, of finger millet along with other cereals (barley, maize,

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oat, rice, and sorghum) and millets (barnyard millet, kodo millet, little millet, and proso millet) to identify the structural similarity of CaM genes with their possible role in calcium signaling and calcium accumulation in cereals. The CaM sequences among these crops ranges from 579 to 623 bp, which could be due to amplification of variable length of the genomic sequence by same CaM specific primer. Multiple sequence alignment reveals a high degree of sequence conservation, although the authors detected some alterations that might be partially due to CaM sequence variation, 579 to 623 bp in cereals and millets. The in silico three-dimensional structural analysis of cloned sequences showed similar structures and reveals a high degree of conserved CaM in cereals and millets, with finger millet and barley CaM having closed evolutionary relationships as compared to others. The small millets and other major cereals (rice, wheat, barley, oat, corn, and sorghum) belong to the same family, Poaceae, but to different subfamilies (see Section I). Phylogentic relationship among cereals and millets based on chloroplast and nuclear genes showed close relationships (Giussani et al. 2001; Doust 2007; Paterson et al. 2009a; also see Section IV), and the subfamily Panicoideae includes two small groups of millets: Pearl millet, foxtail millet, proso millet, and little millet belong to one group, while maize, sorghum, sugarcane and Job’s tears belong to the other group. Members within the group are more similar than across the group. The subfamily Chloridoideae includes finger millet and tef (Doust 2007). Rice, however, belongs to the subfamily Ehrhartoideae, and phylogenetically it is located far from maize, sorghum, sugarcane, and other millets (Doust 2007). Determination of the phylogentic relationship between millets and other cereals will be helpful to identify the grass cereal species closest to the target millet for comparative genomics studies. Availability of genome sequences of foxtail millet (Doust et al. 2009) will be extremely valuable for genome mapping, marker development, and molecular breeding of pearl millet, proso millet, and little millet because of their taxonomic closeness (Doust 2007), as will genome sequence availability of corn and sorghum will be equally useful for genome analysis of sugarcane and Job’s tears. Finger millet and tef genome analysis will also be aided by genome sequences of these cereals of Panicoideae. Even in the absence of local microcolinearity, the overall good collinearity observed between the grass genomes still offers the possibility of increasing the number of markers in a targeted region using RFLP and EST probes without the need to develop additional markers from the species of interest. Molecular markers derived from orthologous regions

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in different grass species can be used to increase the map density at specific genetic loci and facilitate map-based cloning of genes in millets (Kilian et al. 1997). Comparative genomics studies of millets using available grass sequences can help in understanding the molecular mechanisms of genome evolution in the grasses, which is necessary to define the best strategies and the tools necessary to isolate genes of agronomic importance from large and complex cereal genomes. Comparative genomics and genome sequence database of rice (Goff et al. (2002), maize (Schnable et al. 2009), sorghum (Paterson et al. 2009b), and foxtail millet (Doust et al. 2009; Mitros et al. 2010) can be used to align EST and other DNA markers of millets. Millets markers can be mapped on the linkage groups of these species, then located on the millets linkage group by comparative genetics mapping among rice, maize, sorghum, or foxtail millet and the genome of other millets. The aligned EST information should available for further study on genomics and gene cloning. Such approaches have already been used successfully to saturate different genomic regions of sugarcane, barley, and wheat (Kilian et al. 1997; Roberts et al. 1999; Asnaghi et al. 2000; Druka et al. 2000). In sorghum, EST-SSR were developed based on ricesorghum syntenies to enrich the sorghum genetic linkage map (Ramu et al. 2009). Microsatellite markers from subtracted drought stresses EST were also developed in sorghum (Srinivas et al. 2009). In maize, 364,385 ESTs and 27,455 full-length complementary deoxyribonucleic acids (FLcDNAs) are in a database (Soderlund et al. 2009). A new type of DNA marker, single-strand conformational polymorphism (SSCP)-SNP, has been developed in pearl millet using annotated rice genomic sequences to initially predict the intron-exon borders in millet ESTs and then to design primers that would amplify across the introns (Bertin et al. 2005). ESTs-SSRs in pearl millet were developed based on comparative genomics using the rice genome sequence (Senthilvel et al. 2008). Using the rice genome sequence as base, a comparative genomics approach was applied to develop new types of DNA markers, conserved intron scanning primers (CISPs), and tested across several grasses (rice, sorghum, pearl millet, and tef) (Feltus et al. 2006). A similar approach can be used to develop such markers in other millets using available genome sequences of sorghum, maize, and foxtail millet. The current genetic linkage maps and available RFLP, AFLP, EST, and SSR markers in finger millet and tef can be aligned to the foxtail millet genome sequence for development of more markers to saturate the genome (Yu et al. 2006a,b; Dida et al. 2007). In finger millet, SSRs are being developed from the available 1740 ESTs, which will be useful in a comparative genomics study for developing more genomic tools

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(Arya et al. 2009). Although genome synteny among cereals is well established, the linking information between different genomes is still too sparse to accurately pinpoint candidate homologous genes except in the few cases where the similarities in phenotypes are obvious. Soon the grasses, including all of the major cereals and minor millets, will be able to be considered a single entity, and all of the information available on gene structure, gene action, metabolism, physiology, and phenotype accumulated over the past century in the different species will be pooled. An immediate practical implication is that breeders need no longer be restricted to their own species in their search for exploitable variation. Homologous genes and all of their alleles in all species will be available to the cereal breeder/genetic engineer of the early 21st century. E. Exploiting Variation at Waxy Locus to Diversify Food Uses Endosperm starch of cereals consists of amylose and amylopectin. Wild type (nonwaxy) endosperm starch consists of 20% or more of amylose and 80% of amylopectin whereas waxy type consists of 100% amylopectin and lacks amylose. Nonwaxy (Wx) phenotype is dominant over waxy phenotype (wx). Endosperm starch of the waxy type has a stickier texture than that of the non-waxy type. Both types of endosperm have been reported among the landraces of sorghum, rice, foxtail millet, maize, common millet, barley, and Job’s tears (Sakamoto 1996). The waxy types of these cereals are found in east and southeast Asia but are rare in India and farther westward. A core area where people show a strong ethnobotanical preference for waxy cereals, which extends from southern China through northern Thailand to Assam, has been identified (Sakamoto 1996; Yoshida 2002). In adjacent countries such as Taiwan, Japan, and Korea, waxy cereals are grown mainly on upland soils and are used in traditional rituals or eaten only on special occasions. This trait is apparently associated with ethnological preferences in the region (Fogg 1983; Takei 1994). Waxy endosperm arises through the disrupted expression or loss of function of the waxy (GBSS 1) gene that encodes granule-bound starch synthase I (GBSS I) (Sano 1984). Waxy-type cereals are characterized by little or no starch amylose, which constitutes about 20% or more of the total starch in the nonwaxy endosperm. This character has often been neglected in other regions, although waxy maize, which was first reported (Collins 1909) in Chinese landraces, is now globally used for the production of waxy corn starch. Molecular basis of naturally occurring wx mutants in foxtail millet has been well characterized. The waxy foxtail millet probably evolved from

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the nonwaxy type after domestication, since the wild ancestor (S. italica ssp. viridis) has a nonwaxy endosperm (Nakayama et al. 1998). In addition to those two types, an intermediate or low-amylose type foxtail millet germplasm has also been reported (Sakamoto 1987). Amylose content is positively correlated with amounts of GBSS 1 protein among the three phenotypes (Afzal et al. 1996) and is genetically controlled by waxy (GBSS 1) alleles (Nakayama et al. 1998). No other genes that regulate amylose content, such as du in rice (Okuno et al. 1983), are known in foxtail millet. Fukunaga et al. (2002a) determined the sequence of the full-length cDNA and the genomic structure of the waxy (GBSS 1) gene, which revealed multiple origins of the waxy endosperm in foxtail millet. Kawase et al. (2005) classified 841 landraces of foxtail millet into 11 groups based on PCR analysis of the gene to conclude that waxy foxtail millet originated four times independently and low-amylose foxtail millet three times by insertions of transposable elements. More recently, Van et al. (2008) reported several SNPs and small indels in waxy gene in foxtail millet. The waxy phenotype has also been reported in proso millet germplasm from east Asia, with complex inheritance due to the tetraploid nature of this species (Sakamoto 1996; Graybosch and Baltensperger 2009). The waxy trait is being introduced into locally adapted proso millet cultivars in the central Great Plains of the United States (Heyduck et al. 2008). Further, molecular basis of waxy endosperm phenotype in this species revealed 15-bp deletion in one of the waxy loci and the insertion of an adenine residue, which causes a reading frame shift or a point mutation causing a cysteine/tyrosine amino acid polymorphism in other loci (Hunt et al. 2010). Nearly all the cultivated Job’s tears cultivars have waxy phenotype, while the waxy trait has not been reported in its wild relatives (Okuyama et al. 1989). Molecular characterization of the gene is under way, and mutation conferring waxy phenotype may be due to partial deletion of the gene (T. Hachiken and K. Fukunaga, Prefectural University of Hiroshima, Japan, pers. commun.). There are no waxy landraces in Japanese barnyard millet due to the allohexaploid nature of this crop (Yabuno 1987), which requires mutations in three different waxy loci to permit expression of the waxy phenotype. However, several Japanese landraces with approximately half the level of amylose have been reported. Hoshino et al. (2010) used a low-amylose landrace (Noge-Hie) and g-ray radiation to produce a waxy Japanese barnyard millet cultivar (‘Chojuro-mochi’), with its waxy phenotype originating from the partial deletion of waxy genes. Grain of this genotype may be used for making cookies and other foods in Japan.

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The waxy phenotype has not been reported in pearl millet, finger millet, tef, kodo, or fonio (Sakamoto 1996). However, it is possible to develop waxy cultivars in these species through mutations by mutagens such as ethyl methanesulfonate, g-ray, or ion beam, or by transgenic events. Thus, the waxy cultivars of such cereals will be new sticky food sources for human consumption. F. Foxtail Millet, Sorghum and Maize Genome Sequences as Resources for Identifying Variation Associated with High Biomass Production in Bioenergy Grasses Some of the photosynthetic-efficient C4 bioenergy crops include sugarcane, maize, sorghum, foxtail millet, pearl millet, switchgrass, and napiergrass (Perlack et al. 2005; Ragauskas et al. 2006; Carpita and McCann 2008; Doust et al. 2009). These species differ in genome size (1C) [foxtail millet: 490 Mb; sorghum: 730 Mb; pearl millet: 2,352 Mb; maize: 2,605–2,798 Mb; switchgrass (1,372–1,666 Mb in 4, 1,960–2,058 Mb in 6, 2,352–3,136 Mb in 8); napiergrass: 2254 Mb (Bennett and Leitch 1995; Bennett et al. 2000; Doust et al. 2009; Paterson et al. 2009b)], ploidy levels (diploid: foxtail millet, pearl millet, and sorghum; tetraploid: napiergrass; tetraploid, hexaploid, octaploid: switchgrass), breeding systems (inbreeder: foxtail millet; outbreeder: maize, pearl millet, switchgrass, and napiergrass; mixed mating: sorghum) and life-forms (annual: foxtail millet, maize, pearl millet, and sorghum; perennial: napiergrass and switchgrass). Many forms of feedstocks, including maize, rice, sorghum, wheat, barley, and oat, are available for biofuel production. Cereal grains are high in starch content and therefore good feedstock for conversion to biofuels and other bio-based products, with ethanol being commercially produced from these feedstocks in the United States and elsewhere. Among the millet species, pearl millet grain has also been explored for production of ethanol in the United States. The grains contain about 70% starch, which gives it a theoretical ethanol yield of 0.43 L kg1, comparable to barley and oat but inferior to maize, rice, sorghum, and wheat grains (0.52–0.57 L kg1) (http://www.mhprofessional.com/downloads/ products/0011487492/DrapchoCh4.pdf). Furthermore, the fermentation efficiencies of pearl millets, on the basis of starch, are comparable to those of maize and sorghum grains (Wu et al. 2006). Pearl millet therefore could be a potential feedstock for fuel production in areas too dry or too hot to grow maize and sorghum. The genomic relationships among cereals have been established (Gale and Devos 1998). The high degree of genetic synteny among grass

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genomes should facilitate the translation of gene-function discovery in bioenergy model crops (maize and sorghum) (Carpita and McCann 2008; Doust et al. 2009), which have abundant genetic and genomic resources (reviewed in Dwivedi et al. 2007) and their genomes have been recently sequenced (Paterson et al. 2009b; Schnable et al. 2009). Foxtail millet has been recently identified as an experimental model crop to investigate many aspects of plant architecture, genome evolution, and physiology in the bioenergy grasses (Doust et al. 2009). More recently, significant progress has been announced toward sequencing the foxtail millet genome, which is closely related to bioenergy grasses (Doust et al. 2010; Mitros et al. 2010). With the release of maize, sorghum, and foxtail millet genome sequences and the availability of next-generation sequencing technologies (Varshney et al. 2009), genomic and genetic approaches can be explored to study the molecular basis of biomass production, cell wall modification using brown midrib mutants (bm in maize or bmr in sorghum, which alter the cell wall composition, particularly lignin subunit composition) (reviewed in Vermerris et al. 2007), or accumulation of sugar in sweet sorghums and its relationship with grain and biomass production (Rao et al. 2009). Furthermore, sequence variation would also allow a comprehensive survey of genetic diversity to identify and conserve germplasm diversity with bioenergy traits.

IX. CONCLUSIONS AND FUTURE PROSPECTS Gene banks around the world have a large collection of germplasm for most of the millets species. However, more effort is needed to collect landraces of barnyard millet, fonio, tef, and Job’s tears before these priceless genetic resources vanish forever from their habitats. Access to genetic diversity contained in large germplasm collections continues to be a significant challenge. A reduced subset of germplasm in the form of a conventional core or genotype-based ‘‘diversity panel’’ is the ideal pool of diverse germplasm resources for studying population structure and diversity. Landrace diversity in pearl millet and fonio has been found to possess several agronomically beneficial traits. More efforts are therefore needed to collect and characterize landrace in other millets to identify potential germplasm resources for use in crop improvement programs. Precise phenotyping is the key to finding and introducing new genes for biotic and abiotic tolerances. An effective phenotypic screen for lodging and temperature tolerance is urgently needed in millets to identify lodging and high-temperature-tolerant germplasm resources

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for use in breeding. Downy mildew in pearl millet and blast in finger millet have shown large pathogen variability, with some pathotypes being more virulent than others. There is a continuing need to monitor pathogen variability and take effective measures to deploy cultivars with resistance to multiple pathotypes to contain these diseases in farmers’ fields. Among the millets, pearl millet is the only crop in which heterosis has been exploited using CMS-based hybrids for large-scale commercial cultivation in India, the American continent, and Oceania. In years to come, foxtail millet has great potential to exploit heterosis for total biomass and grain yield. Researchers in China have discovered CMS materials, which are being further studied to develop stable CMS seed parents and reliable fertility restorers for the development of hybrids in foxtail millet. As of now, eight angiosperm genomes, including maize, rice, and sorghum, have been sequenced (Paterson et al. 2010). The draft genome sequencing of foxtail millet (Setaria italica) has been completed to 8.3 coverage; it has shown a high degree of synteny to rice and sorghum, suggesting that foxtail millet genome sequences will soon be available to the research community (Mitros et al. 2010). By comparing the genome sequences of maize, rice, and sorghum with that of foxtail millet—all of which are used as food, feed, and biofuel crops—we should be able to find sequence variation across species and relate these differences to beneficial traits. Furthermore, it should be feasible to resequence the elite genetic stocks with contrasting phenotypes of a given crop species. Sequence variation among these genetic stocks could then be related to phenotypic differences, as detected in maize inbreds and hybrids (Lai et al. 2010). With the development of next-generation sequencing technologies, identification and tracking of genetic variations has become so efficient and precise that thousands of variants can be tracked within large populations at a much-reduced cost (Varshney et al. 2009). Moreover, the availability of DNA sequence information should enable the discovery of genes and molecular markers associated with diverse agronomic traits, creating new opportunities for crop improvement (Edwards and Batley 2010). Millets as a group are C4 plants, mostly adapted to marginal lands in the hot, drought-prone arid and semiarid regions of Africa, Asia, and the Americas. The gains in productivity associated with C4 photosynthesis include improved water and nitrogen use efficiencies. Engineering C4 traits into C3 grasses is an attractive target for crop improvement. However, the lack of a small, rapid-cycling genetic model system to study C4 photosynthesis has limited progress in dissecting the regulatory

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networks using the C4 pathway. Setaria virdis (genome size 510 Mb), the wild ancestor of foxtail millet (S. italica) and a close relative of several feed, fuel, and bioenergy grasses, uses the nicotinamide adenine dinucleotide phosphate (NADP)-malic enzyme subtype C4 photosynthetic system to fix carbon and is therefore a potential model system for dissecting C4 photosynthesis (Brutnell et al. 2010). The only major hurdle yet to overcome with S. virdis, however, is to develop an effective transformation and regeneration system. Some progress has already been reported toward regenerating plants from seed callus and establishing a transient transformation system in S. virdis. Engineering C4 traits into C3 plants will go a long way to sustain and stabilize food production, particularly in the developing world, in view of global warming due to climate change. PCR-based markers have been used to assess the structure of genetic diversity in some millets; such studies are needed in other species. Genetic maps of varying density are available for pearl millet, finger millet, foxtail millet, and tef and QTL associated with various agronomic traits have been reported for pearl millet, foxtail millet, and tef. Markeraided breeding is being practiced to incorporate biotic and abiotic stress resistance into the improved genetic background of pearl millet. Pearl millet hybrid with enhanced resistance to downy mildew is widely grown in India. Pearl millet introgression lines combining terminal drought-tolerant QTL (on LG2) and downy mildew–resistant QTL (on LG1 and LG4) are being tested for their agronomic performance in India. There is, however, urgent need to develop genomic resources (markers and genetic maps) for fonio and Job’s tears, two underresearched millets. Lodging is a serious problem in fonio and little positive variability has been identified for this trait in fonio germplasm evaluated so far. Tef-based TILLING has been perfected and is currently used to identify dwarf tef plants from mutagenetically ionized tef populations. Even though grain from millets is more nutritious than most major starch crop and has some medicinal value, production in traditional millets growing areas has been declining in favor of other crops, such as rice, wheat, and cassava. The decline in production has resulted in reduced consumption, which could also be related to changing lifestyle due to overall economic development. Government policies, in addition to erratic rainfall and drudgery associated with processing of minor millets, also contributed to the decline in production of these millets species. An all-front attempt is needed to bring production back to the levels these species were grown to and consumed during the 1960s and 1970s. Doing so includes increasing public awareness of the nutritional value of these millet species to overall human health; enhanced research

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on issues associated with production, processing, and utilization; value addition by developing new products; and government support for marketing and inclusion of millets to distribution through public systems so it reaches needy people. Collective action involving diverse players will be required to develop a promotional strategy for demand expansion to ensure that production of these millets is solidly anchored and sustained in the long run.

ACKNOWLEDGMENTS The authors thank H. C. Sharma of ICRISAT for his critical review of the manuscript; the staff of the ICRISAT library for their efforts in conducting literature searches and arranging for reprints; Jules Janick (editor, Plant Breeding Reviews); and the anonymous reviewers for making useful suggestions on improving the manuscript. Funding support from the BMZ/GTZ-supported project ‘‘Sustainable Conservation and Utilization of Genetic Resources of Two Underutilized Crops—Finger Millet and Foxtail Millet—to Enhance Productivity, Nutrition and Income in Africa and Asia’’ to Sangam Dwivedi is gratefully acknowledged. Sangam Dwivedi highly appreciates the support and encouragement from Dr. William D. Dar (director general, ICRISAT).

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e, and K. Akpagna. 2006. Indigenous knowledge and traditional conservation of fonio millet (Digitaria exils, D. iburua) in Togo. Biodiv. Conserv. 15:2379–2395. Adoukonou-Sagbadja, H., A. Dansi, R. Vodouh
e, and K. Akpagana. 2004. Collecting fonio (Digitaria exilis Kipp. Stapf, D. iburua Stapf) landraces in Togo. Plant Genet. Resour. Newslett. 139:59–63. Adoukonou-Sagbadja, H., V. Schuvert, A. Dansi, G. Jovtchev, A. Meister, K. Pistrick, K. Akpagana, and W. Friedt. 2007. Flow cytometric analysis reveals different nuclear DNA contents in cultivated fonio (Digitaria spp.) and some wild relatives from West Africa. Plant Syst. Evol. 267:163–176. Adugna, H., and R. Hofsvang. 2000. Survey of lepidopterous stem borer pests of sorghum, maize and pearl millet in Eritrea. Crop Prot. 20:151–157. Afzal, M., M. Kawase, H. Nakayama, and K. Okuno. 1996. Variation in electrophoregrams of total seed protein and Wx protein in foxtail millet. p. 191–195. In: J. Janick (ed.), Progress in new crops. ASHS Press, Alexandria, VA. Ahn, S.N., and S.D. Tanksley. 1993. Comparative linkage maps of the rice and maize genomes. Proc. Nat. Acad. Sci. (USA). 90:7980–7984.

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Subject Index

Biography, Margaret M. Jahn, 1–17 Brassica crops, domestication, evolution, history, 19–84 B. carinata, 57–65 B. juncea, 58–65 B. napus, 65–67 B. nigra, 38–41 B. oleracea, 41–51 B. rapa, 51–57 Breeding: melon, 85–150 millets, 247–374 vegetable crop transgenics, 151–246 Cucumismelo, See Melon Cytogenetics, Brassica, 25–36 Disease and pest resistance: melon, 86–150 millets, 247–374 Diversity: melon, 85–150 millets, 247–374 Genome, Brassica, 25–36 Genetics, millets, 247–374 Germplasm: melon, 85–150 millets, 247–374 Grain breeding, millets, 247–374 Jahn, Margaret M. (biography), 1–17 Marker assisted selection, millet, 332–344 Melon, landrace of India, 85–150

Millets, genetic and genomic resources, 247–374 Polyploid, Brassica, 34–36 Transformation and transgenesis: alliums, 210–213 brassicas, 19–84, 199–205 carrot, 219–220 cassava, 216 cowpea, 215 cucurbits, 196–199 eggplant, 187–191 lettuce, 205–210 potato, 191–196 sweet corn, 213–215 tomato, 164–187 sweet potato, 217–218 vegetable crops, 151–246 Vegetable breeding, 151–24 alliums, 210–213 brassicas, 199–205 carrot, 219–220 cassava, 216 cowpea, 215 cucurbits, 196–199 eggplant, 187–191 lettuce, 205–210 melon, 85–150 potato, 191–196 sweet corn, 213–215 tomato, 164–187 sweet potato, 217–218 vegetable crops, 151–246

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Cumulative Subject Index Volumes 1–35

A Adaptation: blueberry, rabbiteye, 5:351–352 durum wheat, 5:29–31 genetics, 3:21–167 raspberry, 32:53–54, 153–184 testing, 12:271–297 Aglaonema breeding, 23:267–269 Allelopathy, 30:231–258 Alexander, Denton, E. (biography), 22:1–7 Alfalfa: honeycomb breeding, 18:230–232 inbreeding, 13:209–233 in vitro culture, 2:229–234 somaclonal variation, 4:123–152 unreduced gametes, 3:277 Allard, Robert W. (biography), 12:1–17 Allium cepa, see Onion Alliums transgenics, 35:210–213 Almond: breeding self-compatible, 8:313–338 domestication, 25:290–291 transformation, 16:103 Alocasia breeding, 23:269 Alstroemaria, mutation breeding, 6:75 Amaranth: breeding, 19:227–285 cytoplasm, 23:191 genetic resources, 19:227–285 Animals, long term selection, 24(2):169–210, 211–234 Aneuploidy: alfalfa, 10:175–176

alfalfa tissue culture, 4:128–130 petunia, 1:19–21 wheat, 10:5–9 Anther culture: cereals, 15:141–186 maize, 11:199–224 Anthocyanin maize aleurone, 8:91–137 pigmentation, 25:89–114 Anthurium breeding, 23:269–271 Antifungal proteins, 14:39–88 Antimetabolite resistance, cell selection, 4:139–141, 159–160 Apomixis: breeding, 18:13–86 genetics, 18:13–86 reproductive barriers, 11:92–96 rice, 17:114–116 Apple: domestication, 25:286–289 fire blight resistance, 29:315–358 genetics, 9:333–366 rootstocks, 1:294–394 transformation, 16:101–102 Apricot: domestication, 25:291–292 transformation, 16:102 Arabidopsis, 32:114–123 Arachis, see Peanut Artichoke breeding, 12:253–269 Avena sativa, see Oat Avocado domestication, 25:307 Azalea, mutation breeding, 6:75–76

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380 B Bacillus thuringensis, 12:19–45 Bacteria, long-term selection, 24(2):225–265 Bacterial diseases: apple rootstocks, 1:362–365 cell selection, 4:163–164 cowpea, 15:238–239 fire blight, 29:315–358 maize, 27:156–159 potato, 19:113–122 raspberry, 6:281–282; 32:219–221 soybean, 1:209–212 sweet potato, 4:333–336 transformation fruit crops, 16:110 Banana: breeding, 2:135–155 domestication, 25:298–299 transformation, 16:105–106 Barley: anther culture, 15:141–186 breeding methods, 5:95–138 diversity, 21:234–235 doubled haploid breeding, 15:141–186 gametoclonal variation, 5:368–370 haploids in breeding, 3:219–252 molelcular markers, 21:181–220 photoperiodic response, 3:74, 89–92, 99 vernalization, 3:109 Bean (Phaseolus): breeding, 1:59–102; 10:199–269; 23:21–72 breeding mixtures, 4:245–272 breeding (tropics), 10:199–269 heat tolerance, 10:149 in vitro culture, 2:234–237 long-term selection, 24(2):69–74 photoperiodic response, 3:71–73, 86–92; 16:102–109 protein, 1:59–102 rhizobia interaction, 23:21–72 seed color genetics, 28:239–315 Beet (table) breeding, 22:357–388 Beta, see Beet Biochemical markers, 9:37–61 Biography: Alexander, Denton E., 22:1–7 Allard, Robert W., 12:1–17 Bliss, Frederick A., 27:1–14 Borlaug, Norman E., 28:1–37

CUMULATIVE SUBJECT INDEX Bringhurst, Royce S., 9:1–8 Burton, Glenn W., 3:1–19 Coyne, Dermot E., 23:1–19 Daubeny, H. A., 32:21–37 Downey, Richard K., 18:1–12 Draper, Arlen D., 13:1–10 Dudley, J.W., 24(1):1–10 Duvick, Donald N., 14:1–11 Frey, Kenneth, J. 34:1–36 Gabelman, Warren H., 6:1–9 Goodman, Major M., 33:1–29 Hallauer, Arnel R., 15:1–17 Harlan, Jack R., 8:1–17 Hymowitz, Theodore, 29:1–18 Jahn, Margaret, M., 35:1–17 Jennings, D., 32:2–21 Jones, Henry A., 1:1–10 Laughnan, John R. 19:1–14 Munger, Henry M., 4:1–8 Redei, George, P., 26:1–33 Peloquin, Stanley J., 25:1–19 Ryder, Edward J., 16:1–14 Salamini, Francesco, 30:1–47 Sears, Ernest Robert, 10:1–22 Simmonds, Norman W., 20:1–13 Sprague, George F., 2:1–11 Vogel, Orville A., 5:1–10 Vuylsteke, Dirk R., 21:1–25 Weinberger, John H., 11:1–10 Yuan, Longping, 17:1–13 Biotechnology: Cucurbitaceae, 27:213–244 Douglas-fir, 27:331–336 politics, 25:21–55 Rosaceae, 27:175–211 Birdsfoot trefoil, tissue culture, 2:228–229 Blackberry, 8:249–312, 29:19–144 mutation breeding, 6:79 Black walnut, 1:236–266 Bliss, Frederick A. (biography), 27:1–14 Blueberry: breeding, 5:307–357;13:1–10; 30:353–414 domestication, 25:304 highbush, 30:353–414 rabbiteye, 5:307–357 Borlaug, Norman, E. (biography), 28:1–37 Bramble. See also Blackberry; Raspberry domestication, 25:303–304 transformation, 16:105

CUMULATIVE SUBJECT INDEX Brachiaria, apomixis, 18:36–39, 49–51 Brassica. See also Cole crops carinata 35:57–65 cytogenetics, 31:21–187 domestication, 35:19–84 evolution, 31:21–87; 35:19–84 history, 35:19–84 juncea, 35:58–65 napus, 35:65–67. See also Canola, Rutabaga nigra, 35:38–41 oleracea, 35:41–45 rapa, 35:51–47. See also Canola transgenics: 35:199–205 Brassicaceae: incompatibility, 15:23–27 molecular mapping, 14:19–23 Breeding: Aglaonema, 23:267–269 alfalfa via tissue culture, 4:123–152 allelopathy, 30:231–258 alliums, 35:210–213 almond, 8:313–338 Alocasia, 23:269 amaranth, 19:227–285 apomixis, 18:13–86 apple, 9:333–366 apple fire blight resistance, 29:315–358 apple rootstocks, 1:294–394 banana, 2:135–155 barley, 3:219–252; 5:95–138; 26:125–169 bean, 1:59–102; 4:245–272; 23:21–7 beet (table), 22:357–388 biochemical markers, 9:37–61 blackberry, 8:249–312; 29:19–144 black walnut, 1:236–266 blueberry, 5:307–357; 30:353–414 brassicas, 35:19–84, 199–205 bromeliad, 23:275–276 cactus, 20:135–166 Calathea, 23:276 carbon isotope discrimination,12:81–113 carrot, 19:157–190, 35:219–220 cassava, 2:73–134; 31:247–275, 35:216 cell selection, 4:153–173 cereal stress resistance, 33:115–144 chestnut, 4:347–397; 33:305–339 chimeras, 15:43–84 chrysanthemum, 14:321–361 citrus, 8:339–374; 30:323–352

381 coffee, 2:157–193; 30:415–447 coleus, 3:343–360 competitive ability, 14:89–138 cowpea, 15:215–274, 35:215 cucumber, 6:323–359 Cucurbitaceae 27:213–244 cucurbits, 27:213–244; 35:196–199 currant, 29:145–175 cytoplasmic DNA, 12:175–210 diallel analysis, 9:9–36 Dieffenbachia, 23:271–272 doubled haploids, 15:141–186; 25:57–88 Dougas-fir, 27:245–253 Dracaena, 23:277 drought tolerance, maize, 25:173–253 durum wheat, 5:11–40 eggplant, 35:187–191 Epepremnum, 23:272–273 epigenetics, 30:49–177 epistasis, 21:27–92 exotic maize, 14:165–187 fern, 23:276 fescue, 3:313–342 Ficus, 23:276 fire blight resistance, 29:315–358 flower color, 25:89–114 foliage plant, 23:245–290 forest tree, 8:139–188 fruit crops, 25:255–320 garlic, 6:81; 23:11–214 gene action 15:315–374 genotype  environment interaction, 16:135–178 gooseberry, 29:145–175 grain legumes, 33:157–304 grapefruit, 13:345–363 grasses, 11:251–274 guayule, 6:93–165 heat tolerance, 10:124–168 Hedera, 23:279–280 herbicide-resistant crops, 11:155–198 heritability, 22:9–111 heterosis, 12:227–251 homeotic floral mutants, 9:63–99 honeycomb, 13:87–139; 18:177–249 human nutrition, 31:325–392 hybrid, 17:225–257 hybrid wheat, 2:303–319; 3:169–191 induced mutations, 2:13–72

382 Breeding (Continued ) insect and mite resistance in cucurbits, 10:199–269 isozymes, 6:11–54 legumes, 26:171–357; 33:157–304 lettuce, 16:1–14; 20:105–133; 35:205–210 maize, 1:103–138, 139–161; 4:81–122; 9:181–216; 11:199–224; 14:139–163, 165–187, 189–236; 25:173–253; 27:119–173; 28:59–100; 31:223–245; 33:9–16; 34:37–182, 83–113, 131–160 marker-assisted selection, 33:145–217, 219–256; 34:247–358 meiotic mutants, 28:163–214 melon, 35:85–150 millets, 35:247–374 mitochondrial genetics, 25:115–238 molecular markers, 9:37–61, 10:184–190; 12:195–226; 13:11–86; 14:13–37, 17:113–114, 179, 212–215; 18:20–42; 19:31–68, 21:181–220, 23:73–174; 24(1):293–309; 26:292–299; 31:210–212, 33:145–217, 219–256; 34:247–348; 35:332–344 mosaics, 15:43–84 mushroom, 8:189–215 negatively associated traits, 13:141–177 oat, 6:167–207 oil palm, 4:175–201; 22:165–219 onion, 20:67–103; 35:210–213 ornamental transgenesis, 28:125–216 palms, 23:280–281 papaya, 26:35–78 pasture legumes, 5:237–305 pea, snap, 212:93–138 peanut, 22:297–356; 30:295–322 pear fire blight resistance, 29:315–358 pearl millet, 1:162–182 perennial rye, 13:265–292 persimmon, 19:191–225 Philodendron, 23:2 phosphate efficiency, 29:394–398 plantain, 2:150–151; 14:267–320; 21:211–25 potato, 3:274–277; 9:217–332; 16:15–86; 19:59–155, 25:1–19; 35:191–196 proteins in maize, 9:181–216

CUMULATIVE SUBJECT INDEX quality protein maize (QPM), 9:181–216 raspberry, 6:245–321; 32:1–37, 39–53 recurrent restricted phenotypic selection, 9:101–113 recurrent selection in maize, 9:115–179; 14:139–163 rice, 17:15–156; 23:73–174 rol genes, 26:79–103 Rosaceae, 27:175–211 rose, 17:159–189; 31:227–334 rubber (Hevea), 29:177–283 rutabaga, 8:217–248 sesame, 16:179–228 snap pea, 21:93–138 somatic hybridization, 20:167–225 sorghum drought tolerance, 31:189–222 sorghum male sterility, 25:139–172 soybean, 1:183–235; 3:289–311; 4:203–243; 21:212–307; 30:250–294 soybean fatty acids, 30:259–294 soybean hybrids, 21:212–307 soybean nodulation, 11:275–318 soybean recurrent selection, 15:275–313 spelt, 15:187–213 statistics, 17:296–300 strawberry, 2:195–214 sugarcane, 16:272–273; 27:15–158 supersweet sweet corn, 14:189–236 sweet cherry, 9:367–388 sweet corn, 1:139–161; 14:189–236; 35:213–215 sweet potato, 4:313–345; 35:217–218 Syngonium, 23:274 tomato, 4:273–311 transgene technology, 25:105–108 triticale, 5:41–93; 8:43–90 vegetable crop transgenics, 35:151–246 Vigna, 8:19–42 virus resistance, 12:47–79 wheat, 2:303–319; 3:169–191; 5:11–40; 11:225–234; 13:293–343, 28:1–37, 39–78 wheat,rust resistance, 13:293–343 white clover, 17:191–223 wild relatives, 30:149–230 wild rice, 14:237–265 Bringhurst, Royce S. (biography), 9:1–8 Broadbean, in vitro culture, 2:244–245 Bromeliad breeding, 23:275–276

CUMULATIVE SUBJECT INDEX Brown, Anthony, H.D. (biography), 31:1–20 Burton, Glenn W. (biography), 3:1–19 C Cactus: breeding, 20:135–166 domestication, 20:135–166 Cajanus, in vitro culture, 2:224 Calathea breeding, 23:276 Canola, R.K. Downey, designer, 18:1–12 Carbohydrates, 1:144–148 Carbon isotope discrimination, 12:81–113 Carica papaya, see Papaya Carnation, mutation breeding, 6:73–74 Carrot: breeding, 19: 157–190 transgenics, 35:219–220 Cassava: breeding, 2:73–134; 31:247–275 long-term selection, 24(2):74–79 transgenics: 35:216 Castanea, see Chestnut Cell selection, 4:139–145, 153–173 Cereal breeding, see Grain breeding Cereals: diversity, 21:221–261 stress resistance, 33:31–114 Cherry. See also Sweet cherry domestication, 25:202–293 Chestnut breeding, 4:347–397; 33:305–339 Chickpea, in vitro culture, 2:224–225 Chimeras and mosaics, 15:43–84 Chinese cabbage, heat tolerance, 10:152 Chromosome, petunia, 1:13–21, 31–33 Chrysanthemum: breeding, 14:321–361 mutation breeding, 6:74 Cicer, see Chickpea Citrus: breeding (seedlessness), 30:323–352 domestication, 25:296–298 protoplast fusion, 8:339–374 Clonal repositories, see National Clonal Germplasm Repository Clone identification (DNA), 34:221–295 Clover: in vitro culture, 2:240–244 molecular genetics, 17:191–223 Coffea arabica, see Coffee

383 Coffee, 2:157–193; 30:415–437 Cold hardiness: breeding nectarines and peaches, 10:271–308 wheat adaptation, 12:124–135 Cole crops: Chinese cabbage, heat tolerance, 10:152 gametoclonal variation, 5:371–372 rutabaga, 8:217–248 Coleus, 3:343–360 Competition, 13:158–165 Competitive ability breeding, 14:89–138 Controlling elements, see Transposable elements Corn, see Maize; Sweet corn Cotton, heat tolerance 10:151 Cowpea: breeding, 15:215–274 heat tolerance, 10:147–149 in vitro culture, 2:245–246 photoperiodic response, 3:99 transgenics, 35:215 Coyne, Dermot E. (biography), 23:1–19 Cranberry domestication, 25:304–305 Crop domestication and selection, 24(2):1–44 Cryopreservation, 7:125–126, 148–151, 167 buds, 7:168–169 genetic stability, 7:125–126 meristems, 7:168–169 pollen, 7:171–172 seed, 7:148–151,168 Cucumber, breeding, 6:323–359 Cucumis sativus, see Cucumber Cucumis melo, see Melon Cucurbitaceae: insect and mite resistance, 10:309–360 mapping, 27:213–244 Cucurbits: mapping, 27:213–244 transgenics: 35:196–199 Currant breeding, 29:145–175 Cybrids, 3:205–210; 20: 206–209 Cytogenetics: alfalfa, 10:171–184 blueberry, 5:325–326 Brassica, 31:21–187; 35:25–36 cassava, 2:94 citrus, 8:366–370

384 Cytogenetics (Continued ) coleus, 3:347–348 durum wheat, 5:12–14 fescue, 3:316–319 Glycine, 16:288–317 guayule, 6:99–103 maize mobile elements, 4:81–122 maize-tripsacum hybrids, 20:15–66 meiotic mutants, 28:163–214 oat, 6:173–174 polyploidy terminology, 26:105–124 pearl millet, 1:167 perennial rye, 13:265–292 petunia, 1:13–21, 31–32 potato, 25:1–19 raspberry, 32: 135–137 rose, 17:169–171 rye, 13:265–292 Saccharum complex, 16:273–275 sesame, 16:185–189 sugarcane, 27:74–78 triticale, 5:41–93; 8:54 wheat, 5:12–14; 10:5–15; 11:225–234 Cytoplasm: breeding, 23: 175–210; 25:115–138 cybrids, 3:205–210; 20:206–209 incompatibility, 25:115–138 male sterility, 25:115–138,139–172 molecular biology of male sterility, 10:23–51 organelles, 2:283–302; 6:361–393 pearl millet, 1:166 petunia, 1:43–45 sorghum male sterility, 25:139–172 wheat, 2:308–319 D Dahlia, mutation breeding, 6:75 Date palm domestication, 25:272–277 Daubeny, Hugh A. (biography), 32:21–37 Daucus, see Carrot Diallel cross, 9:9–36 Dieffenbachia breeding, 23:271–272 Diospyros, see Persimmon Disease and pest resistance: antifungal proteins, 14:39–88 apple rootstocks, 1:358–373 banana, 2:143–147 barley, 26:135–169 blackberry, 8:291–295

CUMULATIVE SUBJECT INDEX black walnut, 1:251 blueberry, rabbiteye, 5:348–350 cassava, 2:105–114; 31:247–275 cell selection, 4:143–145, 163–165 chestnut blight, 4: 347–397; 33:305–339 citrus, 8:347–349 coffee, 2:176–181 coleus, 3:353 cowpea, 15:237–247 durum wheat, 5:23–28 fescue, 3:334–336 herbicide-resistance, 11:155–198 host-parasite genetics, 5:393–433 induced mutants, 2:25–30 lettuce, 1:286–287 maize, 27:119–173; 31:223–245; 34:131–160 melon, 35: 86–150 millets, 35:247–374 ornamental transgenesis, 28:145–147 papaya, 26:161–357 potato, 9:264–285, 19:69–155 raspberry, 6:245–321; 32:184–247 rose, 31:277–324 rutabaga, 8:236–240 soybean, 1:183–235 spelt, 15:195–198 strawberry, 2:195–214 verticillium wilt, 33:115–144 virus resistance, 12:47–79 wheat rust, 13:293–343 Diversity: landraces, 21:221–261 legumes, 26:171–357 maize, 33:4–7 melon, 35:85–150 millets, 35:247–374 raspberry, 32:54–58 DNA: clone identification, 34:221–295 methylation, 18:87–176; 30:49–177 Doubled haploid breeding, 15:141–186; 25:57–88 Douglas-fir breeding, 27:245–353 Downey, Richard K. (biography), 18:1–12 Dracaena breeding, 23:277 Draper, Arlen D. (biography), 13:1–10 Drought resistance: cereals, 33:31–114 durum wheat, 5:30–31

CUMULATIVE SUBJECT INDEX maize, 25:173–253 sorghum, 31:189–222 soybean breeding, 4:203–243 wheat adaptation, 12:135–146 Dudley, J.W. (biography), 24(1):1–10 Durum wheat, 5:11–40 Duvick, Donald N. (biography), 14:1–11 E Eggplant transgenics: 35:187–191 Elaeis, see Oil palm Embryo culture: in crop improvement, 5:181–236 oil palm, 4:186–187 pasture legume hybrids, 5:249–275 Endosperm: balance number, 25:6–7 maize, 1:139–161 sweet corn, 1:139–161 Endothia parasitica, 4:355–357 Epepremnum breeding, 23:272–273 Epigenetics, 30:49–177 Epistasis, 21:27–92 Escherichia coli, long-term selection, 24(2):225–224 Evolution: Brassica, 31:21–187 coffee, 2:157–193 fruit, 25: 255–320 grapefruit, 13:345–363 maize, 20:15–66 sesame, 16:189 Exploration, 7:9–11, 26–28, 67–94 F Fabaceae, molecular mapping, 14:24–25 Fatty acid genetics and breeding, 30:259–294 Fern breeding, 23:276 Fescue, 3:313–342 Festuca, see Fescue Fig domestication, 25:281–285 Fire blight resistance, 29:315–358 Flavonoid chemistry, 25:91–94 Floral biology: almond, 8:314–320 blackberry, 8:267–269 black walnut, 1:238–244 cassava, 2:78–82

385 chestnut, 4:352–353 coffee, 2:163–164 coleus, 3:348–349 color, 25:89–114 fescue, 3:315–316 garlic: 23:211–244 guayule, 6:103–105 homeotic mutants, 9:63–99 induced mutants, 2:46–50 pearl millet, 1:165–166 pistil in reproduction, 4:9–79 pollen in reproduction, 4:9–79 raspberry, 32:90–92 reproductive barriers, 11:11–154 rutabaga, 8:222–226 sesame, 16:184–185 sweet potato, 4:323–325 Flower: color genetics, 25:89–114 color transgenesis, 28:28–139 Forage breeding: alfalfa inbreeding, 13:209–233 diversity, 21:221–261 fescue, 3:313–342 perennials, 11:251–274 white clover, 17:191–223 Foliage plant breeding, 23:245–290 Forest crop breeding: black walnut, 1:236–266 chestnut, 4:347–397 Douglas-fir, 27:245–353 ideotype concept, 12:177–187 molecular markers, 19:31–68 quantitative genetics, 8:139–188 rubber (Hevea), 29:177–283 Fragaria, see Strawberry Frey, Kenneth J. (biography), 34:1–36 Fruit, nut, and beverage crop breeding: almond, 8:313–338 apple, 9:333–366 apple fire blight resistance, 29:315–358 apple rootstocks, 1:294–394 banana, 2:135–155 blackberry, 8:249–312; 29:19–144 blueberry, 5:307–357; 13:1–10; 30:323–414 breeding, 25:255–320 cactus, 20:135–166 cherry, 9:367–388 chestnut, 4:347–397; 33:305–339

386 Fruit, nut (Continued ) citrus, 8:339–374; 30:323–352 coffee, 2:157–193; 30:415–437 currant, 29:145–175 domestication, 25:255–320 fire blight resistance, 29:315–358 genetic transformation, 16:87–134 gooseberry, 29:145–175 grapefruit, 13:345–363 ideotype concept, 12:175–177 incompatability, 28:215–237 melon, 35:85–150 mutation breeding, 6:78–79 nectarine (cold hardy), 10:271–308 origins, 25:255–320 papaya, 26:35–78 peach (cold hardy), 10:271–308 pear fireblight resistance, 29:315–358 persimmon, 19:191–225 plantain, 2:135–155 raspberry, 6:245–321; 32:1–353 strawberry, 2:195–214 sweet cherry, 9:367–388 Fungal diseases: apple rootstocks, 1:365–368 banana and plantain, 2:143–145, 147 barley, Fusarium head blight, 26:125–169 cassava, 2:110–114 cell selection, 4:163–165 chestnut blight, 4:355–397; 33:305–339 coffee, 2:176–179 cowpea, 15:237–238 durum wheat, 5:23–27 Fusarium head blight (barley), 26:125–169 host-parasite genetics, 5:393–433 lettuce, 1:286–287 maize foliar, 27:119–173; 31:223–245 potato, 19:69–155 raspberry, 6:245–281; 32:184–221 rose, 31:277–324 soybean, 1:188–209 spelt, 15:196–198 strawberry, 2:195–214 sweet potato, 4:333–336 transformation, fruit crops, 16:111–112 verticillium wilt, Solanaceae, 33:115–144

CUMULATIVE SUBJECT INDEX wheat rust, 13:293–343 Fusarium head blight (barley), 26:125–169 G Gabelman, Warren H. (biography), 6:1–9 Gametes: almond, self compatibility, 7:322–330 blackberry, 7:249–312 competition, 11:42–46 epigenetics, 30:49–177 forest trees, 7:139–188 maize aleurone, 7:91–137 maize anthocynanin, 7:91–137 mushroom, 7:189–216 polyploid, 3:253–288 rutabaga, 7:217–248 transposable elements, 7:91–137 unreduced, 3:253–288 Gametoclonal variation, 5:359–391 barley, 5:368–370 brassica, 5:371–372 potato, 5:376–377 rice, 5:362–364 rye, 5:370–371 tobacco, 5:372–376 wheat, 5:364–368 Garlic breeding, 6:81; 23:211–244 Genes: action, 15:315–374 apple, 9:337–356 Bacillus thuringensis, 12:19–45 incompatibility, 15:19–42 incompatibility in sweet cherry, 9:367–388 induced mutants, 2:13–71 lettuce, 1:267–293 maize endosperm, 1:142–144 maize protein, 1:110–120, 148–149 petunia, 1:21–30 quality protein in maize, 9:183–184 Rhizobium, 23:39–47 rol in breeding, 26:79–103 rye perenniality, 13:261–288 soybean, 1:183–235 soybean nodulation, 11:275–318 sweet corn, 1:142–144 wheat rust resistance, 13:293–343 Genetic engineering (transgeneic breeding): bean, 1:89–91 cereal stress resistance, 33:31–114

CUMULATIVE SUBJECT INDEX DNA methylation, 18:87–176 fire blight resistance, 29:315–358 fruit crops, 16:87–134 host-parasite genetics, 5:415–428 legumes, 26:171–357 maize mobile elements, 4:81–122 ornamentals, 125–162 papaya, 26:35–78 rol genes, 26:79–103 salt resistance, 22:389–425 sugarcane, 27:86–97 transformation by particle bombardment, 13:231–260 transgene technology, 25:105–108 virus resistance, 12:47–79 Genetic load and lethal equivalents, 10:93–127 Genetics: adaptation, 3:21–167 almond, self compatibility, 8:322–330 amaranth, 19:243–248 Amaranthus, see Amaranth apomixis, 18:13–86 apple, 9:333–366 Bacillus thuringensis, 12:19–45 bean seed color: 28:219–315 bean seed protein, 1:59–102 beet, 22:357–376 blackberry, 8:249–312; 29:19–144 black walnut, 1:247–251 blueberry, 13:1–10 blueberry, rabbiteye, 5:323–325 carrot, 19:164–171 chestnut blight, 4:357–389 chimeras, 15:43–84 chrysanthemums, 14:321–361 clover, white, 17:191–223 coffee, 2:165–170 coleus, 3:3–53 cowpea, 15:215–274 Cucurbitaceae, 27:213–344 cytoplasm, 23:175–210 DNA methylation, 18:87–176 domestication, 25:255–320 durum wheat, 5:11–40 epigenetics, 30:49–177 fatty acids in soybean, 30:259–294 fire blight resistance, 29:315–358 forest trees, 8:139–188 flower color, 25:89–114

387 fruit crop transformation, 16:87–134 gene action, 15:315–374 green revolution, 28:1–37, 39–78 history, 24(1):11–40 host-parasite, 5:393–433 incompatibility: circumvention, 11:11–154 molecular biology, 11:19–42; 28:215–237 sweet cherry, 9:367–388 induced mutants, 2:51–54 insect and mite resistance in Cucurbitaceae, 10:309–360 isozymes, 6:11–54 lettuce, 1:267–293 maize adaptedness, 28:101–123 maize aleurone, 8:91–137 maize anther culture, 11:199–224 maize anthocynanin, 8:91–137 maize endosperm, 1:142–144 maize foliar diseases, 27:118–173 maize male sterility, 10:23–51 maize mobile elements, 4:81–122 maize mutation, 5:139–180 maize quality protein, 9:1183–184; 34:83–113 maize seed protein, 1:110–120, 148–149 maize soil acidity tolerance, 28:59–123 mapping, 14:13–37 markers to manage germplasm, 13:11–86 maturity, 3:21–167 meiotic mutants, 163–214 metabolism and heterosis, 10:53–59 millets, 247–374 mitochondrial, 25:115–138 molecular mapping, 14:13–37 mosaics, 15:43–84 mushroom, 8:189–216 oat, 6:168–174 organelle transfer, 6:361–393 overdominance, 17:225–257 pea, 21:110–120 pearl millet, 1:166, 172–180 perennial rye, 13:261–288 petunia, 1:1–58 phosphate mechanisms, 29: 359–419 photoperiod, 3:21–167 plantain, 14:264–320 polyploidy terminology, 26:105–124 potato disease resistance, 19:69–165

388 Genetics (Continued ) potato ploidy manipulation, 3:274–277; 16:15–86 quality protein in maize, 9:183–184 quantitative trait loci, 15:85–139 quantitative trait loci in animals selection, 24(2):169–210, 211–224 raspberry, 32:9–353 reproductive barriers, 11:11–154 rhizobia, 23:21–72 rice, hybrid, 17:15–156, 23:73–174 Rosaceae, 27:175–211 rose, 17:171–172 rubber (Hevea), 29:177–283 rutabaga, 8:217–248 salt resistance, 22:389–425 selection, 24(1):111–131, 143–151, 269–290 snap pea, 21:110–120 sesame, 16:189–195 soybean, 1:183–235 soybean nodulation, 11:275–318 spelt, 15:187–213 supersweet sweet corn, 14:189–236 sweet corn, 1:139–161; 14:189–236 sweet potato, 4:327–330 temperature, 3:21–167 tomato fruit quality, 4:273–311 transposable elements, 8:91–137 triticale, 5:41–93 virus resistance, 12:47–79 wheat gene manipulation, 11:225–234 wheat male sterility, 2:307–308 wheat molecular biology, 11:235–250 wheat rust, 13:293–343 white clover, 17:191–223 yield, 3:21–167; 34:37–182 Genome: Brassica, 31:21–187; 35:25–36 Glycine, 16:289–317 Poaceae, 16:276–281 Genomics: coffee, 30:415–437 grain legumes, 26:171–357 Genotype  environment, interaction, 16:135–178 Germplasm, see also National Clonal Germplasm Repositories; National Plant Germplasm System acquisition and collection, 7:160–161

CUMULATIVE SUBJECT INDEX apple rootstocks, 1:296–299 banana, 2:140–141 blackberry, 8:265–267 black walnut, 1:244–247 Brassica, 31:21–187 cactus, 20:141–145 cassava, 2:83–94, 117–119; 31:247–275 cereal stress resistance, 33:31–114 chestnut, 4:351–352 coffee, 2:165–172 distribution, 7:161–164 enhancement, 7:98–202 evaluation, 7:183–198 exploration and introduction, 7:9–18, 64–94 genetic markers, 13:11–86 guayule, 6:112–125 isozyme, 6:18–21 grain legumes, 26:171–357 legumes, 26:171–357 maintenance and storage, 7:95–110, 111–128, 129–158, 159–182; 13:11–86 maize, 14:165–187; 33:9–16 melon, 35:85–150 management, 13:11–86 millets, 35:247–374 oat, 6:174–176 peanut, 22:297–356 pearl millet, 1:167–170 plantain, 14:267–320 potato, 9:219–223 preservation, 2:265–282; 23:291–344 raspberry, 32:75–90 rights, 25:21–55 rutabaga, 8:226–227 sampling, 29:285–314 sesame, 16:201–204 spelt, 15:204–205 sweet potato, 4:320–323 triticale, 8:55–61 wheat, 2:307–313 wild relatives, 30:149–230 Gesneriaceae, mutation breeding, 6:73 Gladiolus, mutation breeding, 6:77 Glycine, genomes, 16:289–317 Glycine max, see Soybean Goodman, Major M. (biography), 33:1–29 Gooseberry breeding, 29:145–175

CUMULATIVE SUBJECT INDEX Grain breeding: amaranth, 19:227–285 barley, 3:219–252, 5:95–138; 26:125–169 cereal stress resistance, 33:31–114 diversity, 21:221–261 doubled haploid breeding, 15:141–186 ideotype concept, 12:173–175 maize, 1:103–138, 139–161; 5:139–180; 9:115–179, 181–216; 11:199–224; 14:165–187; 22:3–4; 24(1): 11–40, 41–59, 61–78; 24(2): 53–64, 109–151; 25:173–253: 27:119–173; 28:59–100, 101–123; 31:223–245; 33:9–16. 34:37–82, 83–113, 131–160 maize history, 24(2):31–59, 41–59, 61–78 millets, 35: 247–374 oat, 6:167–207; 34:5–9 pearl millet, 1:162–182 rice, 17:15–156; 24(2):64–67 sorghum, 25:139–172; 31:189–222 spelt, 15:187–213 transformation, 13:231–260 triticale, 5:41–93; 8:43–90 wheat, 2:303–319; 5:11–40; 11:225–234, 235–250; 13:293–343; 22:221–297; 24(2):67–69; 28:1–37, 39–78 wild rice, 14:237–265 Grape: domestication, 25:279–281 transformation, 16:103–104 Grapefruit: breeding, 13:345–363 evolution, 13:345–363 Grass breeding: breeding, 11:251–274 mutation breeding, 6:82 recurrent selection, 9:101–113 transformation, 13:231–260 Growth habit, induced mutants, 2:14–25 Guayule, 6:93–165 H Hallauer, Arnel R. (biography), 15:1–17 Haploidy. See also Unreduced and polyploid gametes apple, 1:376 barley, 3:219–252 cereals, 15:141–186 doubled, 15:141–186; 25:57–88

389 maize, 11:199–224 petunia, 1:16–18, 44–45 potato, 3:274–277; 16:15–86 Harlan, Jack R. (biography), 8:1–17 Heat tolerance breeding, 10:129–168 Herbicide resistance: breeding needs, 11:155–198 cell selection, 4:160–161 decision trees, 18:251–303 risk assessment, 18:251–303 transforming fruit crops, 16:114 Heritability estimation, 22:9–111 Heterosis: gene action, 15:315–374 overdominance, 17:225–257 plant breeding, 12:227–251 plant metabolism, 10:53–90 rice, 17:24–33 soybean, 21:263–320 Hevea, see Rubber History: raspberry, 32:45–51 raspberry improvement, 32:59–66, 309–314 Honeycomb: breeding, 18:177–249 selection, 13:87–139, 18:177–249 Hordeum, see Barley Host-parasite genetics, 5:393–433 Human nutrition: breeding 31:325–392 quality protein maize, 34:97–101 Hyacinth, mutation breeding, 6:76–77 Hybrid and hybridization. See also Heterosis barley, 5:127–129 blueberry, 5:329–341 chemical, 3:169–191 interspecific, 5:237–305 maize high oil selection, 24(1):153–175 maize history, 24(1): 31–59, 41–59, 61–78 maize long-term selection, 24(2):43–64, 109–151 raspberry, 32:92–94 rice, 17:15–156 soybean, 21:263–307 verification, 34:193–205 wheat, 2:303–319 Hymowitz, Theodore (biography), 29:1–18

390 I Ideotype concept, 12:163–193 Inbreeding depression, 11:84–92 alfalfa, 13:209–233 cross pollinated crops, 13:209–233 Incompatibility: almond, 8:313–338 molecular biology, 15:19–42, 28:215–237 pollen, 4:39–48 reproductive barrier, 11:47–70 sweet cherry, 9:367–388 Incongruity, 11:71–83 Industrial crop breeding: guayule, 6:93–165 rubber (Hevea), 29:177–283 sugarcane, 27:5–118 Insect and mite resistance: apple rootstock, 1:370–372 black walnut, 1:251 cassava, 2:107–110 clover, white, 17:209–210 coffee, 2:179–180 cowpea, 15:240–244 Cucurbitaceae, 10:309–360 durum wheat, 5:28 maize, 6:209–243 raspberry, 6:282–300; 32:221–242 rutabaga, 8:240–241 sweet potato, 4:336–337 transformation fruit crops, 16:113 wheat, 22:221–297 white clover, 17:209–210 Intergeneric hybridization, papaya, 26:35–78 Interspecific hybridization: blackberry, 8:284–289 blueberry, 5:333–341 Brassica, 31:21–187 cassava, 31:247–275 citrus, 8:266–270 issues, 34:161–220 pasture legume, 5:237–305 raspberry, 32:146–152 rose, 17:176–177 rutabaga, 8:228–229 Vigna, 8:24–30 Intersubspecific hybridization, rice, 17:88–98

CUMULATIVE SUBJECT INDEX Introduction, 3:361–434; 7:9–11, 21–25 In vitro culture: alfalfa, 2:229–234; 4:123–152 barley, 3:225–226 bean, 2:234–237 birdsfoot trefoil, 2:228–229 blackberry, 8:274–275 broadbean, 2:244–245 cassava, 2:121–122 cell selection, 4:153–173 chickpea, 2:224–225 citrus, 8:339–374 clover, 2:240–244 coffee, 2:185–187 cowpea, 2:245–246 embryo culture, 5:181–236, 249–275 germplasm preservation, 7:125, 162–167 introduction, quarantines, 3:411–414 legumes, 2:215–264 mungbean, 2:245–246 oil palm, 4:175–201 pea, 2:236–237 peanut, 2:218–224 petunia, 1:44–48 pigeon pea, 2:224 pollen, 4:59–61 potato, 9:286–288 raspberry, 32:120–122 sesame, 16:218 soybean, 2:225–228 Stylosanthes, 2:238–240 wheat, 12:115–162 wingbean, 2:237–238 zein, 1:110–111 Ipomoea, see Sweet potato Isozymes, in plant breeding, 6:11–54 J Jahn, Margaret M. (biography), 35:1–17 Jennings, Derek (biography), 32:2–21 Jones, Henry A. (biography), 1:1–10 Juglans nigra, see Black walnut K Karyogram, petunia, 1:13 Kiwifruit: domestication, 25:300–301 transformation, 16:104

CUMULATIVE SUBJECT INDEX L Lactuca sativa, see Lettuce Landraces, diversity, 21:221–263 Laughnan, Jack R. (bibliography), 19:1–14 Legumes. See also Oilseed, peanut, soybean breeding, 33:157–304 cowpea, 15:215–274 genomics, 26:171–357; 33:157–304 pasture legumes, 5:237–305 peanut, 22:297–356; 30:295–322 soybean fatty acid manipulation, 259–294 Vigna, 8:19–42 Legume tissue culture, 2:215–264 Lethal equivalents and genetic load, 10:93–127 Lettuce: genes, 1:267–293 breeding, 16:1–14; 20:105–133 transgenics, 35:2–5-210 Lingonberry domestication, 25:300–301 Linkage: bean, 1:76–77 isozymes, 6:37–38 lettuce, 1:288–290 maps, molecular markers, 9:37–61 petunia, 1:31–34 Lotus: hybrids, 5:284–285 in vitro culture, 2:228–229 Lycopersicon, see Tomato M Maize: anther culture, 11:199–224; 15:141–186 anthocyanin, 8:91–137 apomixis, 18:56–64 biotic resistance, 34:131–160 breeding, 1:103–138, 139–161; 27:119–173; 33:9–16 carbohydrates, 1:144–148 cytoplasm, 23:189 diversity, 33:4–7 doubled haploid breeding, 15:141–186 drought tolerance, 25:173–253 exotic germplasm utilization, 14:165–187 foliar diseases, 27:119–173

391 germplasm, 33:9–16 high oil, 22:3–4; 24(1):153–175 history of hybrids, 23(1): 11–40, 41–59, 61–78 honeycomb breeding, 18:226–227 hybrid breeding, 17:249–251 insect resistance, 6:209–243 isozymes, 33:7–8 long-term selection, 24(2):53–64, 109–151 male sterility, 10:23–51 marker-assisted selection, 24(1):293–309 mobile elements, 4:81–122 mutations, 5:139–180 origins, 20:15–66 origins of hybrids, 24(1):31–50, 41–59, 61–78 overdominance, 17:225–257 physiological changes with selection, 24(1):143–151 protein, storage, 1:103–138 protein, quality 9:181–216; 34:83–113 recurrent selection, 9:115–179; 14:139–163 RFLF changes with selection, 24(1):111–131 selection for oil and protein, 24(1):79–110, 153–175 soil acidity tolerance, 28:59–100 supersweet sweet corn, 14:189–236 transformation, 13:235–264 transposable elements, 8:91–137 unreduced gametes, 3:277 yield, 27–182 vegetative phase change, 131–160 Male sterility: chemical induction, 3:169–191 coleus, 3:352–353 genetics, 25:115–138, 139–172 lettuce, 1:284–285 molecular biology, 10:23–51 pearl millet, 1:166 petunia, 1:43–44 rice, 17:33–72 sesame, 16:191–192 sorghum, 25:139–172 soybean, 21:277–291 wheat, 2:303–319 Malus spp, see Apple Malus  domestica, see Apple Malvaceae, molecular mapping, 14:25–27

392 Mango: domestication, 25:277–279 transformation, 16:107 Manihot esculenta, see Cassava Mapping: Cucurbitaceae, 27:213–244 Rosaceae, 27:175–211 Marker-assisted selection, see Selection conventional breeding, 33:145–217 gene pyramiding, 33:210–256 millets, 35:332–344 strategies, 34:247–348 Medicago. See also Alfalfa in vitro culture, 2:229–234 Meiosis: mutants, 28:239–115 petunia, 1:14–16 Melon, landraces of India, 35:85–150 Metabolism and heterosis, 10:53–90 Microprojectile bombardment, transformation, 13:231–260 Millets, genetic and genomic resources, 35:247–374 Mitochondrial genetics, 6:377–380; 25:115–138 Mixed plantings, bean breeding, 4:245–272 Mobile elements. See also Transposable elements maize, 4:81–122; 5:146–147 Molecular biology: apomixis, 18:65–73 comparative mapping, 14:13–37 cytoplasmic male sterility, 10:23–51 DNA methylation, 18:87–176 herbicide-resistant crops, 11:155–198 incompatibility, 15:19–42 legumes, 26:171–357 molecular markers, 9:37–61, 10:184–190; 12:195–226; 13:11–86; 14:13–37; 17:113–114, 179, 212–215; 18:20–42; 19:31–68, 21:181–220, 23:73–174, 24(1):203–309; 26:292–299; 33:145–217, 219–256; 34:247–358; 35:332–344 papaya, 26:35–78 raspberry, 32:126–134 rol genes, 26:79–103 salt resistance, 22:389–425 somaclonal variation, 16:229–268

CUMULATIVE SUBJECT INDEX somatic hybridization, 20:167–225 soybean nodulation, 11:275–318 strawberry, 21:139–180 transposable (mobile) elements, 4:81–122; 8:91–137 virus resistance, 12:47–79 wheat improvement, 11:235–250 Molecular markers, 9:37–61, 10:184–190; 12:195–226; 13:11–86; 14:13–37; 17:113–114, 179, 212–215; 18:20–42; 19:31–68, 21:181–220, 23:73–174; 33:145–217, 219–256; 34:247–358 alfalfa, 10:184–190 apomixis, 18:40–42 barley, 21:181–220 clover, white, 17:212–215 forest crops, 19:31–68 fruit crops, 12:195–226 maize selection, 24(1):293–309 mapping, 14:13–37 millets, 35:332–344 plant genetic resource mangement, 13:11–86 rice, 17:113–114, 23:73–124 rose, 17:179 somaclonal variation, 16:238–243 strategies, 34:247–358 wheat, 21:181–220 white clover, 17:212–215 Monosomy, petunia, 1:19 Mosaics and chimeras, 15:43–84 Mungbean, 8:32–35 in vitro culture, 2:245–246 photoperiodic response, 3:74, 89–92 Munger, Henry M. (biography), 4:1–8 Musa, see Banana, Plantain Mushroom, breeding and genetics, 8:189–215 Mutants and mutation: alfalfa tissue culture, 4:130–139 apple rootstocks, 1:374–375 banana, 2:148–149 barley, 5:124–126 blackberry, 8:283–284 cassava, 2:120–121 cell selection, 4:154–157 chimeras, 15:43–84 coleus, 3:355 cytoplasmic, 2:293–295 gametoclonal variation, 5:359–391

CUMULATIVE SUBJECT INDEX homeotic floral, 9:63–99 induced, 2:13–72 long term selection variation, 24(1):227–247 maize, 1:139–161, 4:81–122; 5:139–180 mobile elements, see Transposable elements mosaics, 15:43–84 petunia, 1:34–40 sesame, 16:213–217 somaclonal variation, 4:123–152; 5:147–149 sweet corn, 1:139–161 sweet potato, 4:371 transposable elements, 4:181–122; 8:91–137 tree fruits, 6:78–79 vegetatively-propagated crops, 6:55–91 zein synthesis, 1:111–118 Mycoplasma diseases, raspberry, 6:253–254 N National Clonal Germplasm Repository (NCGR), 7:40–43 cryopreservation, 7:125–126 genetic considerations, 7:126–127 germplasm maintenance and storage, 7:111–128 identification and label verification, 7:122–123 in vitro culture and storage, 7:125 operations guidelines, 7:113–125 preservation techniques, 7:120–121 virus indexing and plant health, 7:123–125 National Plant Germplasm System (NPGS). See also Germplasm history, 7:5–18 information systems, 7:57–65 operations, 7:19–56 preservation of genetic resources, 23:291–34 National Seed Storage Laboratory (NSSL), 7:13–14, 37–38, 152–153 Nectarines, cold hardiness breeding, 10:271–308 Nematode resistance: apple rootstocks, 1:368

393 banana and plantain, 2:145–146 coffee, 2:180–181 cowpea, 15:245–247 raspberry, 32:235–237 soybean, 1:217–221 sweet potato, 4:336 transformation fruit crops, 16:112–113 Nicotiana, see Tobacco Nodulation, soybean, 11:275–318 Nutriltion (human), 31:325–392 O Oat breeding, 6:167–207; 34:5–9 Oil palm: breeding, 4:175–201, 22:165–219 in vitro culture, 4:175–201 Oilseed breeding: canola, 18:1–20 oil palm, 4:175–201; 22:165–219 peanut, 22:295–356; 30:295–322 sesame, 16:179–228 soybean, 1:183–235; 3:289–311; 4:203–245; 11:275–318; 15:275–313 Olive domestication, 25:277–279 Onion, breeding history, 20:57–103 Opuntia, see Cactus Organelle transfer, 2:283–302; 3:205–210; 6:361–393 Ornamentals breeding: chrysanthemum, 14:321–361 coleus, 3:343–360 petunia, 1:1–58 rose, 17:159–189; 31:277–324 transgenesis, 28:125–162 Ornithopus, hybrids, 5:285–287 Orzya, see Rice Overdominance, 17:225–257 Ovule culture, 5:181–236 P Palm (Arecaceae): foliage breeding, 23:280–281 oil palm breeding, 4:175–201; 22:165–219. Panicum maximum, apomixis, 18:34–36, 47–49 Patents, raspberry, 32: 108–115

394 Papaya: breeding, 26:35–78 domestication, 25:307–308 transformation, 16:105–106 Parthenium argentatum, see Guayule Paspalum apomixis, 18:51–52 Paspalum notatum, see Pensacola bahiagrass Passionfruit transformation, 16:105 Pasture legumes, interspecific hybridization, 5:237–305 Pea: breeding, 21:93–138 flowering, 3:81–86, 89–92 in vitro culture, 2:236–237 Peach: cold hardiness breeding, 10:271–308 domestication, 25:294–296 transformation, 16:102 Peanut: breeding, 22:297–356 in vitro culture, 2:218–224 Pear: domestication, 25:289–290 transformation, 16:102 Pearl millet: apomixis, 18:55–56 breeding, 1:162–182 Pecan transformation, 16:103 Peloquin, Stanley, J. (biography), 25:1–19 Pennisetum americanum, see Pearl millet Pensacola bahiagrass, 9:101–113 apomixis, 18:51–52 selection, 9:101–113 Pepino transformation, 16:107 Peppermint, mutation breeding, 6:81–82 Perennial grasses, breeding, 11:251–274 Perennial rye breeding, 13:261–288 Persimmon: breeding, 19:191–225 domestication, 25:299–300 Petunia spp., genetics, 1:1–58 Phaseolin, 1:59–102 Phaseolus vulgaris, see Bean Philodendrum breeding, 23:273 Phosphate molecular mechanisms, 29:359–419 Phytophthora fragariae, 2:195–214 Pigeon pea, in vitro culture, 2:224 Pineapple domestication, 25:305–307

CUMULATIVE SUBJECT INDEX Pistil, reproductive function, 4:9–79 Pisum, see Pea Plantain: breeding, 2:135–155; 14:267–320; 21:1–25 domestication, 25: 298 Plant breeders rights, 25:21–55 Plant breeding: epigenetics, 30:49–177 politics, 25:21–55 prediction, 19:15–40 Plant exploration, 7:9–11, 26–28, 67–94 Plant introduction, 3:361–434; 7:9–11, 21–25 Plastid genetics, 6:364–376. See also Organelle Plum: domestication, 25:293–294 transformation, 16:103–140 Poaceae: molecular mapping, 14:23–24 Saccharum complex, 16:269–288 Pollen: reproductive function, 4:9–79 storage, 13:179–207 Polyploidy. See also Haploidy alfalfa, 10:171–184 alfalfa tissue culture, 4:125–128 apple rootstocks, 1:375–376 banana, 2:147–148 barley, 5:126–127 blueberry, 13:1–10 Brassica, 35:34–36 citrus, 30:322–352 gametes, 3:253–288 isozymes, 6:33–34 petunia, 1:18–19 potato, 16:15–86; 25:1–19 reproductive barriers, 11:98–105 sweet potato, 4:371 terminology, 26:105–124 triticale, 5:11–40 Pomegranate domestication, 25:285–286 Population genetics, see Quantitative genetics Potato: breeding, 9:217–332, 19:69–165 cytoplasm, 23:187–189 disease resistance breeding, 19:69–165 gametoclonal variation, 5:376–377

CUMULATIVE SUBJECT INDEX heat tolerance, 10:152 honeycomb breeding, 18:227–230 mutation breeding, 6:79–80 photoperiodic response, 3:75–76, 89–92 ploidy manipulation, 16:15–86 transgenics, 35:191–196 unreduced gametes, 3:274–277 Propagation, raspberry, 32:116–126 Protein: antifungal, 14:39–88 bean, 1:59–102 induced mutants, 2:38–46 maize, 1:103–138, 148–149; 9:181–216 Protoplast fusion, 3:193–218; 20: 167–225 citrus, 8:339–374 mushroom, 8:206–208 Prunus: amygdalus, see Almond avium, see Sweet cherry Pseudograin breeding, amaranth, 19:227–285 Psophocarpus, in vitro culture, 2:237–238 Q Quality protein maize, 9:181–216; 34:83–113 Quantitative genetics: epistasis, 21:27–92 forest trees, 8:139–188 gene interaction, 24(1):269–290 genotype  environment interaction, 16:135–178 heritability, 22:9–111 maize RFLP changes with selection, 24(1):111–131 mutation variation, 24(1): 227–247 overdominance, 17:225–257 population size & selection, 24(1):249–268 selection limits, 24(1):177–225 statistics, 17:296–300 trait loci (QTL), 15:85–139; 19:31–68 variance, 22:113–163 Quantitative trait loci (QTL), 15:85–138; 19:31–68 animal selection, 24(2):169–210, 211–224 marker-assisted selection, 33:145–217, 219–256

395 selection limits: 24(1):177–225 Quarantines, 3:361–434; 7:12, 35–37 R Rabbiteye blueberry, 5:307–357 Raspberry, breeding and genetics, 6:245–321, 32:1–353 Recurrent restricted phenotypic selection, 9:101–113 Recurrent selection, 9:101–113, 115–179; 14:139–163 soybean, 15:275–313 Red stele disease, 2:195–214 Redei, George P. (biography), 26:1–33 Regional trial testing, 12:271–297 Reproduction: barriers and circumvention, 11:11–154 foliage plants, 23:255–259 garlic, 23:211–244 Rhizobia, 23:21–72 Rhododendron, mutation breeding, 6:75–76 Ribes, see Currant, Gooseberry Rice. See also Wild rice anther culture, 15:141–186 apomixis, 18:65 cytoplasm, 23:189 doubled haploid breeding, 15:141–186 gametoclonal variation, 5:362–364 heat tolerance, 10:151–152 honeycomb breeding, 18:224–226 hybrid breeding, 17:1–15, 15–156; 23:73–174 long-term selection 24(2): 64–67 molecular markers, 17:113–114; 23:73–174 photoperiodic response, 3:74, 89–92 Rosa, see Rose Rosaceae, synteny, 27:175–211 Rose breeding, 17:159–189; 31:277–324 Rubber (Hevea) breeding, 29:177–283 Rubus, see Blackberry; Raspberry Rust, wheat, 13:293–343 Rutabaga, 8:217–248 Ryder, Edward J. (biography), 16:1–14 Rye: gametoclonal variation, 5:370–371 perennial breeding, 13:261–288 triticale, 5:41–93

396 S Saccharum complex, 16:269–288 Salamini, Francisco (biography), 30:1–47 Salt resistance: cell selection, 4:141–143 cereals, 33:31–114 durum wheat, 5:31 yeast systems, 22:389–425 Sears, Ernest R. (biography), 10:1–22 Secale, see Rye Seed: apple rootstocks, 1:373–374 banks, 7:13–14, 37–40, 152–153 bean, 1:59–102; 28:239–315 citrus, 30:322–350 garlic, 23:211–244 lettuce, 1:285–286 maintenance and storage, 7:95–110, 129–158, 159–182 maize, 1:103–138, 139–161, 4:81–86 pearl millet, 1:162–182 protein, 1:59–138, 148–149 raspberry, 32:94–101 rice production, 17:98–111, 118–119, 23:73–174 soybean, 1:183–235, 3:289–311 synthetic, 7:173–174 variegation, 4:81–86 wheat (hybrid), 2:313–317 Selection. See also Breeding bacteria, 24(2): 225–265 bean, 24(2):69–74 cell, 4:139–145, 153–173 crops of the developing world, 24(2):45–88 divergent selection for maize ear length, 24(2):153–168 domestication, 24(2):1–44 Escherichia coli, 24(2):225–265 gene interaction, 24(1):269–290 genetic models, 24(1):177–225 honeycomb design, 13:87–139; 18:177–249 limits, 24(1):177–225 maize high oil, 24(1):153–175 maize history, 24(1):11–40, 41–59, 61–78 maize inbreds, 28:101–123 maize long term, 24(1):79–110, 111–131, 133–151; 24(2):53–64, 109–151

CUMULATIVE SUBJECT INDEX maize oil & protein, 24(1):79–110, 153–175 maize physiological changes, 24(1): 133–151 maize RFLP changes, 24(1):111–131 marker assisted, 9:37–61, 10:184–190; 12:195–226; 13:11–86; 14:13–37; 17:113–114, 179, 212–215; 18:20–42; 19:31–68, 21:181–220, 23:73–174, 24(1):293–309; 26:292–299; 31:210–212, 33:145–217, 219–256; 34:247–348, 35:332–344 millets, 35:332–344 mutation variation, 24(1):227–268 population size, 24(1):249–268 prediction, 19:15–40 productivity gains in US crops, 24(2):89–106 quantitative trait loci, 24(1):311–335 raspberry, 32:102–108, 143–146 recurrent restricted phenotypic, 9:101–113 recurrent selection in maize, 9:115–179; 14:139–163 rice, 24(2):64–67 wheat, 24(2):67–69 Sesame breeding, 16:179–228 Sesamum indicum, see Sesame Simmonds, N.W. (biography), 21:1–13 Snap pea breeding, 21:93–138 Solanaceae: incompatibility, 15:27–34 molecular mapping, 14:27–28 verticillium wilt, 33:115–144 Solanum tuberosum, see Potato Somaclonal variation. See also Gametoclonal variation alfalfa, 4:123–152 isozymes, 6:30–31 maize, 5:147–149 molecular analysis, 16:229–268 mutation breeding, 6:68–70 rose, 17:178–179 transformation interaction, 16:229–268 utilization, 16:229–268 Somatic embryogenesis, 5:205–212; 7:173–174 oil palm, 4:189–190

CUMULATIVE SUBJECT INDEX Somatic genetics. See also Gametoclonal variation; Somaclonal variation alfalfa, 4:123–152 legumes, 2:246–248 maize, 5:147–149 organelle transfer, 2:283–302 pearl millet, 1:162–182 petunia, 1:43–46 protoplast fusion, 3:193–218 wheat, 2:303–319 Somatic hybridization. See also Protoplast fusion, 20:167–225 Sorghum: drought tolerance, 31:189–222 male sterility, 25:139–172 photoperiodic response, 3:69–71, 97–99 transformation, 13:235–264 Southern pea, see Cowpea Soybean: cytogenetics, 16:289–317 disease resistance, 1:183–235 drought resistance, 4:203–243 fatty acid manipulation, 30:259–294 genetics and evolution, 29:1–18 hybrid breeding, 21:263–307 in vitro culture, 2:225–228 nodulation, 11:275–318 photoperiodic response, 3:73–74 recurrent selection, 15:275–313 semidwarf breeding, 3:289–311 Spelt, agronomy, genetics, breeding, 15:187–213 Sprague, George F. (biography), 2:1–11 Sterility, 11:30–41. See also Male sterility Starch, maize, 1:114–118 Statistics: advanced methods, 22:113–163 history, 17:259–316 Strawberry: biotechnology, 21: 139–180 domestication, 25:302–303 red stele resistance breeding, 2:195–214 transformation, 16:104 Stenocarpella ear rot, 31:223–245 Stress resistance: cell selection, 4:141–143, 161–163 cereals, 33:31–114 transformation fruit crops, 16:115 Stylosanthes, in vitro culture, 2:238–240

397 Sugarcane: breeding, 27:15–118 mutation breeding, 6:82–84 Saccharum complex, 16:269–288 Synteny, Rosaceae, 27:175–211 Sweet cherry: domestication, 25:202–293 pollen-incompatibility and selffertility, 9:367–388 transformation, 16:102 Sweet corn, see also Maize: endosperm, 1:139–161 supersweet (shrunken2), 14:189–236 transgenics, 35:213–215 Sweet potato: breeding, 4:313–345; 6:80–81 transgenics, 35: 217–218 T Tamarillo transformation, 16:107 Taxonomy: amaranth, 19:233–237 apple, 1:296–299 banana, 2:136–138 blackberry, 8:249–253 brassicas, 35:19–83 cassava, 2:83–89 chestnut, 4:351–352 chrysanthemum, 14:321–361 clover, white, 17:193–211 coffee, 2:161–163 coleus, 3:345–347 fescue, 3:314 garlic, 23:211–244 Glycine, 16:289–317 guayule, 6:112–115 oat, 6:171–173 pearl millet, 1:163–164 petunia, 1:13 plantain, 2:136; 14:271–272 raspberry, 32:51–52 rose, 17:162–169 rutabaga, 8:221–222 Saccharum complex, 16:270–272 sweet potato, 4:320–323 triticale, 8:49–54 Vigna, 8:19–42 white clover, 17:193–211 wild rice, 14:240–241

398 Testing: adaptation, 12:271–297 honeycomb design, 13:87–139 Tissue culture, see In vitro culture Tobacco, gametoclonal variation, 5:372–376 Tomato: breeding for quality, 4:273–311 heat tolerance, 10:150–151 Toxin resistance, cell selection, 4:163–165 Transformation and transgenesis alfalfa, 10:190–192 alliums, 35:210–213 allelopathy, 30:231–258 barley, 26:155–157 brassicas, 35:199–205 carrot, 35:219–220 cassava, 35:216 cereals, 13:231–260; 33:31–114 cowpea, 35:215 cucurbits, 35:196–199 eggplant, 35:187–191 fire blight resistance, 29:315–358 fruit crops, 16:87–134 lettuce, 35:205–210 mushroom, 8:206 ornamentals, 28:125–162 papaya, 26:35–78 potato, 35:191–196 raspberry, 16:105; 32:133–134 rice, 17:179–180 somaclonal variation, 16:229–268 sugarcane, 27:86–97 sweet corn, 35:213–215 tomato, 35:164–187 sweet potato, 35:217–218 vegetable crops, 35:1511–246 white clover, 17:193–211 Transpiration efficiency, 12:81–113 Trilobium, long-term selection, 24(2):211–224 Transposable elements, 4:81–122; 5:146–147; 8:91–137 Tree crops, ideotype concept, 12:163–193 Tree fruits, see Fruit, nut, and beverage crop breeding Trifolium, see Clover; White Clover Trifolium hybrids, 5:275–284 in vitro culture, 2:240–244

CUMULATIVE SUBJECT INDEX Tripsacum: apomixis, 18:51 maize ancestry, 20:15–66 Trisomy, petunia, 1:19–20 Triticale, 5:41–93; 8:43–90 Triticosecale, see Triticale Triticum: Aestivum, see Wheat Turgidum, see Durum wheat Tulip, mutation breeding, 6:76 U United States National Plant Germplasm System, see National Plant Germplasm System Unreduced and polyploid gametes, 3:253–288; 16:15–86 Urd bean, 8:32–35 V Vaccinium, see Blueberry, Variance estimation, 22:113–163 Vegetable rootstock, and tuber breeding: alliums transgenics, 35:210–213 artichoke, 12:253–269 bean, 1:59–102; 4:245–272, 24(2):69–74; 28:239–315 bean (tropics), 10:199–269 beet (table), 22:257–388 brassica transgenics, 35:19–84, 199–205 carrot 19: 157–190, 35; 219–220 cassava, 2:73–134; 24(2):74–79; 31:247–275; 35:216 cowpea, 35:215 cucumber, 6:323–359 cucurbit, 10:309–360; 35:196–199 eggplant transgenics, 35:187–191 lettuce, 1:267–293; 16:1–14; 20:105–133; 35:205–210 melon, 35:85–150 mushroom, 8:189–215 onion, 20:67–103 pea, 21:93–138 peanut, 22:297–356 potato, 9:217–232; 16:15–86l; 19:69–165; 35:191–196 rutabaga, 8:217–248 snap pea, 21:93–138

CUMULATIVE SUBJECT INDEX

399

Solanaceae, verticillium wilt, 33:115–144 tomato, 4:273–311, 35:164–187 sweet corn, 1:139–161; 14:189–236; 35:213–215 sweet potato, 4:313–345; 6:80–8135: 213–215 vegetable crop transgenics: 151–246 verticillium wilt, Solanaceae, 22:115–144 Verticillium wilt, Solanaceae, 33:115–144 Vicia, in vitro culture, 2:244–245 Vigna, see Cowpea, Mungbean in vitro culture, 2:245–246; 8:19–42 Virus diseases: apple rootstocks, 1:358–359 clover, white, 17:201–209 coleus, 3:353 cowpea, 15:239–240 indexing, 3:386–408, 410–411, 423–425 in vitro elimination, 2:265–282 lettuce, 1:286 maize, 142–156 papaya, 26:35–78 potato, 19:122–134 raspberry, 6:247–254; 32:242–247 resistance, 12:47–79 soybean, 1:212–217 sweet potato, 4:336 transformation fruit crops, 16:108–110 white clover, 17:201–209 Vogel, Orville A. (biography), 5:1–10 Vuylsteke, Dirk R. (biography), 21:1–25

Wheat: anther culture, 15:141–186 apomixis, 18:64–65 chemical hybridization, 3:169–191 cold hardiness adaptation, 12:124–135 cytogenetics, 10:5–15 cytoplasm, 23:189–190 diversity, 21:236–237 doubled haploid breeding, 15:141–186 drought tolerance, 12:135–146 durum, 5:11–40 gametoclonal variation, 5:364–368 gene manipulation, 11:225–234 green revolution, 28; 1–37, 39–58 heat tolerance, 10:152 hybrid, 2:303–319; 3:185–186 insect resistance, 22:221–297 in vitro adaptation, 12:115–162 long-term selection, 24(2):67–69 molecular biology, 11:235–250 molecular markers, 21:191–220 photoperiodic response, 3:74 rust interaction, 13:293–343 triticale, 5:41–93 vernalization, 3:109 White clover, molecular genetics, 17:191–223 Wild rice, breeding, 14:237–265 Winged bean, in vitro culture, 2:237–238

W

Z

Walnut (black), 1:236–266 Walnut transformation, 16:103 Weinberger, John A. (biography), 11:1–10

Zea mays, see Maize, Sweet corn Zein, 1:103–138 Zizania palustris, see Wild rice

Y Yeast, salt resistance, 22:389–425 Yuan, Longping (biography), 17:1–13

Cumulative Contributor Index Volumes 1–35

Abbott, A.G., 27:175 Abdalla, O.S., 8:43 Acquaah, G., 9:63 Aldwinckle, H.S., 1:294; 29:315 Alexander, D.E., 24(1):53 Anderson, N.O., 10:93; 11:11 Aronson, A.I., 12:19 Aruna, R., 30:295 Aru´s, P., 27:175 Ascher, P.D., 10:9 Ashok Kumar, A., 31:189 Ashri, A., 16:179 Atlin, G.N., 34:83 Babu, R., 34:83 Baggett, J.R., 21:93 Bajic, V., 33:31 Balaji, J., 26:171 Baltensperger, D.D., 19:227; 35:247 Barker, T., 25:173 Bartels, D., 30:1 Basnizki, J., 12:253 Bassett, M.J., 28:239 Beck, D.L., 17:191 Beebe, S., 23:21–72 Beineke, W.F., 1:236 Bell, A.E., 24(2):211 Below, F.E., 24(1):133 Bertin, C. 30:231 Bertioli, D.J., 30:179 Berzonsky, W.A., 22:221 Bhat, S.R., 31:21; 35:19 Bingham, E.T., 4:123; 13:209

Binns, M.R., 12:271 Bird, R. McK., 5:139 Bjarnason, M., 9:181 Blair, M.W., 26; 30:179 Bliss, F.A., 1:59; 6:1 Boase, M.R., 14:321 Borlaug, N.E., 5:1 Boyer, C.D., 1:139 Bravo, J.E., 3:193 Brennan, R., 32:1 Brenner, D.M., 19:227 Bressan, R.A., 13:235; 14:39; 22:389 Bretting, P.K., 13:11 Broertjes, C., 6:55 Brown, A.H.D., 21:221 Brown, J.W.S., 1:59 Brown, S.K., 9:333, 367 Buhariwalla, H.K., 26:171 B€ unger, L., 24(2):169 Burnham, C.R., 4:347 Burton, G.W., 1:162; 9:101 Burton, J.W., 21:263 Byrne, D., 2:73 Camadro, E.L., 26:105 Campbell, K.G., 15:187 Campos, H., 25:173 Cantrell, R.G., 5:11 Cardinal, A.J., 30:259 Carputo, D., 25:1; 26:105; 28:163 Carvalho, A., 2:157 Casas, A.M., 13:235 Cervantes-Martinez, C.T., 22:9

Plant Breeding Reviews, Volume 35, First Edition. Edited by Jules Janick. Ó 2012 Wiley-Blackwell. Published 2012 by John Wiley & Sons, Inc. 401

402 Chandler, M.A., 34:131 Chen, J., 23:245 Cherry, M., 27:245 Chew, P.S., 22:165 Choo, T.M., 3:219; 26:125 Chopra, V.L., 31:21 Christenson, G.M., 7:67 Christie, B.R., 9:9 Clark, J.R., 29:19 Clark, R.L., 7:95 Clarke, A.E., 15:19 Clegg, M.T., 12:1 Cl ement-Demange, A., 29:177 Clevidence, B.A., 31:325 Comstock, J.G., 27:15 Condon, A.G., 12:81 Conicella, C., 28:163 Conner, A.J., 34:161 Consiglio, F., 28:163 Cooper, M, 24(2):109; 25:173 Cooper, R.L., 3:289 Cornu, A., 1:11 Costa, W.M., 2:157 Cregan, P., 12:195 Crouch, J.H., 14:267; 26:171 Crow, J.F., 17:225 Cummins, J.N., 1:294 Dambier, D. 30:323 Dana, S., 8:19 Das, B., 34:83 Dean, R.A., 27:213 De Groote, H., 34:83 De Jong, H., 9:217 Dekkers, J.C.M., 24(1):311 Deroles, S.C., 14:321 Dhillon, B.S., 14:139 Dhillon, N.P.S., 35:85 Diao, X., 35:247 Dias, J.S., 35:151 D’Hont, A., 27:15 Dickmann, D.I., 12:163 Ding, H., 22:221 Dirlewanger, E., 27:175 Dodds, P.N., 15:19 Dolan, D., 25:175 Donini, P., 21:181 Dowswell, C., 28:1 Doyle, J.J., 31:1 Draper, A.D., 2:195

CUMULATIVE CONTRIBUTOR INDEX Drew, R., 26:35 Dudley, J.W. 24(1):79 Dumas, C., 4:9 Duncan, D.R., 4:153 Duvick, D.N., 24(2):109 Dwivedi, S.L., 26:171; 30:179; 33:311; 35:247 Ebert, A.W., 30:415 Echt, C.S., 10:169 Edmeades, G., 25:173 Ehlers, J.D., 15:215 England, F., 20:1 Eubanks, M.W., 20:15 Evans, D.A., 3:193; 5:359 Everett, L.A., 14:237 Ewart, L.C., 9:63 Farquhar, G.D., 12:81 Fasoula, D.A., 14:89; 15:315; 18:177 Fasoula, V.A., 13:87; 14:89; 15:315; 18:177 Fasoulas, A.C., 13:87 Fazuoli, L.C., 2:157 Fear, C.D., 11:1 Ferris, R.S.B., 14:267 Finn, C.E., 29:19 Flore, J.A., 12:163 Forsberg, R.A., 6:167 Forster, B.P., 25:57 Forster, R.L.S., 17:191 Fowler, C., 25:21 Frei, U., 23:175 French, D.W., 4:347 Friesen, D.K., 28:59; 34:83 Froelicher, Y. 30:323 Frusciante, L., 25:1; 28:163 Fukunaga, K., 35:247 Gai, J., 21:263 Galiba, G., 12:115 Galletta, G.J., 2:195 Garcia-Mas, J., 35:85 Gao, Y., 33:115 Gehring, C., 33:31 Gepts, P., 24(2):1 Glaszmann, J.G., 27:15 Gmitter, F.G., Jr., 8:339; 13:345 Gold, M.A., 12:163 Goldman, I.L. 19:15; 20:67; 22:357; 24(1):61; 24(2):89; 35:1

CUMULATIVE CONTRIBUTOR INDEX Goldway, M., 28:215 Gonsalves, D., 26:35 Goodnight, C.J., 24(1):269 Gordon, S.G., 27:119 Gradziel, T.M., 15:43 Gressel, J., 11:155; 18:251 Gresshof, P.M., 11:275 Griesbach, R.J., 25:89 Griffin, W.B., 34:161 Grombacher, A.W., 14:237 Grosser, J.W., 8:339 Grumet, R., 12:47 Gudin, S., 17:159 Guimar~ aes, C.T., 16:269 Gupta, P.K., 33:145 Gustafson, J.P., 5:41; 11:225 Guthrie, W.D., 6:209 Habben, J., 25:173 Haley, S.D., 22:221 Hall, A.E., 10:129; 12:81; 15:215 Hall, H.K., 8:249; 29:19; 32:1, 39 Hallauer, A.R., 9:115; 14:1,165; 24(2):153 Hamblin, J., 4:245 Hancock, J.F., 13:1 Hancock, J.R., 9:1 Hanna, W.W., 13:179 Harlan, J.R., 3:1 Harris, M.O., 22:221 Hasegawa, P.M. 13:235; 14:39; 22:389 Hash, C., 35:247 Havey, M.J., 20:67 Haytowitz, D.B., 31:325 Henny, R.J., 23:245 Hill, W.G., 24(2):169 Hillel, J., 12:195 Hjalmarsson, I., 29:145 Hoa, T.T.T., 29:177 Hodgkin, T., 21:221 Hokanson, S.C., 21:139; 31:277 Holbrook, C.C., 22:297 Holden, J.M., 31:325 Holland, J.B., 21:27; 22:9; 33:1 Hor, T.Y., 22:165 Howe, G.T., 27:245 Hummer, K., 32:1, 39 Hunt, L.A., 16:135 Hutchinson, J.R., 5:181 Hymowitz, T., 8:1; 16:289

403 Ivan Ortiz-Monasterio, J., 28:39 Jackson, S.A., 33:257 Jain, A., 29:359 Jamieson, A.R., 32:39 Janick, J., 1:xi; 23:1; 25:255 Jansky, S., 19:77 Jayaram, Ch., 8:91 Jayawickrama, K., 27:245 Jenderek, M.M., 23:211 Jifon, J., 27:15 Johnson, A.A.T., 16:229; 20:167 Johnson, G.R., 27:245 Johnson, R., 24(1):293 Jones, A., 4:313 Jones, J.S., 13:209 Joobeur, T., 27:213 Ju, G.C., 10:53 Kang, H., 8:139 Kann, R.P., 4:175 Kapazoglou, A., 30:49 Karmakar, P.G., 8:19 Kartha, K.K., 2:215, 265 Kasha, K.J., 3:219 Kaur, H., 30:231 Keep, E., 6:245 Keightley, P.D., 24(1):227 Kirti, P.B., 31:21 Kleinhofs, A., 2:13 Knox, R.B., 4:9 Koebner, R.M.D., 21:181 Kollipara, K.P., 16:289 Koncz, C., 26:1 Kononowicz, A.K., 13:235 Konzak, C.F., 2:13 Kovacevic, N.M., 30:49 Krikorian, A.D., 4:175 Krishnamani, M.R.S., 4:203 Kronstad, W.E., 5:1 Kuehnle, A.R., 28:125 Kulakow, P.A., 19:227 Kumar, A., 33:145 Kumar, J., 33:145 Lamb, R.J., 22:221 Lambert, R.J., 22:1; 24(1):79:153 Lamborn, C., 21:93 Lamkey, K.R., 15:1; 24(1):xi; 24(2):xi; 31:223

404 Lavi, U., 12:195 Layne, R.E.C., 10:271 Lebowitz, R.J., 3:343 Lee, E.A., 34:37 Lee, M., 24(2):153 Lehmann, J.W., 19:227 Lenski, R.E., 24(2):225 Levings, III, C.S., 10:23 Lewers, K.R., 15:275 Li, J., 17:1,15 Liedl, B.E., 11:11 Lin, C.S., 12:271 Lockwood, D.R., 29:285 Lovell, G.R., 7:5 Lower, R.L., 25:21 Lukaszewski, A.J., 5:41 Luro, F., 30:323 Lyrene, P.M., 5:307; 30:353 Maas, J. L., 21:139 Mackenzie, S.A., 25:115 Maheswaran, G., 5:181 Maizonnier, D., 1:11 Malnoy, M., 29:285 Marcotrigiano, M., 15:43 Martin, F.W., 4:313 Matsumoto, T.K. 22:389 May, G.D., 33:257 McCoy, T.J., 4:123; 10:169 McCreight, J.D., 1:267; 16:1; 35:85 McDaniel, R.G., 2:283 McKeand, S.E., 19:41 McKenzie, R.I.H., 22:221 McRae, D.H., 3:169 Medina-Filho, H.P., 2:157 Mejaya, I.J., 24(1):53 Michler, C.H., 33:305 Mikkilineni, V., 24(1):111 Miles, D., 24(2):211 Miles, J.W., 24(2):45 Miller, R., 14:321 Ming, R., 27:15; 30:415 Mir, R.R., 33:145 Mirkov, T.E., 27:15 Mobray, D., 28:1 Mondragon Jacobo, C., 20:135 Monti, L.M., 28:163 Monforte, A.J., 35: 85 Moose, S.P., 24(1):133

CUMULATIVE CONTRIBUTOR INDEX Morgan, E.R., 34:161 Morrison, R.A., 5:359 Mowder, J.D., 7:57 Mroginski, L.A., 2:215 Mudalige-Jayawickrama, 28:125 Muir, W.M., 24(2):211 Mumm, R.H., 24(1):1 Murphy, A.M., 9:217 Mutschler, M.A., 4:1 Myers, J.R., 21:93 Myers, O., Jr., 4:203 Myers, R.L., 19:227 Namkoong, G., 8:1 Narro Leo´n, L.A., 28:59 Nassar, N.M.A., 31:248 Navazio, J., 22:357 Nelson, P.T., 33:1 Neuffer, M.G., 5:139 Newbigin, E., 15:19 Nielen, S., 30:179 Nigam, S.N., 30:295 Nikki Jennings, S. 32:1, 39 Nybom, H., 34:221 Nyquist, W.E., 22:9 Ohm, H.W., 22:221 Ollitrault, P., 30:323 O’Malley, D.M., 19:41 Ortiz, R., 14:267; 16:15; 21:1; 25:1, 139; 26:171; 28:1, 39; 30:179; 31:248; 33:31; 35:151 Osborn, T.C., 27:1 Palacios, N., 34:83 Palmer, R.G., 15:275, 21:263; 29:1; 31:1 Pandey, S., 14:139; 24(2):45; 28:59; 35:85 Pardo, J.M., 22:389 Parliman, B.J., 3:361 Paterson, A.H., 14:13; 26:15 Patterson, F.L., 22:221 Peairs, F.B., 22:221 Pedersen, J.F., 11:251 Peiretti, E.G., 23:175 Peloquin, S.J., 26:105 Perdue, R.E., Jr., 7:67 Peterson, P.A., 4:81; 8:91 Pickering, R., 34:161 Pitrat, M., 35:85

CUMULATIVE CONTRIBUTOR INDEX Pixley, K.V., 34:83 Polidoros, A.N., 18:87; 30:49 Pollak, L.M. 31:325 Porter, D.A., 22:221 Porter, R.A., 14:237 Powell, W., 21:181 Prakash, S., 31:21; 35:19 Prasad, M., 35:247 Prasartsee, V., 26:35 Pratt, R.C., 27:119 Pretorius, Z.A., 31:223 Priyadarshan, P.M., 29:177 Quiros, C.F., 31:21 Ramash, S., 31:189 Ratcliffe, R.H., 22:221 Ray, D.T., 6:93 Reddy, B.V.S., 25:139; 31:189 Redei, G.P., 10:1; 24(1):11 Reimann-Phillipp, R., 13:265 Reinbergs, E., 3:219 Reitsma, K.R., 35:85 Reynolds, M.P., 28:39 Rhodes, D., 10:53 Richards, C.M., 29:285 Richards, R.A., 12:81 Riedeman, E.S., 34:131 Roath, W.W., 7:183 Robinson, R.W., 1:267; 10:309 Robertson, L., 34:1 Rochefored, T.R., 24(1):111 Ron Parra, J., 14:165 Roos, E.E., 7:129 Ross, A.J., 24(2):153 Rossouw, J.D., 31:223 Rotteveel, T., 18:251 Rowe, P., 2:135 Russell, W.A., 2:1 Rutter, P.A., 4:347 Ryder, E.J., 1:267; 20:105 Sahi, S.V., 2:359 Samaras, Y., 10:53 Sanjana Reddy, P., 31:189 Sansavini, S., 16:87 Santra, D., 35:247 Sapir, G., 28:215 Saunders, J.W., 9:63

405 Savidan, Y., 18:13 Sawhney, R.N., 13:293 Schaap, T., 12:195 Schaber, M.A., 24(2):89 Schneerman, M.C., 24(1):133 Schnell, R.J., 27:15 Schroeck, G., 20:67 Schussler, J., 25:173 Scott, D.H., 2:195 Seabrook, J.E.A., 9:217 Sears, E.R., 11:225 Seebauer, J.R., 24(1):133 Senthilvel, S., 36:247 Serraj, R., 26:171 Shands, Hazel L., 6:167 Shands, Henry L., 7:1, 5 Shannon, J.C., 1:139 Shanower, T.G., 22:221 Sharma, A., 35:85 Shattuck, V.I., 8:217; 9:9 Shaun, R., 14:267 Sidhu, G.S., 5:393 Silva, da, J., 27:15 Silva, H.D., 31:223 Simmonds, N.W., 17:259 Simon, P.W., 19:157; 23:211; 31:325 Singh, B.B., 15:215 Singh, P.K., 35:85 Singh, R.J., 16:289 Singh, S.P., 10:199 Singh, Z., 16:87 Slabbert, M.M., 19:227 Sleper, D.A., 3:313 Sleugh, B.B., 19 Smith, J.S.C., 24(2):109 Smith, K.F., 33:219 Smith, S.E., 6:361 Snoeck, C., 23:21 Sobral, B.W.S., 16:269 Socias i Company, R., 8:313 Soh, A.C., 22:165 Sondahl, M.R., 2:157 Spoor, W., 20:1 Stafne, E.T., 29:19 Stalker, H.T., 22:297; 30:179 Steadman, J.R., 23:1 Steffensen, D. M., 19:1 Stern, R.A., 28:215 Stevens, M.A., 4:273

406 Stoner, A.K., 7:57 Stuber, C.W., 9:37; 12:227 Subudhi, P., 33:31 Sugiura, A., 19:191 Sun, H., 21:263 Suzaki, J.Y., 26:35 Tai, G.C.C., 9:217 Talbert, L.E., 11:235 Tan, C.C., 22:165 Tani, E., 30:49 Tarn, T.R., 9:217 Tehrani, G., 9:367 Teshome, A., 21:221 Tew, T.L., 27:15 Thomas, W.T.B., 25:57 Thompson, A.E., 6:93 Thro, A.M., 34:1 Thudi, M., 33:257 Tiefenthaler, A.E., 24(2):89 Timmerman-Vaughan, G.M., 34:161 Tollenaar, M., 34:37 Towill, L.E., 7:159, 13:179 Tracy, W.F., 14:189; 24(2):89; 34:131 Trethowan, R.M., 28:39 Tripathi, S., 26:35 Troyer, A.F., 24(1):41; 28:101 Tsaftaris, A.S., 18:87; 30:49 Tsai, C.Y., 1:103 Twumasi-Afriyie, S., 83 Ullrich, S.E., 2:13 Upadhyaya, H.D., 26:171; 39:179; 33:31; 35:247 Uribelarrea, M., 24(1):133 Vanderleyden, J., 23:21 Van Ginkel, M. 34:297 Van Harten, A.M., 6:55 Varshney, R.K., 33:257 Varughese, G., 8:43 Vasal, S.K., 9:181; 14:139 Vasconcelos, M.J., 29:359 Vega, F.E., 30:415 Vegas, A., 26:35 Veilleux, R., 3:253; 16:229; 20:167; 33:115 Venkatachalam, P., 29:177 Villareal, R.L., 8:43 Vivak, B., 34:83

CUMULATIVE CONTRIBUTOR INDEX Vogel, K.P., 11:251 Volk, G.M., 23:291; 29:285 Vuylsteke, D., 14:267 Wallace, B., 29:145 Wallace, D.H., 3:21; 13:141 Walsh, B. 24(1):177 Wan, Y., 11:199 Wang, Y.-H., 27:213 Waters, C., 23:291 Weber, C.A., 32:39 Weber, K., 24(1):249 Weeden, N.F., 6:11 Wehner, T.C., 6:323 Weising, K., 34:221 Welander, M., 26:79 Wenzel, G. 23:175 Weston, L.A. 30:231 Westwood, M.N., 7:111 Wheeler, N.C., 27:245 Whitaker, T.W., 1:1 Whitaker, V.M., 31:277 White, D.W.R., 17:191 White, G.A., 3:361; 7:5 Widholm, J.M., 4:153; 11:199 Widmer, R.E., 10:93 Widrlechner, M.P., 13:11 Wilcox, J.R., 1:183 Williams, E.G., 4:9; 5:181, 237 Williams, M.E., 10:23 Williamson, B., 32:1 Wilson, J.A., 2:303 Woeste, K.E., 33:305 Wong, G., 22:165 Woodfield, D.R., 17:191 Worthen, L.M., 33:305 Wright, D., 25:173 Wright, G.C., 12:81 Wu, K.-K., 27:15 Wu, L., 8:189 Wu, R., 19:41 Wu, X.-M. 35:19 Xin, Y., 17:1 Xu, S., 22:113 Xu, Y., 15:85; 23:73 Yamada, M., 19:191 Yamamoto, T., 27:175

CUMULATIVE CONTRIBUTOR INDEX Yan, W., 13:141 Ye, G., 33:219; 34:297 Yang, W.-J., 10:53 Yonemori, K., 19:191 Yopp, J.H., 4:203 Yun, D.-J., 14:39

407 Zeng, Z.-B., 19:41 Zhu, L.-H., 26:79 Zimmerman, M.J.O., 4:245 Zinselmeier, C., 25:173 Zitter, T.A., 33:115 Zohary, D., 12:253