Plant Breeding Reviews, Volume 46 1st Edition

vi CONTENTS III. History of IWG Breeding IV. Breeding Methodologies by Program V. Breeding Goals and Progress VI. Modern Breeding Tools VII. Rate of Intermediate Wheatgrass Domestication VIII. Future Directions Literature Cited 4 Understanding Environmental Modulation of Heterosis 140 146 162 175 190 195 197 219 Zhi Li, Jiabin Sun, and Candice N. Hirsch I. Introduction of Heterosis II. Models and Mechanisms to Explain Heterosis III. Genotype-by-Environment Interaction IV.Inbred Lines Generally Have More Instability Across Environments than Hybrids V.Higher Heterosis Levels are Observed Under Stress Conditions VI.Variation in Heterosis is also Observed Under Natural Conditions VII. Conclusion and Future Prospects Literature Cited 220 221 224 5 239 Breeding of Hemp (Cannabis sativa) 226 227 231 232 233 Lawrence B. Smart, Jacob A. Toth, George M. Stack, Luis A. Monserrate, and Christine D. Smart I. Introduction II. Taxonomy and Domestication of Hemp III. Sex Determination in Hemp IV. Control of Pollination V. Breeding and Selection Schemes VI. Target Traits for Genetic Improvement VII. Germplasm Resources VIII. Genomic Resources IX. Future Directions Literature Cited 240 245 247 250 255 259 277 278 279 279 CONTENTS 6 vii Genetic Resources and Breeding Priorities in Phaseolus Beans: Vulnerability, Resilience, and Future Challenges 289 Travis A. Parker, Jorge Acosta Gallegos, James Beaver, Mark Brick, Judith K. Brown, Karen Cichy, Daniel G. Debouck, Alfonso Delgado-Salinas, Sarah Dohle, Emmalea Ernest, Consuelo Estevez de Jensen, Francisco Gomez, Barbara Hellier, Alexander V. Karasev, James D. Kelly, Phillip McClean, Phillip Miklas, James R. Myers, Juan M. Osorno, Julie S. Pasche, Marcial A. Pastor-Corrales, Timothy Porch, James R. Steadman, Carlos Urrea, Lyle Wallace, Christine H. Diepenbrock, and Paul Gepts I.Description of Crop Vulnerability and Its Relevance in Phaseolus II.Background on the Origin, Diversification, and Domestication of the Genus Phaseolus III.Urgency and Extent of Crop Vulnerabilities and Threats to Food Security IV. Genetic Erosion in the Centers of Origin V. Status of Plant Genetic Resources in the NPGS VI. Genomic and Genotypic Characterization Data VII.Prospects, Future Development, and Gaps in Genetic Diversity VIII. Epilogue Literature Cited 7 Club Wheat – A Review of Club Wheat History, Improvement, and Spike Characteristics in Wheat 294 296 318 325 352 361 371 381 385 421 Kimberly A. Garland-Campbell I. Introduction II. Spike Architecture in Grasses III. Club Wheat History IV. Club Wheat Breeding V.Major Genes for Control of Spike Charactersitics in Wheat VI. Conclusion Literature Cited 423 424 426 432 444 454 455 viii 8 CONTENTS Predicting Genotype × Environment × Management (G × E × M) Interactions for the Design of Crop Improvement Strategies: Integrating Breeder, Agronomist, and Farmer Perspectives 467 Mark Cooper, Carlos D. Messina, Tom Tang, Carla Gho, Owen M. Powell, Dean W. Podlich, Frank Technow, and Graeme L. Hammer I. Three Perspectives of G × E × M Interactions II. Foundations for G × E × M Prediction III. The Breeder’s Equation and Beyond IV.G × E × M Considerations for Designing Multi-Environment Trials V. Breeder’s Questions: G × E × M → G × (E × M) VI. Agronomist’s Questions: G × E × M → M × (E × G) VII. Farmer’s Questions: G × E × M → (G × M) × E VIII. Integrating the Different G × E × M Perspectives IX.G × E × M Predictions Beyond the Training Data Boundaries X.Prediction-Based Crop Improvement: Future Prospects Literature Cited 9 Root Phenes for Improving Nutrient Capture in Low-Fertility Environments 470 476 480 482 510 520 525 531 548 555 560 587 Christopher F. Strock and Hannah M. Schneider I. The Need for Nutrient-Efficient Crops II.Root Phenes are Important for Resource Aqusition and Plant Growth III. Root Ideotypes for Improved Nutrient Acquisition IV. Phenotyping Methodology and Technology V.Deployment Strategies for Root Phenes in Crop Breeding Programs VI. Conclusions Literature Cited 10 Role of the Genomics–Phenomics–Agronomy Paradigm in Plant Breeding 589 590 596 605 610 614 615 627 Chunpeng James Chen, Jessica Rutkoski, James C. Schnable, Seth C. Murray, Lizhi Wang, Xiuliang Jin, Benjamin Stich, Jose Crossa, Ben J. Hayes, and Zhiwu Zhang I. Introduction II. Agronomy and Genomics (A-G) 630 631 CONTENTS ix III. Genomics and Phenomics (G-P) IV. Phenomics and Agronomy (P-A) V. Merge G-P-A through GWAS VI. Merge G-P-A through Blup VII. Merge G-P-A through Bayesian Methods VIII. Merge G-P-A through Ml IX. Conclusion and Future Prospects Literature Cited 636 641 644 647 649 654 658 659 Cumulative Contributor Index Cumulative Subject Index 675 685 List of Contributors Kayla R. Altendorf Seed and Cereal Research Unit, USDA ARS, Prosser, WA, USA James A. Anderson Department of Agronomy & Plant Genetics, University of Minnesota, St. Paul, MN, USA Prabin Bajgain Department of Agronomy & Plant Genetics, University of Minnesota, St. Paul, MN, USA James Beaver Departamento de Cultivos y Ciencias Agro-Ambientales, University of Puerto Rico, Mayagüez, PR, USA Mark Brick Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, USA Judith K. Brown School of Plant Sciences, University of Arizona, Tucson, AZ, USA Douglas J. Cattani Department of Plant Science, University of Manitoba, Winnipeg, MB, Canada Chunpeng James Chen Department of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA, USA Karen Cichy Sugarbeet and Bean Research Unit, USDA-ARS, East Lansing, MI, USA Patrick J. Conner Department of Horticulture, University of Georgia, Tifton, GA, USA xi xii List of Contributors Mark Cooper Queensland Alliance for Agriculture and Food Innovation (QAAFI), The University of Queensland, Brisbane, Queensland, Australia ARC Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, Queensland, Australia Jared L. Crain Department of Plant Pathology, Kansas State University, Manhattan, KS, USA Timothy E. Crews The Land Institute, Salina, KS, USA Jose Crossa Biometrics and Statistics Unit, International Maize and Wheat Improvement Center (CIMMYT), Texcoco, México Daniel G. Debouck Programa de Recursos Genéticos, CIAT, Cali, Colombia Lee R. DeHaan The Land Institute, Salina, KS, USA Alfonso Delgado-Salinas Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, México Christine H. Diepenbrock Department of Plant Sciences, University of California, Davis, CA, USA Sarah Dohle Department of Plant Science, Delaware Valley University, Doylestown, PA, USA Emmalea Ernest Cooperative Extension Vegetable & Fruit Program, University of Delaware, Georgetown, DE, USA Jorge Acosta Gallegos Campo Experimental Bajío, INIFAP, Celaya, México Kimberly A. Garland-Campbell USDA-ARS Wheat Health, Genetics and Quality Unit, Washington State University, Pullman, WA, USA List of Contributors xiii Paul Gepts Department of Plant Sciences, University of California, Davis, CA, USA Carla Gho Corteva Agriscience, Johnston, IA, USA Irwin L. Goldman Department of Horticulture, University of Wisconsin-Madison, Madison, WI, USA Francisco Gomez Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA Graeme L. Hammer Queensland Alliance for Agriculture and Food Innovation (QAAFI), The University of Queensland, Brisbane, Queensland, Australia ARC Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, Queensland, Australia Ben J. Hayes Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, Queensland, Australia Barbara Hellier Plant Germplasm Introduction and Testing Research Unit, USDA-ARS, Pullman, WA, USA Candice N. Hirsch Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN, USA Ying Hu College of Plant Protection, Jilin Agricultural University, Changchun, Jilin, China Consuelo Estevez de Jensen Departamento de Cultivos y Ciencias Agro-Ambientales, University of Puerto Rico, Mayagüez, PR, USA Xiuliang Jin Ministry of Agriculture, Chinese Academy of Agricultural Sciences/ Key Laboratory of Crop Physiology and Ecology, Institute of Crop Sciences, Beijing, China xiv List of Contributors Alexander V. Karasev Department of Entomology, Plant Pathology and Nematology, University of Idaho, Moscow, ID, USA James D. Kelly Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, USA Steven R. Larson Forage and Range Research, USDA ARS, Logan, UT, USA Zhi Li State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China Phillip McClean Department of Plant Sciences, North Dakota State University, Fargo, ND, USA Carlos D. Messina Corteva Agriscience, Johnston, IA, USA Horticultural Sciences Department, University of Florida, Gainesville, FL, USA Phillip Miklas Grain Legume Genetics Physiology Research Unit, USDA-ARS, Prosser, WA, USA Luis A. Monserrate School of Integrative Plant Science, Cornell University, Geneva, NY, USA Seth C. Murray Department of Soil and Crop Sciences, Texas A&M University, College Station, College Station, TX, USA James R. Myers Department of Horticulture, Oregon State University, Corvallis, OR, USA Juan M. Osorno Department of Plant Sciences, North Dakota State University, Fargo, ND, USA Travis A. Parker Department of Plant Sciences, University of California, Davis, CA, USA List of Contributors xv Julie S. Pasche Department of Plant Sciences, North Dakota State University, Fargo, ND, USA Marcial A. Pastor-Corrales Beltsville Agricultural Center, Soybean Genomics and Improvement Center, USDA-ARS, Beltsville, MD, USA Dean W. Podlich Corteva Agriscience, Johnston, IA, USA Jesse A. Poland King Abdullah University of Science and Technology, Thuwal, Makkah, Saudi Arabia Timothy Porch Tropical Agriculture Research Station, USDA-ARS, Mayagüez, PR, USA Owen M. Powell Queensland Alliance for Agriculture and Food Innovation (QAAFI), The University of Queensland, Brisbane, Queensland, Australia ARC Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, Queensland, Australia Jessica Rutkoski Department of Crop Sciences, University of Illinois at Urbana- Champaign, Urbana, IL, USA James C. Schnable Department of Agronomy and Horticulture, University of Nebraska- Lincoln, Lincoln, NE, USA Hannah M. Schneider Centre for Crop Systems Analysis, Wageningen University & Research, Wageningen, The Netherlands Christine D. Smart School of Integrative Plant Science, Cornell University, Geneva, NY, USA Lawrence B. Smart School of Integrative Plant Science, Cornell University, Geneva, NY, USA George M. Stack School of Integrative Plant Science, Cornell University, Geneva, NY, USA xvi List of Contributors James R. Steadman Department of Plant Pathology, University of Nebraska, Lincoln, NE, USA Benjamin Stich Institute for Quantitative Genetics and Genomics of Plants, Heinrich Heine University, Düsseldorf, Germany Christopher F. Strock Breeding Insight, Cornell University, Ithaca, NY, USA Jiabin Sun State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China Tom Tang Corteva Agriscience, Johnston, IA, USA Frank Technow Corteva Agriscience, Tavistock, Ontario, Canada Jacob A. Toth School of Integrative Plant Science, Cornell University, Geneva, NY, USA M. Kathryn Turner The Land Institute, Salina, KS, USA Carlos Urrea Department of Agronomy and Horticulture, University of Nebraska, Scottsbluff, NE, USA Lyle Wallace Plant Germplasm Introduction and Testing Research Unit, USDA-ARS, Pullman, WA, USA Lizhi Wang Department of Industrial and Manufacturing Systems Engineering, Iowa State University, Ames, IA, USA Anna Westerbergh Department of Plant Biology, Uppsala BioCenter, Linnean Centre for Plant Biology in Uppsala, Swedish University of Agricultural Sciences, Uppsala, Sweden List of Contributors xvii Margaret L. Worthington Department of Horticulture, University of Arkansas, Fayetteville, AR, USA Zhiwu Zhang Department of Crop and Soil Sciences, Washington State University, Pullman, WA, USA 1 Dani Zamir: Pioneer in Tomato Genetics and Quantitative Trait Dissection Irwin L. Goldman Department of Horticulture, University of Wisconsin-Madison, Madison, WI, USA ABSTRACT The dedicatory chapters for PBR have traditionally not had abstracts; but if there is a strong sense that there should be one I can write it-however this hasn’t always been done. KEYWORDS: Tomato, quantitative trait loci, introgression lines, tomato genome, overdominance, introgression breeding OUTLINE I. INTRODUCTION II. UNDERSTANDING QUANTITATIVE GENETIC VARIATION III. CLONING OF QUANTITATIVE TRAIT LOCI IV. CHARACTERIZATION OF GENETIC PHENOMENA V. SEQUENCING THE TOMATO GENOME VI. PRACTICAL PLANT BREEDING VII. SCIENTIFIC IMPACT VIII. LIST OF SCIENTIFIC JOURNAL PUBLICATIONS OF DANI ZAMIR ACKNOWLEDGMENTS LITERATURE CITED Plant Breeding Reviews, Volume 46, First Edition. Edited by Irwin Goldman. © 2023 John Wiley & Sons, Inc. Published 2023 by John Wiley & Sons, Inc. 1 2 Irwin L. Goldman ABBREVIATIONS ILs QTL CWR Introgression Lines Quantitative Trait Locus Crop Wild Relative I. INTRODUCTION For more than four decades, Dani Zamir has been among the most influential scientists in plant breeding throughout the world (Figure 1.1). Professor Zamir has spent his career at the Hebrew University of Jerusalem, in Rehovot, Israel, where he and his students have made great strides in improving our understanding of the genetic basis of quantitative traits in crop plants and in developing tools for advancing the science of plant breeding. Zamir was able to combine those efforts with practical plant breeding, leading to the development of highly productive cultivars and the establishment of practical breeding programs in horticultural species. He also mentored many undergraduate and graduate students in plant genetics and taught a popular course. Now Professor Emeritus, Dani Zamir’s work on tomato genomics, genetics, and breeding continues into his fifth decade of work on Fig. 1.1. Dani Zamir, Professor Emeritus, Hebrew University of Jerusalem, Israel. Source: Photo credit: D. Zamir. Dani Zamir 3 the crop. This dedication focuses on a few of his key accomplishments in the field of plant breeding and plant genetics. Dani Zamir was born in 1950 in Israel. Following his military service, he received degrees from the Hebrew University of Jerusalem (undergraduate) and the University of California-Davis (graduate), completing his doctorate in 1981. He started his career as a lecturer in genetics at the Hebrew University’s Faculty of Agriculture in Rehovot, Israel, in 1982 and was appointed senior lecturer in 1985. In 1992, he became associate professor and in 1996, professor of Genetics. He retired from his formal teaching and research at the University in 2018 and is now Professor Emeritus. Zamir also held adjunct appointments in genetics at Seoul University in South Korea and Cornell University in Ithaca, New York. Throughout his career, Zamir taught a popular course in general genetics to undergraduates at Hebrew University and was a mentor for numerous students. Zamir has also founded two companies, each of which has achieved substantial success. The first, AB Seeds, initiated approximately 20 years ago, is a breeding and genetics company specializing in crop seeds including tomato. The company was sold to De Ruiter in 2008 and later purchased by Monsanto. More recently, Zamir and his student Yaniv Semel established the company Phenome Networks, which has developed proprietary software for managing complex breeding programs and the phenotypic and genotypic data that they generate. The company, based in Rehovot, Israel, serves a wide variety of public and private customers and helps users track crossing, trialing, phenotyping, and genotyping activities that are core components of breeding programs. Zamir has served on the advisory boards of a number of institutions, journals, and projects, including Genoplante (France), the Max Planck Institute for Plant Breeding (Germany), the Department of Plant Molecular Biology at the University of Barcelona (Spain), the Grapevine Genome Project (Italy), the International SOL Genome Project, and the journals G3: Genes, Genomes, Genetics; Scientific Data; The Plant Journal; and Scientific Reports. Zamir was also recipient of the Kaye Innovation Prize from the Hebrew University of Jerusalem in 2007, the EMET Prize in Agriculture in 2015, which recognizes excellence in academic and professional achievements that have significant influence on society, and the highly prestigious Israel Prize 2020. The Israel Prize is awarded by the State of Israel and is considered the highest honor the state bestows on an individual. It is highly selective and awarded annually in a formal state ceremony attended by the President, Prime Minister, and other 4 Irwin L. Goldman dignitaries. The recipients of the prize are Israeli citizens or organizations who have displayed excellence in their field(s) or have contributed strongly to the culture of Israel. Receipt of this award is a singular achievement and a powerful indicator of the impact of Dani Zamir’s work in agricultural science. II. UNDERSTANDING QUANTITATIVE GENETIC VARIATION Dani Zamir has long been a proponent of understanding and utilizing genetic variability, particularly that from crop wild relatives (CWRs), to improve modern crops. Among his most well-known projects was the development of tomato (Solanum lycopersicon) introgression lines (ILs) containing small, molecular marker- defined chromosomal segments from the wild species Solanum pennellii. His approach, which became known as Introgression Breeding, is predicated on the idea that crop domestication may have left behind useful allelic variation. In a publication that has been cited nearly 1,300 times, Eshed and Zamir (1995) argued that some of this variation may be valuable in a modern breeding context and that genetic tools could be developed to identify and introgress that variation into modern cultivars without the disadvantages of using CWRs directly as parents in a breeding program. The approach gained worldwide acclaim and has been attempted in a number of crop species. The resulting progenies from these types of approaches are called Introgression Lines, or ILs. Zamir (2001) later suggested that a genetic infrastructure could be developed based on “exotic libraries” where individual breeding lines or cultivars in the library would contain a marker-defined chromosomal segment from a CWR that had been introgressed through sexual recombination. A full set of lines of this sort would constitute a library of the genome of the CWR, albeit nested inside the genome of cultivated crop accessions. A scientist could obtain lines from the library to screen for traits of interest and potentially identify one or more lines carrying segments with valuable traits. These lines could then be easily introgressed into breeding material or cultivars using the markers flanking the introgression. These ideas were later more fully expanded to consider how this approach could be used to source natural variation for plant breeding programs (Zamir 2008). Zamir’s key insights into the value of allelic variation in CWRs were (1) that there were ways to access their value without using their entire genome as a parent in a breeding program and (2) that the genome of the wild relative could be assembled piece by piece into a library that Dani Zamir 5 was based on a cultivated genetic background. Plant breeders have long been aware of the pitfalls of using CWR as parents, including substantial linkage drag with undesirable traits, introduction of sterility and incompatibility, and limited recombination between wild and cultivated chromosomes. Granted, there are numerous examples of introgressions of important alleles from CWRs into cultivated crops; though these almost always involved substantial backcrossing to the cultivated parent to remove the genome of the wild parent and retain only the small segment associated with the trait of interest. In a number of these cases, unwanted segments of wild species chromosomes remain and are difficult to remove because of limited recombination at or near the unwanted genes of interest. The IL approach circumvents this problem by pre-developing a set of marker-defined ILs and allowing for a more custom-designed breeding approach (Figure 1.2). But of even greater value may be the use of CWRs as a source for valuable quantitative trait locus (QTL) variation. Zamir and his students and colleagues were among the first to propose and demonstrate a practical approach to utilizing the potential of CWRs as sources of important quantitative variation (Zamir 2008). Prior to this time, CWRs were primarily considered as sources of valuable qualitative genetic variants, particularly for traits such as disease resistance. Traits like yield and productivity were considered mainly in the context of cultivated genetic IL8–1 IL6–2 IL6–2–2 IL6–3 IL6–4 IL12–1 12 IL12–1–1 IL12–4 IL11–3 IL11–4 IL11–4–1 F1 IL1–2 IL3–2 IL4–4 IL6–3 IL10–1 IL12–1 IL12–3 IL11–2 IL12–3–1 IL11–1 11 S. lycopersicum cv. M82 S. pennellii IL12–2 IL5–2 IL5–4 IL5–3 IL4–3 IL4–4 IL10–1–1 IL10–1 IL10–2 IL10–3 10 IL10–2–2 IL9–2–5 IL9–2–6 6 IL12–4–1 IL5–1 5 IL5–5 IL4–1–1 4 IL4–3–2 IL4–1 IL4–2 IL3–1 IL3–2 IL3–3 IL3–5 IL9–3 IL9–2 IL9–1–2 IL9–1–3 9 IL9–3–2 IL9–1 IL2–8 IL3–4 IL2–1–1 IL2–5 8 IL9–3–1 IL2–2 3 IL2–3 IL2–4 2 IL2–6–5 IL8–1–5 IL8–1–1 IL8–1 IL8–2 IL8–3 IL8–3–1 IL8–2–1 IL1–1–3 IL1–2 IL1–4–18 IL7–5–5 IL7–5 7 IL7–3 IL7–4–1 IL7–1 IL7–2 IL7–4 IL1–4 IL1–3 IL1–1 1 IL2–1 (b) IL1–1–2 (a) Fig. 1.2. The S. pennellii Introgression Line (IL) population. (a) Genome introgressions in the 76 S. pennellii ILs, which are nearly isogenic to each other and to M82 and differ only for the marked introgressed chromosome segments. (b) Green fruits of the wild species, S. pennellii, the lycopene-rich red fruits of S. lycopersicum, their F1 hybrid and six ILs. Source: D. Zamir. 6 Irwin L. Goldman backgrounds. But an important insight offered by Zamir and colleagues focused on the observation that bottlenecks caused by domestication and modern breeding may have left behind valuable quantitative traits. By going back to CWRs, some of these valuable quantitative traits could be accessed; however, introgressing them carefully into cultivated backgrounds using very precise marker-delineated segments was the key to harnessing their potential. The IL concept provided a framework for how this could be accomplished. More specifically, Eshed et al. (1996) conducted a series of field trials with ILs and their hybrids in two distinct genetic backgrounds. Seven out of 8 hybrids displayed from 7 to 13% higher yield than their near-isogenic controls (without introgressions). This finding demonstrated a significant interaction between the introgression and genetic background for yield in tomato. When the two introgressions with the largest yield advantage were combined into a single genetic background, a 20% yield increase compared to the control was realized. The IL system is used by hundreds of researchers and breeders in academia and industry around the world. It has become the most helpful tool for identifying and introducing beneficial genes into cultivated varieties from their wild relatives. Moreover, the success of the tomato ILs has become a model for the development of similar systems in other agricultural crops (rice, barley, and wheat, for example) in China, Japan, Korea, and other countries. III. CLONING OF QUANTITATIVE TRAIT LOCI Dani Zamir has been among the world pioneers in applying molecular markers for mapping quantitative traits in plants. One of the most important achievements in this area was the first example of cloning and characterization of a QTL, performed by Zamir and his student Eyal Fridman, currently a researcher in Israel’s Volcani Institute. This was the first example of a cloned QTL from any organism. Their efforts identified a QTL for levels of soluble solids, primarily sugars, in tomato fruit that was determined by a variant of the enzyme invertase. The milestone article, published in April 2000 (Fridman et al. 2000), has been one of the most notable achievements of Israeli science in genetics and agriculture. In parallel with Zamir’s work, a QTL gene for fruit size in tomato that segregated in one of the ILs was identified by Steven Tanksley from Cornell University, one of Zamir’s research partners for many years, and this article was published in July 2000 (Frary et al. 2000). Dani Zamir 7 To clone this QTL, Fridman et al. (2000) first identified a moderate QTL known as Brix-9-2-5, which increases sugar yield of tomatoes without compromising yield. This QTL was mapped to a single-nucleotide polymorphism (SNP)-defined region of 484 base pairs within a flower- and fruit-specific cell wall invertase gene (LIN5). LIN5 is considered a “sink gene” that is involved with the unloading of sugars into the fruit. Further QTL analysis with segregating populations from five tomato species localized the functional polymorphism of Brix- 9- 2- 5 to an amino acid near the catalytic site of the invertase crystal, which affects enzyme kinetics and fruit sink strength (Fridman et al. 2004). The work helped demonstrate the relationship between genetic variation at the sequence level and the manifestation of a QTL. This first cloning of an important crop QTL highlighted the value of the IL approach, and the enormous collection of characterized lines, advanced by Zamir and colleagues over many years. IV. CHARACTERIZATION OF GENETIC PHENOMENA Dani Zamir’s commitment to working with tomato extends through five decades, and he is therefore in an enviable position to study and describe the history of tomato genetics and breeding. Working with a large multinational team, Zamir and colleagues examined the modern history of tomato domestication and breeding through the lens of the cumulative genetic information collected by researchers throughout the years (Lin et al.2014). Their work revealed that modern tomato can be partially described by two independent sets of QTLs that conferred important changes to tomato fruit. These QTL, particularly fruit mass QTLs known as fw1.1, fw5.2, fw7.2, fw12.1, and len12.1, are responsible for the large size of modern tomato fruit, which is more than 100× larger than its wild progenitor. They also proposed a two-step evolution of tomato fruit mass through domestication sweeps associated with these QTL. In addition to changes in fruit mass, they reported several QTL on chromosome 5 that confer greater fruit firmness (fir5.1) and higher soluble solids (ssc5.1, ssc5.2, and ssc5.3) were likely selected during the development of processing tomatoes. Processing tomatoes are largely used for the production of tomato paste, which is a staple of processed foods such as ketchup. This genetic signature of processing tomato was facilitated by the presence of a very large centromere on chromosome 5, which likely reduced the amount of recombination present in the region where these QTL reside (Lin et al. 2014) (Figure 1.3). 8 Irwin L. Goldman Fig. 1.3. Dani Zamir with multi-loculed tomato germplasm. Source: Photo credit: M. Schwartz. Among Zamir’s important contributions to agricultural research are his insights into understanding the genetic basis of overdominance (Semel et al. 2006), epistasis (Eshed and Zamir 1995), and heterosis itself (Lippman and Zamir 2007; Lippman et al. 2007; Krieger et al. 2010). For as long as humans have bred plants and animals, they have recognized the phenomenon of hybrid vigor, or heterosis, in which the F1 progeny of a cross exceeds the value of the parents in terms of productivity. Despite the obvious importance of heterosis to global food production, its genetic basis has remained poorly understood; perhaps in part because many loci contribute to yield and productivity traits, and these loci behave in a variety of different ways. In a collaboration with Uri Krieger and Zachary Lippman, Zamir worked out genetic effects at the locus known as SINGLE FLOWER TRUSS (SFT), which codes for a protein that produces the flowering hormone florigen (Lifschitz et al. 2006). Heterosis has been associated with several potential explanations, including the dominance hypothesis, the overdominance hypothesis, and epistasis. The overdominance hypothesis suggests that interaction between alleles at a locus is the cause of hybrid vigor. Identification of a number of examples of putative overdominance have revealed the phenomenon of Dani Zamir 9 pseudo-overdominance, where dominant loci are linked and appear as an overdominant locus. Krieger et al. (2010) examined a tomato mutant, sft-e4537, which displayed overdominant-type heterosis and possessed a missense mutation in the gene SFT. Plants carrying this mutation in the homozygous recessive condition flower very late and their flowering branches quickly revert to vegetative branches. Heterozyogtes display substantial heterosis, derived from a suppression of growth termination mediated by the SELF PRUNING (SP) gene, an antagonist of SFT. This elegant example of a mechanism for overdominance illustrates how this elusive genetic phenomenon is a plausible explanation for heterosis in tomato. That is not to say that all loci behave in this manner, but the confirmation of a truly overdominant locus goes a long way to confirming the truth of one of the most widely held hypotheses of heterosis. Interestingly, this example also confirms the importance of epistasis, one of the three primary hypotheses for heterosis, given that the SFT and SP loci interact in this example. V. SEQUENCING THE TOMATO GENOME Zamir was the leader of the SOL Genome Project, in which the complete DNA sequence of the tomato was deciphered (Tomato Genome Consortium 2012). To this end, Prof. Zamir organized research groups from the United States, the United Kingdom, the Netherlands, Italy, France, India, Korea, and Japan into a group known as the International Tomato Genome Sequencing Project, who worked together to sequence the tomato genome. Zamir was one of the two corresponding authors of the article on the tomato genome published in 2012 in Nature that garnered the issue’s cover and a special feature (Tomato Genome Consortium 2012). This paper has now been cited more than 2,000 times and represents a tremendous multinational effort to sequence the genome of one of our most important crops. The International Tomato Genome Sequencing Project was begun in 2004 by an international consortium of scientists from Korea, China, the United Kingdom, India, the Netherlands, France, Japan, Spain, Italy, and the United States. The group found that tomato genome was highly syntenic with other sequenced solanaceae crops and comprised more low-copy sequences than other crop genomes. They compared the cultivated genome to the related wild species Solanum pimpinellifolium, and the two genomes were divergent for only 0.6% of their nucleotides. However, the cultivated genome was 8% divergent from potato with a number of chromosomal inversions differing between the 10 Irwin L. Goldman two. The researchers found two genome triplications in the history of tomato, one of which is approximately 130 million years ago and the other about 60 million years ago. These large-scale events were key to the diversification of genes for fruit fleshiness and color, particularly the more recent triplication event. As critically important as this international effort was, Zamir’s involvement in the ultimate success of the tomato genome project goes far deeper. Over many decades, Zamir collaborated with Cornell University scientist Steve Tanskley, who played a key role in building the molecular marker linkage map that was used to piece together much of the early information about the tomato genome and the location of traits of interest. Zamir’s career spans the critical period from the early 1980s through the early 2000s which saw the development of molecular markers for plant breeding applications. Beginning with allozyme markers in the 1980s, then restriction fragment length polymorphisms (RFLPs) in the late 1980s and early 1990s, polymerase chain reaction (PCR)-based markers in the 1990s, and finally sequence-based markers in the 2000s, the possibility of associating chromosome segments with some type of molecular marker improved dramatically during this period. High-density molecular marker linkage maps became common by the 1990s and expanded dramatically in the 2000s with sequence-based markers. These developments were greatly facilitated by improvements in genome sequencing, particularly next-generation technologies that became available more recently. In addition, tomato, along with maize and rice, was always among the most well-developed models for marker systems in crops. Zamir was instrumental in the iterative development of marker-based information in tomato, contributing to virtually all of these developments over a period of decades. Marker- based regions were critical to the sequencing effort. Thus, the sequencing of the tomato genome represents one of the more recent successes of Zamir’s collaborations, built piece by piece on a foundation of tomato breeding and genetics knowledge. VI. PRACTICAL PLANT BREEDING Dani Zamir lives up to his principles by being involved in practical breeding. Based on the new methods he had developed, he has bred, together with a seed company he founded, AB Seeds, a processed tomato variety, ‘AB2’, which was a leading variety in California for a number of years. In many ways, this hybrid variety served as practical proof of the principles described by Zamir’s scholarly work. The QTL Dani Zamir 11 for yield in this variety were first identified and described in Zamir’s earlier work (Eshed et al. 1996). Zamir won the Kaye Innovation Award from the Hebrew University for his achievements in applied research based on this development. Over the years, Zamir has collected tomato varieties from all major collections in the world. In the years 2007–2010, he grew more than 5,000 varieties simultaneously on the experimental farms in Acre, Israel, in the framework of the EU consortium EUSOL. He described them all phenotypically and invited the scientific community to examine and use them. Hundreds of scientists from all over the world came to Acre and searched for phenotypes of interest. Likewise, in the early 2000s, Zamir and colleagues performed a large-scale experiment on mutagenesis in the cultivated tomato. After scanning hundreds of thousands of second- generation (F2) plants in the field, hundreds of new mutations were isolated. Each mutation was genetically and phenotypically described, and the results were posted online for the benefit of the entire scientific community. These mutants are available to anyone in the world who requests them. Molecular characterization of these mutations, whether in collaboration with the Zamir lab or by others, is responsible for numerous important discoveries in plant development and metabolism. The results of these efforts have fueled the development of new tomato cultivars and spawned new research projects based on the phenotypic diversity present in the collections (Figures 1.4 and 1.5). Zamir has not limited his activities to tomato. Throughout his career, he has established infrastructure for programs in genomic-based breeding of rose and Lisianthus in the Faculty of Agriculture. He assembled an extensive collection of rose varieties and added additional researchers from the Faculty of Agriculture to a long-term project in which these varieties are being characterized genetically and metabolically. These efforts are particularly important given the loss of public sector breeding programs in recent decades. Establishment of new breeding programs is a way to re-energize public breeding programs in horticultural crops that have been neglected, perhaps because of the difficulty in finding funding to support them. Marker-assisted selection has been used extensively for many plant breeding applications, including introgressing chromosomal segments from wild species. Because small segments can be defined by marker- linked regions, it may be possible to reduce the linkage drag associated with less desirable traits. A number of examples of wild species introgressions in rice and tomato have led to improved agronomic performance and new cultivars. Marker- linked Solanum pennellii introgressions backcrossed into cultivated tomato by Zamir and 12 Fig. 1.4. Irwin L. Goldman AB1 tomato cultivar. Source: Photo credit: D. Zamir. colleagues led to the incorporation of the QTL Brix-9-2-5, which conferred higher levels of soluble solids in processing tomatoes (Lippman et al. 2007). Zamir’s company AB Seeds, based in Israel, used this introgression to develop the processing tomato cultivar ‘AB2’, which was widely grown in California’s tomato processing industry (Vogel 2014). The success of this approach combines the power of the IL concept pioneered by Eshed and Zamir with pyramiding of genes for traits of interest. Sacco et al. (2013) showed how introgressions from S. pennellii carrying useful QTL could be pyramided in a single genotype. In their study, QTL controlling ascorbic acid, phenol composition, and soluble solids were introgressed into a recurrent parent and stabilized in the homozygous condition. Zamir has also argued for a more thoughtful and comprehensive database of crop phenotypes, which can be used to improve crops in the future. Zamir’s work to develop large collections of tomato genotypes Dani Zamir 13 Fig. 1.5. Field trials of tomato germplasm in Israel. Source: Photo credit: D. Zamir. described earlier, including mutants, and make them available to the scientific community, is an example of his interest in preserving phenotypic information. In a landmark paper in PLoS Biology in 2013 (Zamir 2013), he advocates for an online system that is capable of storing, managing, and retrieving data related to crop phenotypes and their genotypes. This would take advantage of prior work in phenotyping, which is largely lost as individual scientists retire or stop their projects for other reasons. A public repository would advance the collective effort, as it would preserve unique phenotypes in a catalog that could be retrieved by any worker interested in that crop. It is perhaps this emphasis that led Zamir and his former student Yaniv Semel to develop Phenome Networks, an Israeli company that has built proprietary software for managing the complex data stream necessary for modern breeding programs. The software helps the breeder manage phenotypic and genotypic data, as well as pedigrees and trial information. VII. SCIENTIFIC IMPACT Dani Zamir’s scientific influence on crop breeding and genetics is reflected in the large number of citations his publications have received – over 34,000 citations to date in scientific journals (Google Scholar, 14 Irwin L. Goldman https://scholar.google.com/ 2021), which is an extraordinary number in the field of plant breeding. This is also reflected in his high h-index, measured at 95. The h-index is a measure of the degree to which an author is cited by others, and demonstrates the impact of Zamir’s work in the research community. The paper with the largest number of citations from Zamir’s work, in addition to the tomato genome sequence paper which has more than 2,000 citations, is the IL concept of Eshed and Zamir (1995) which has nearly 1,300 citations. In addition, Zamir is a co-author on 15 publications that have more than 500 citations each, a truly remarkable accomplishment. For 35 years, Prof. Zamir taught the introductory course in genetics to students of the Faculty of Agriculture at Hebrew University in Rehovot, Israel. It is likely that he personally instructed more than 9,000 students during this period. Zamir has mentored generations of graduate students, including 17 MS students, 20 PhD students, and 8 postdoctoral fellows, most of whom continue to pursue genetics and plant breeding research. Several of his students continue in academic and applied research at the leading universities in Israel and abroad. Many of his students are involved in breeding in seed companies. Prof. Zamir is an avid and dedicated s upporter of teaching and education in applied genetics and has published an important article on this subject (Fridman and Zamir 2012). Dani Zamir is a decorated scientist, academic, plant breeder, entrepreneur, and mentor. His career stands as an outstanding example of how a sustained focus on a particular species, coupled with persistence and insight, can lead to dramatic advancements in science and technology. When Zamir began his career in plant breeding in the 1970s, we may not have predicted that specific chromosome segments from tomato’s wild relatives would play such an important role in the improvement of quantitative traits. Likewise, we may not have predicted that tools would become available to clone these genes or to dissect the genetic basis of some of the most perplexing phenomena in crop genetics. Dani Zamir’s work has encompassed all of these achievements. By any measure, Zamir’s career has been an unqualified success. He is recognized not only for the knowledge he has helped to uncover, but for the efforts to organize the community to harness their resources toward improvement of the tomato. VIII. LIST OF SCIENTIFIC JOURNAL PUBLICATIONS OF DANI ZAMIR 1. Zamir, D., R.A. Jones, and N. Kedar. 1980. Anther culture of male sterile Lycopersicon esculentum mutants. Plant Sci. Lett. 17:353–361. Dani Zamir 15 2. Zamir, D., S.D. Tanksley, and R.A. Jones. 1981. Genetic analysis of the origin of plants regenerated from anther tissues of Lycopersicon esculentum. Plant Sci. Lett. 21:121–127. 3. Zamir, D., S.D. Tanksley, and R.A. Jones. 1981. Low temperature effect on selective fertilization of pollen mixtures of wild and cultivated tomato species. Theor. Appl. Genet. 59:235–238. 4. Tanksley, S.D., D. Zamir, and C.M. Rick. 1981. Evidence for extensive overlap in sporophytic and gametophytic gene expression in Lycopersicon esculentum. Science 213:453–455. 5. Zamir, D., S.D. Tanksley, and R.A. Jones. 1982. Haploid selection for low temperature tolerance of tomato pollen. Genetics 101:129–137. 6. Palmer, J.D., and D. Zamir. 1982. Chloroplast DNA evolution and phylogenetic relationships in Lycopersicon. Proc. Natl. Acad. Sci. U.S.A. 79:5006–5010. 7. Zamir, D. 1983. Pollen irradiation in tomato: minor effects on enzymic gene transfer. Theor. Appl. Genet. 66:147–151. 8. Zamir, D., and G. Ladizinsky. 1984. Genetics of allozyme variants in lentil. Euphytica 33:329–336. 9. Zamir, D., N. Navot, and J. Rudich. 1984. Enzyme polymorphism in Citrullus lanatus and C. colocynthis in Israel and Sinai. Plant Syst. Evol. 146:163–170. 10. Zamir, D., T. Ben- David, and J. Rudich. 1984. Frequency distributions and linkage relationships of 2-tridecadone in interspecific segregating generations of tomato. Euphytica 33:481–488. 11. Miltau, O., D. Zamir, and J. Rudich. 1984. Breeding for chilling tolerance in tomato: an examination of selection criteria. Eucarpia 9:45–50. 12. Zamir, D., and I. Chet. 1985. Electrophoretic patterns of soluble enzymes in Trichoderma viride. Can. J. Microbiol. 31:578–580. 13. Goldring, A., D. Zamir, and Ch. Degani. 1985. Duplicated phosphoglucose isomerase genes in acocado. Theor. Appl. Genet. 71:491–494. 14. Perl-Treves, R., D. Zamir, N. Navot, and E. Galun. 1985. Phylogeny of Cucumis based on isozyme variability and its comparison with the plastom phylogeny. Theor. Appl. Genet. 71:430–436. 15. Pinkas, R., D. Zamir, and G. Ladizinsky. 1985. Allozyme divergence and evolution in the genus Lens. Plant. Syst. Evol. 151:131–140. 16. Miltau, O., D. Zamir, and J. Rudich. 1985. Growth rates of Lycopersicon species at low temperatures. Z. Pflanzenzuchtg. 96:193–199. 17. Navot, N., and D. Zamir. 1986. Linkage relationships of 19 protein coding genes in watermelon. Theor. Appl. Genet. 72:274–278. 16 Irwin L. Goldman 18. Zamir, D. and Y. Tadmor. 1986. Unequal segregation of nuclear genes in plants. Bot. Gaz. 147:355–358. 19. Zamir, D., and M. Tal. 1987. Genetic analysis of sodium, potassium and chloride in an interspecific Lycopersicon cross. Euphytica 36:187–191. 20. Gadish, I., and D. Zamir. 1987. Differential zygotic abortion abortion in an interspecific Lycopersicon cross. Genome 29:156–159. 21. Navot, N., and D. Zamir. 1987. Isozyme and seed protein phylogeny of the genus Citrullus (Cucurbitaceae). Plant Syst. Evol. 156:61–67. 22. Tadmor, Y., D. Zamir, and G. Ladizinsky. 1987. Genetic mapping of an ancient translocation in the genus Lens. Theor. Appl. Genet. 73:883–892. 23. Zamir, D., and I. Gadish. 1987. Pollen selection for low temperature adaptation in tomato. Theor. Appl. Genet. 74:545–548. 24. Czosnek, H., R. Ber, Y. Antignus, S. Cohen, and D. Zamir. 1988 Isolation of the tomato yellow leaf curl virus – a gemini virus. Phytopathology 78:508–512. 25. Czosnek, H., R. Ber, N. Navot, D. Zamir, Y. Antignus, and S. Cohen. 1988. Detection of tomato yellow leaf curl virus in lysates of plants and insects by hybridization with viral DNA probe. Plant Dis. 72:949–591. 26. Tanksley, S.D., and D. Zamir. 1988. Double tagging of a male sterile gene in tomato using morphological and enzymic marker genes. Hort Sci. 23:387–388. 27. Young, N.D., D. Zamir, M. Ganal, and S.D. Tanksley. 1988. Use of isogenic lines and simultaneous probing to identify DNA markers tightly linked to the Tm-2a gene in tomato. Genetics 120:579–585. 28. Zamir, D., and S.D. Tanksley. 1988. Tomato genome is comprised largely of fast evolving, low copy number sequences. Mol. Gen. Genet. 213:254–261. 29. Czosnek, H., R. Ber, N. Navot, Y. Antignus, S. Cohen, and D. Zamir, 1989. Tomato yellow leaf curl virus DNA forms in the viral capsid, in infected plants and in the insect vector. J. Phytopathol. 125:47–54. 30. Sarfatti, M., J. Katan, R. Fluhr, and D. Zamir. 1989. An RFLP marker in tomato linked to the Fusarium oxysporum resistance gene I2. Theor. Appl. Genet. 78:755–759. 31. Navot, N., M. Sarfatti, and D. Zamir. 1990. Linkage relationships of genes affecting bitterness and flesh color in watermelon. J. Hered. 81:162–165. 32. Kagan-Zur, V., Y. Mizrahi, D. Zamir, and N. Navot. 1990. A tomato triploid hybrid whose double genome parent is the male. J. Am. Soc. Hortic. Sci. 116:342–345. Dani Zamir 17 33. Zakay, Y., N. Navot, M. Zeidan, N. Kedar, H.D. Rabinowitch, H. Czosnek, and D. Zamir. 1990. Screening Lycopersicon accessions for resistance to the tomato yellow leaf curl virus: presence of viral DNA and symptom development. Plant Dis. 75:279–281. 34. Perl-Treves, R., M. Abu-Abied, N. Magal, E. Galun, and D. Zamir. 1990. Genetic mapping of tomato cDNA clones encoding the c hloroplastic and cytosolic isozymes of superoxide dismutase. Biochem. Genet. 28:543–552. 35. Katan, T., D. Zamir, M. Sarfatti, and J. Katan. 1991. Vegetative compatibility groups and sub-groups in Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathology 81:255–262. 36. Paterson, A.H., S. Damon, J.D. Hewitt, D. Zamir, H.D. Rabinowitch, S.E. Lincoln, E.S. Lander, and S.D. Tanksley. 1991. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations and environments. Genetics 127:181–197. 37. Ber, R., N. Navot, D. Zamir, Y. Antignus, S. Cohen, and H. Czosnek. 1991. Infection of tomato by the tomato yellow leaf curl virus: susceptibility to infection, symptom development and accumulation of viral DNA. Arch Virol. 112:169–180. 38. Pnueli, L., M. Abu-Abeid, D. Zamir, Zs. Schwarz-Sommer, and E. Lifschitz. 1991. Members of a new gene family in tomato are temporarily expressed during flower development and their domains share a common ancestor with the homeotic genes from Antirrhinum and Arabidopsis. Plant J. 1:255–266. 39. Behare, J., H. Laterrot, M. Sarfatti, and D. Zamir. 1991. RFLP mapping of the Stemphylium resistance gene in tomato. Mol. Plant- Microbe Int. 4:489–492. 40. Sarfatti, M., M. Abu-Abied, J. Katan, and D. Zamir. 1991. RFLP mapping of I1, a new locus in tomato conferring resistance against Fusarium oxysporum f. sp. lycopersici race 1. Theor. Appl. Genet. 82:22–26. 41. Navot, N., E. Pichersky, M. Zeidan, D. Zamir, and H. Czosnek. 1991. Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185:151–161. 42. Saranga, Y., A. Marani, D. Zamir, and J. Rudich. 1991 Breeding tomatoes for salt tolerance: field screening of Lycopersicon accessions for yield and dry matter production. J. Am. Soc. Hort. Sci. 116:1067–1161. 43. Segal, G., M. Sarfatti, M.A. Chaffer, N. Ori, D. Zamir, and R. Fluhr. 1992. Genetic and physical correlation in the region surrounding the I2 Fusarium oxysporum resistance locus in tomato. Mol. Gen. Genet. 231:179–185. 18 Irwin L. Goldman 44. Navot, N., M. Zeidan, E. Pichersky, D. Zamir, and H. Czosnek. 1992. Use of polymerase chain reaction to amplify tomato yellow leaf curl virus DNA from infected plants and viruliferous whiteflies. Phytopathology 82:1199–1202. 45. Eshed, Y., M. Abu-Abied, Y. Saranga, and D. Zamir. 1992. Lycopersicon esculentum lines containing small overlapping introgressions from L. pennellii. Theor. Appl. Genet. 83:1027–1034. 46. Saranga, Y., A. Cahaner, D. Zamir, A. Marani, and J. Rudich. 1992. Breeding tomatoes for salt tolerance: inheritance of salt tolerance and related traits in interspecific populations. Theor. Appl. Genet. 84:390–396. 47. Saranga, Y., D. Zamir, A. Marani, and J. Rudich. 1993. Breeding tomatoes for salt tolerance: variations in ions concentration associated with response to salinity. J. Am. Soc. Hortic. Sci. 118:405–408. 48. Elias, K.S., D. Zamir, T. Lichtman- Pleban, and T. Katan. 1993. Population structure of Fusarium oxysporum f. sp. lycopersici: restriction fragment length polymorphisms provide genetic evidence that vegetative compatibility group is an indicator of evolutionary origin. Mol. Plant-Microbe Int. 6:565–572. 49. Czosnek, H., B. Gronenborn, E. Remetz, M. Zeidan, N. Navot, H.D. Rabinowitch, S. Vidavsky, N. Kedar, Y. Gafni, T. Zur-Kunik, and D. Zamir. 1993. Replication of tomato yellow leaf curl virus DNA in agroinoculated leaf discs from various tomato genotypes. Plant Mol. Biol. 22:995–1005. 50. Zamir, D.,I. Ekstein-Michelson, Y. Zakay, N. Navot, M. Zeidan, M. Sarfatti, Y. Eshed, E. Harel, T. Pleban, H. Van-Oss,N. Kedar, H. Rabinowitch, and H. Czosnek. 1994. Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, TY-1. Theor. Appl. Genet. 88:141–146. 51. Kunik, T., R. Salomon, Y. Gafni, N. Navot, M. Zeidan, I. Michelson, D. Zamir, and H. Czosnek. 1994. Transgenic tomato plants expressing the tomato yellow leaf curl virus capsid protein are resistant to the virus. Nat. Biotechnol. 12:500–504. 52. Michelson, I., D. Zamir, and H. Czosnek. 1994. Impaired replication and translocation of tomato yellow leaf curl virus (TYLCV) in a tomato (Lycopersicon esculentum) breeding line containing the L. chilense TYLCV tolerance gene Ty-1. Phytopathology 84:928–933. 53. Eshed, Y., and D. Zamir. 1994. Introgressions from Lycopersicon pennellii can improve the soluble-solids yield of tomato hybrids. Theor. Appl. Genet. 88:891–897. 54. Eshed, Y., and D. Zamir. 1994. A genomic library of Lycopersicon pennelliiin L. esculentum:a tool for fine mapping of genes. Euphytica 79:175–179. Dani Zamir 19 55. Ori, N., I. Paran, D. Aviv, Y. Eshed, S.D. Tanksley, D. Zamir, and R. Fluhr. 1994. A genomic search for the gene conferring resistance to Fusarium wilt in tomato. Euphytica 79:201–204. 56. Paran, I., M. Horowitz, D. Zamir, and S. Wolf. 1994. Purity determination of tomato hybrids using RAPD markers. HortScience 30:377. 57. Czosnek, H., M. Zeidan, I. Ekstein, T. Zur-Kunik, Y. Gafni, B. Gronenborn, and D. Zamir. 1995. Tomato yellow leaf curl virus, a gemini-virus with a single genomic component: molecular analysis of infection and new ways for tomato protection. Acta Hortic. 377:251–257. 58. Paran, I., I. Goldman, S.D. Tanksley, and D. Zamir. 1995. Recombinant inbred lines for genetic mapping in tomato. Theor. Appl. Genet. 90:542–548. 59. Goldman, I., I. Paran, and D. Zamir. 1995. Quantitative trait locus analysis of a recombinant inbred line population derived from Lycopersicon esculentum × Lycopersicon cheesmanii cross. Theor. Appl. Genet. 90:925–932. 60. Eshed, Y., and D. Zamir. 1995. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield associated QTL. Genetics 141:1147–1162. 61. Tanksley, S.D., S. Grandillo, T.M. Fulton, D. Zamir, Y. Eshed, V. Petiard, J. Lopez, and T. Beck-Bunn. 1996. Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor. Appl. Genet. 92:213–224. 62. Eshed, Y., G. Gera, and D. Zamir. 1996. A genome-wide search for wild-species alleles that increase horticultural yield of processing tomatoes.Theor. Appl. Genet. 93:877–886. 63. Eshed, Y., and D. Zamir. 1996. Less than additive epistatic interactions of QTL in tomato. Genetics 143:1807–1817. 64. Ori, N., Y. Eshed, P. Pinto, I. Paran, D. Zamir, and R. Fluhr. 1997. TAO-1 a representative of the molybdenum cofactor containing hydroxylases from tomato. J. Biol. Chem. 272:1019–1025. 65. Paran, I., I. Goldman, and D. Zamir. 1997. QTL analysis of morphological traits in tomato recombinant inbred line population. Genome 40:242–248. 66. Michelson, I., M. Zeidan, E. Zamski, D. Zamir, and H. Czosnek. 1997. Localization of tomato yellow leaf curl virus (TYLCV) in susceptible and tolerant nearly isogenic tomato lines. Acta Hortic. 477:407–414. 67. Ori, N., Y. Eshed, I. Paran, G. Presting, D. Aviv, S. Tanksley, D. Zamir, and R. Fluhr. 1997. The I2C family from the wilt disease resistance locus belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell 9:521–532. 20 Irwin L. Goldman 68. Fulton, T.M., T. Beck- Bunn, D. Emmatty, Y. Eshed, J. Lopez, J. Uhlig, D. Zamir. and S.D. Tanksley. 1997. QTL analysis of an advanced backcross of Lycopersicon peruvianum to the cultivated tomato and comparison of QTLs found in other wild species. Theor. Appl. Genet. 95:881–894. 69. Tanksley, S.D., D. Bernachi, T. Beck-Bunn, D. Emmatty, Y. Eshed, S. Inai, J. Lopez, V. Petiard, H. Sayama, J. Uhlig, and D. Zamir. 1997. Evaluations of yield and quality on a pair of processing tomato inbreds nearly isogenic for the Tm2a gene for resistance to the tobacco mosaic virus. Euphytica 99:77–83. 70. Parnis, A., O. Cohen, T. Gutfinger, D. Hareven, D. Zamir, and E. Lifschitz. 1997. Two different developmental mutants of tomato, Mouse-ear and Curl, are associated with two distinct modes of abnormal transcriptional regulation of a knotted gene. Plant Cell 9:2143–2158. 71. Bernacchi, D., T. Beck-Bunn, Y. Eshed, S. Inai, J. Lopez, V. Petiard, J. Uhlig, D. Zamir, and S.D. Tanksley. 1997. Advanced backcross QTL analysis of tomato: I. Identification of QTL for traits of agronomic importance from Lycopersicon hirsutum. Theor. Appl. Genet. 97:381–397. 72. Bernacchi, D., T. Beck-Bunn,D. Emmaty, Y. Eshed, S. Inai, J. Lopez, V. Petiard, J. Uhlig, D. Zamir, and S.D. Tanksley. 1997. Advanced backcross QTL analysis of tomato: evaluation of near- isogenic lines carrying single donor introgressions for desirable wild QTL alleles derived from Lycopersicon hirsutum and L. pimpinellifolium. Theor. Appl. Genet. 97:170–180. 73. Pnueli, L., L. Carmel-Goren, D. Hareven, T. Gutfinger, J. Alvarez, M. Ganal, D. Zamir, and E. Lifschitz. 1998. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989. 74. Grandillo, S., D. Zamir, and S.D. Tanksley. 1999. Genetic improvement of processing tomatoes: a twenty-year perspective. Euphytica 110:85–97. 75. Diwan, N., R. Fluhr, Y. Eshed, D. Zamir, and S.D. Tanksley. 1999. Mapping of Ve in tomato: a gene conferring resistance to the broad spectrum pathogen, Verticillium dahliae race 1. Theor. Appl. Genet. 98:315–319. 76. Zamir, D., S. Grandillo, and S.D. Tanksley. 1999. Genes from wild species for the improvement of yield and quality of processing tomatoes. Acta Hortic. 487:285–288. 77. Ronen, G., M. Cohen, D. Zamir, and J. Hirschberg. 1999. R egulation of carotenoids biosynthesis during tomato fruit development: Dani Zamir 21 expression of the gene lycopene epsilon cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J. 17:341–352. 78. Ron, M., R. Kantety, G.B. Martin, N. Avidan, Y. Eshed, D. Zamir, and A. Avni. 2000. High resolution linkage analysis and physical characterization of the EIX- responding locus in tomato. Theor. Appl. Genet. 100:184–189. 79. Qilin, P., L. Yong-Sheng, O. Budai-Hadrian, M. Sela, L. Carmel- Goren, D. Zamir, and R. Fluhr. 2000. Comparative genetics of NBS-LRR resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322. 80. Fridman, E., T. Pleban, and D. Zamir. 2000. A recombination hotspot delimits a wild species QTL for tomato sugar content to 484- bp within an invertase gene. Proc. Natl. Acad. Sci. U.S.A. 97:4718–4723. 81. Fulton, T.M., S. Grandillo, T. Beck-Bunn, E. Fridman, A. Frampton, J. Lopez, V. Petiard, J. Uhlig, D. Zamir, and S.D. Tanksley. 2000. Advan ced backcross analysis of Lycopersicon esculentum × L. parviflorum cross. Theor. Appl. Genet. 100:1025–1042. 82. Ronen, G., L. Carmel-Goren, D. Zamir, and J. Hirschberg. 2000. An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta (B) and old-gold (og) color mutations in tomato. Proc. Natl. Acad. Sci. U.S.A. 97:11102–11107. 83. Monforte, A.J., E. Friedman, D. Zamir, and S.D. Tanksley. 2001. Comparison of a set of allelic QTL- NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm utilization. Theor. Appl. Genet. 102:572–590. 84. Sela, M., O. Budai-Hadrian, P. Qilin, L. Carmel-Goren, R. Vunsch, D. Zamir, and R. Fluhr. 2001. Genome-wide analysis for Fusarium resistance in tomato reveals multiple complex loci. Mol. Genet. Genom. 265:1104–1111. 85. Zamir, D. 2001. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2:983–989. 86. Fridman, E., Y.S. Liu, L. Carmel- Goren, A. Gur, M. Shoresh, T. Pleban, Y. Eshed, and D. Zamir. 2002. Two tightly linked QTLs modify tomato sugar content via different physiological pathways. Mol. Genet. Genom. 266:821–826. 87. Isaacson, T., G. Ronen, D. Zamir, and J. Hirschberg. 2002. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for production of carotene and xanthophylls in plants. Plant Cell 14:333–342. 88. Tadmor, Y., E. Fridman, A. Gur, O. Larkov, U. Ravid, D. Zamir, and E. Lewinsohn. 2002. Identification of malodorous, a wild species 22 Irwin L. Goldman allele affecting tomato aroma that was selected against during domestication. J. Agric. Food Chem.50:2005–2009. 89. Guterman, I., M. Dafny-Yelin, M. Shalit, M. Emanuel, N. Shaham, D. Piestun, A. Zuker, M. Ovadis, M. Lavy, N. Lavid, E. Lewinsohn, E. Pichersky, A. Vainstein, D. Zamir, Z. Adam, D. Weiss. 2002. An integrated genomic approach to discovering fragrance-related genes in rose petals. Flowering Newsletter 32:31–37. 90. Lavid, N., J. Wang, M. Shalit, I. Guterman, E. Bar, T. Beuerle, N. Menda, S. Shafir, D. Zamir, Z. Adam, A. Vainstein, D. Weiss, E. Pichersky, and E. Lewinsohn. 2002. O-methyltransferases involved in the biosynthesis of volatile phenolic derivatives in rose petals. Plant Physiol. 129:1899–1907. 91. Guterman, I., M. Shalit, N. Menda, D. Piestun, M. Dafny-Yelin, G. Shalev, O. Davydov, M. Ovadis, M. Emanuel, J. Wang, Z. Adam, E. Pichersky, E. Lewinsohn, D. Zamir, A. Vainstein, and D. Weiss. 2002. Rose scent: genomic approach to discover novel floral fragrance-related genes. Plant Cell 14:2325–2338. 92. Shalit, M., I. Guterman, H. Volpin, E. Bar, T. Tamari, N. Menda, Z. Adam, D. Zamir, A. Vainstein, D. Weiss, E. Pichersky, and E. Lewinsohn. 2003. Volatile ester formation in roses: identification of an acetyl-CoA: geraniol/citronellol acetyltransferase in developing rose petals. Plant Physiol. 131: 1868–1876. 93. Fridman, E., and D. Zamir. 2003. Functional divergence of a syntenic gene family in tomato, potato and Arabidopsis. Plant Physiol. 131:603–609. 94. Carmel-Goren, L., Y.S. Liu, E. Lifschitz, and D. Zamir. 2003. 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