Septoria and St agonospora Diseases of Cereals: A Compilation of Global Research M. van Ginkel, A. McNab, and J. Krupinsky, editors Septoria and Stagonospora Diseases of Cereals: A Compilation of Global Research Proceedings of the Fifth International Septoria Workshop September 20-24, 1999 CIMMYT, Mexico M. van Ginkel, A. McNab, and J. Krupinsky, editors Dedicated to the memory of Dr. Zahir Eyal ii The Organizing Committee expresses it sincere thanks to the Workshop Sponsors: Bayer de México, S.A., and Zeneca Mexicana, S.A. CIMMYT (www.cimmyt.mx or www.cimmyt.cgiar.org) is an internationally funded, nonprofit scientific research and training organization. Headquartered in Mexico, the Center works with agricultural research institutions worldwide to improve the productivity, profitability, and sustainability of maize and wheat systems for poor farmers in developing countries. It is one of 16 similar centers supported by the Consultative Group on International Agricultural Research (CGIAR). The CGIAR comprises over 55 partner countries, international and regional organizations, and private foundations. It is co-sponsored by the Food and Agriculture Organization (FAO) of the United Nations, the International Bank for Reconstruction and Development (World Bank), the United Nations Development Programme (UNDP), and the United Nations Environment Programme (UNEP). Financial support for CIMMYT’s research agenda also comes from many other sources, including foundations, development banks, and public and private agencies. CIMMYT supports Future Harvest, a public awareness campaign that builds understanding about the importance of agricultural issues and international agricultural research. Future Harvest links respected research institutions, influential public figures, and leading agricultural scientists to underscore the wider social benefits of improved agriculture—peace, prosperity, environmental renewal, health, and the alleviation of human suffering (www.futureharvest.org). © International Maize and Wheat Improvement Center (CIMMYT) 1999. Responsibility for this publication rests solely with CIMMYT. The designations employed in the presentation of material in this publication do not imply the expressions of any opinion whatsoever on the part of CIMMYT or contributory organizations concerning the legal status of any country, territory, city, or area, or of its authorities, or concerning the delimitation of its frontiers or boundaries. Printed in Mexico. Correct citation: van Ginkel, M., A. McNab, and J. Krupinsky, eds. 1999. Septoria and Stagonospora Diseases of Cereals: A Compilation of Global Research. Mexico, D.F.: CIMMYT. ISBN: 970-648-035-8 AGROVOC descriptors: Wheats; Triticum; Triticum aestivum; Soft wheat; Triticum durum; Hard wheat; Winter crops; Plant diseases; Fungal diseases; Septoria; Stagonospora; Blotches; Mycosphaerella; Epidemiology; Plant breeding; Selection; Disease resistance; Genetic control; Gene location; Cultural control; Plant response; Research projects Additional Keywords: Triticum tauschii AGRIS category codes: H20 Plant Diseases F30 Plant Genetics and Breeding Dewey decimal classification: 632.4 Additional information on CIMMYT is available on the WorldWideWeb at: www.cimmyt.cgiar.org. iii Table of Contents vi In Memoriam, Dr. Zahir Eyal vii Foreword 1 Opening remarks 1 Historical Aspects and Future Challenges of an International Wheat Program S. Rajaram 19 Session 1: Pathogen Biology 19 Biology of the Septoria/Stagonospora Pathogens: An Overview A.L. Scharen 23 Molecular Analysis of a DNA Fingerprint Probe from Mycosphaerella graminicola S.B. Goodwin and J.R. Cavaletto 26 Characterization of Septoria tritici Variants and PCR Assay for Detecting Stagonospora nodorum and Septoria tritici in Wheat S. Hamza, M. Medini, T. Sassi, S. Abdennour, M. Rouassi, A.B. Salah, M. Cherif, R. Strange, and M. Harrabi 32 Populations of Septoria spp. Affecting Winter Wheat in the Forest-Steppe Zone of the Ukraine S. Kolomiets 34 Septoria passerinii Closely Related to the Wheat Pathogen Mycosphaerella graminicola S.B. Goodwin and V.L. Zismann 37 Septoria/Stagonospora Leaf Spot Diseases on Barley in North Dakota, USA J.M. Krupinsky and B.J. Steffenson (poster) 39 Interrelations among Septoria tritici Isolates of Varying Virulence S. Ezrati, S. Schuster, A. Eshel, and Z. Eyal (poster) 41 Session 2: The Infection Process 41 Stagonospora and Septoria Pathogens of Cereals: The Infection Process B.M. Cunfer 46 Aggressiveness of Phaeosphaeria nodorum Isolates and Their In Vitro Secretion of Cell-Wall- Degrading Enzymes P. Halama, F. Lalaoui, V. Dumortier, and B. Paul 50 Growth of Stagonospora nodorum Lesions A.M. Djurle (poster) 51 Session 3A: Host-Parasite Interactions 51 Genetic Control of Avirulence in Mycosphaerella graminicola (Anamorph Septoria tritici) G.H.J. Kema and E.C.P. Verstappen 53 Cytogenetics of Resistance of Wheat to Septoria Tritici Leaf Blotch L.S. Arraiano, A.J. Worland, and J.K.M. Brown 54 A Possible Gene-for-Gene Relationship for Septoria Tritici Leaf Blotch Resistance in Wheat P.A. Brading, G.H.J. Kema, and J.K.M. Brown 56 Diallel Analysis of Septoria Tritici Blotch Resistance in Winter Wheat X. Zhang, S.D. Haley, and Y. Jin 59 Analysis of the Septoria Monitoring Nursery L. Gilchrist, C. Velazquez, and J. Crossa 63 Session 3B: Host Parasite Interactions 63 Host – Parasite Interactions: Stagonospora nodorum E. Arseniuk and P.C. Czembor 71 Identification of a Molecular Marker Linked to Septoria Nodorum Blotch Resistance in Triticum tauschii Using F2 Bulked Segregant N.E.A. Murphy, R. Loughman, R. Wilson, E.S. Lagudah, R. Appels, and M.G.K. Jones 74 Inheritance of Septoria Nodorum Blotch Resistance in a Triticum tauschii Accession Controlled by a Single Gene N.E.A. Murphy, R. Loughman, R. Wilson, E.S. Lagudah, R. Appels, and M.G.K. Jones 77 Session 4: Population Dynamics 77 Population Genetics of Mycosphaerella graminicola and Phaeosphaeria nodorum B.A. McDonald, C.C. Mundt, and J. Zhan 83 Characterization of Less Aggressive Stagonospora nodorum Isolates from Wheat E. Arseniuk, H.S. Tsang, J.M. Krupinsky, and P.P. Ueng 85 A Vertically Resistant Wheat Selects for Specifically Adapted Mycosphaerella graminicola Strains C. Cowger, C.C. Mundt, and M.E. Hoffer iv 87 Genetic Variability in a Collection of Stagonospora nodorum Isolates from Western Australia N.E.A. Murphy, R. Loughman, E.S. Lagudah, R. Appels, and M.G.K. Jones 90 Mating Type-Specific PCR Primers for Stagonospora nodorum Field Studies R.S. Bennett, S.-H. Yun, T.Y. Lee, B.G. Turgeon, B. Cunfer, E. Arseniuk, and G.C. Bergstrom (poster) 93 Session 5: Epidemiology 93 Epidemiology of Mycosphaerella graminicola and Phaeosphaeria nodorum: An Overview M.W. Shaw 98 Spore Dispersal of Leaf Blotch Pathogens of Wheat (Mycosphaerella graminicola and Septoria tritici) C.A. Cordo, M.R. Simón, A.E. Perelló, and H.E. Alippi 102 Epidemiology of Seedborne Stagonospora nodorum: A Case Study on New York Winter Wheat D.A. Shah and G.C. Bergstrom 108 Sessions 6A and 6B: Cultural Practices and Disease Management 108 Influence of Cultural Practices on Septoria/Stagonospora Diseases J.M. Krupinsky 111 Disease Management Using Varietal Mixtures C.C. Mundt, C. Cowger, and M.E. Hoffer 117 Session 6C: Breeding for Disease Resistance 117 Breeding for Resistance to the Septoria/Stagonospora Blights of Wheat M. van Ginkel and S. Rajaram 127 Breeding for Resistance to Septoria and Stagonospora Blotches in Winter Wheat in the United States G. Shaner 131 Septoria tritici Resistance of Wheat Cultivars at Different Growth Stages M. Díaz de Ackermann, M.M. Kohli, and V. Ibañez 134 Septoria tritici Resistance Sources and Breeding Progress at CIMMYT, 1970-99 L. Gilchrist, B. Gomez, R. Gonzalez, S. Fuentes, A. Mujeeb-Kazi, W. Pfeiffer, S. Rajaram, R. Rodriguez, B. Skovmand, M. van Ginkel, and C. Velazquez (Field presentation) 140 Selecting Wheat for Resistance to Septoria/Stagonospora in Patzcuaro, Michoacan, Mexico R.M. Gonzalez I., S. Rajaram, and M. van Ginkel 145 Varieties and Advanced Lines Resistant to Septoria Diseases of Wheat in Western Australia R. Loughman, R.E. Wilson, I.M. Goss, D.T. Foster, and N.E.A. Murphy 148 Field Resistance of Wheat to Septoria Tritici Leaf Blotch, and Interactions with Mycosphaerella graminicola Isolates J.K.M. Brown, G.H.J. Kema, H.-R. Forrer, E.C.P. Verstappen, L.S. Arraiano, P.A. Brading, E.M. Foster, A. Hecker, and E. Jenny 150 Using Precise Genetic Stocks to Investigate the Control of Stagonospora nodorum Resistance in Wheat C.M. Ellerbrook, V. Korzun, and A.J. Worland (poster) 154 Evaluating Triticum durum x Triticum tauschii Germplasm for Resistance to Stagonospora nodorum L.R. Nelson and M.E. Sorrells (poster) 156 Sources of Resistance to Septoria passerinii in Hordeum vulgare and H. vulgare subsp. spontaneum H. Toubia-Rahme and B.J. Steffenson (poster) 159 Soft Red Winter Wheat with Resistance to Stagonospora nodorum and Other Foliar Pathogens B.M. Cunfer and J.W. Johnson (poster) 160 Partial Resistance to Stagonospora nodorum in Wheat C.G. Du, L.R. Nelson, and M.E. McDaniel (poster) 163 Comparison of Methods of Screening for Stagonospora nodorum Resistance in Winter Wheat D.E. Fraser, J.P. Murphy, and S. Leath (poster) 167 Response of Winter Wheat Genotypes to Artificial Inoculation with Several Septoria tritici Populations M. Mincu (poster) 170 Comparison of Greenhouse and Field Levels of Resistance to Stagonospora nodorum S.L. Walker, S. Leath, and J.P. Murphy (poster) 173 Session 6D: Chemical Control 173 Adjusting Thresholds for Septoria Control in Winter Wheat Using Strobilurins L.N. Jørgensen, K.E. Henriksen, and G.C. Nielsen 177 Concluding Remarks 177 The Septoria/Stagonospora Blotch Diseases of Wheat: Past, Present, and Future Z. Eyal (paper presented by A.L. Scharen) 183 List of Participants v In Memoriam, Dr. Zahir Eyal Our friend and colleague, Professor Zahir Eyal, died Friday, July 30, 1999. Zahir was intimately involved in all of the International Septoria Workshops, from the first in 1976 held in Griffin, Georgia, USA, until the fifth, and present, one held in CIMMYT, Mexico. He put forward his many ideas for program and participants in a forceful, but thoughtful way, and was able to settle disputes with good humor and a smile. Until the last few days of his life, Dr. Eyal continued to work on plans for this Septoria/Stagonospora workshop. After finishing agricultural high school in Israel, Zahir went to the USA, where he earned his B.Sc. degree from Oklahoma State University and his Ph.D. from Rutgers. This was followed by a post-doctoral term at Purdue, where he studied with Jack Schafer and the late Ralph Caldwell. His work on septoria of cereals began when he joined the Department of Botany at Tel Aviv University in 1967. He developed an integrated program of fundamental and applied research aimed at minimizing the economic impact of cereal pathogens, particularly Septoria tritici, on production. He reached out to colleagues in many countries and to international organizations, most especially CIMMYT, for cooperation. Over the years, Zahir contributed greatly to those programs. During his tenure at Tel Aviv University, Professor Eyal served two terms as Head of the Department of Botany (1984-87 and 1992-94). Professor Eyal was an enthusiastic teacher, well-loved by students, both undergraduate and graduate. He taught in English or in Hebrew with equal facility, sharing his knowledge and insights with students and faculty during two sabbaticals at Montana State University and at several other institutions. The numerous publications he authored with his students and the important posts those students occupy today attest to the excellence of his teaching abilities. Zahir’s research and outreach programs incorporated ideas that were new to his country; they were solidly anchored in basic science and innovative to the end. These programs not only improved wheat production in Israel but had positive effects on cereal improvement programs throughout the world. At the time of his death, Professor Eyal was Director of the Institute for Cereal Crop Improvement at Tel Aviv University, where germplasm of wild ancestors of cultivated small grains are being preserved, characterized, and utilized in breeding improved cultivars. Dr. Eyal’s contributions to research, teaching, university administration, and international agriculture are many and far reaching. He received the Hazera Seed Co. Melamed Award in 1968, the A.C. Cohen Award in 1978, and in 1995 was made a Fellow of the American Phytopathological Society. Professor Eyal served as President of the Israeli Phytopathological Society from 1979 to 1982. He will be fondly remembered and sadly missed by his multitude of friends, colleagues, and students throughout the world. vi Foreword In the mid-1970s the idea of holding a septoria workshop began to take hold among a small group of scientists in the USA. They were interested in exchanging ideas and finding ways to manage the septoria diseases that affect wheat and other cereals all over the world. The first workshop was organized in a matter of a few months and held in Griffin, Georgia, in 1976. Among the 50 scientists who attended were a few researchers from outside the US. The enthusiasm of that first workshop led to the development of the second, which was a truly international meeting attended by more than 100 scientists from many countries, held in Bozeman, Montana, in 1983. Since then, international septoria workshops have been held about every five years: in Zurich, Switzerland, in 1989; in Radzikow, Poland, in 1994; and this year at CIMMYT in El Batan, Mexico. Each workshop has expanded the network of scientists who share their knowledge and pose the many questions that remain to be solved about these diseases and their management. The Zurich workshop had increased participation by workers from Europe and Africa. The Radzikow workshop brought increased participation from scientists in eastern Europe. The early workshops focused on the biology of the pathogens and breeding strategies, subjects in which there remain many unanswered questions. The 1994 workshop and the current one emphasize molecular approaches to the genetics of the pathogens. The Fifth International Workshop provides another opportunity to focus on the Septoria/ Stagonospora diseases, but also to see them in the context of the worldwide programs of CIMMYT, which emphasize collaboration with developing countries with the aim of developing stable high yielding wheat varieties that possess durable resistance to the diseases. This workshop also gives us the opportunity to remember our friend and colleague, Zahir Eyal, who passed away not long ago. An integral part of the program development process and the discussions at each workshop, he organized the scientific program for this workshop as well. Zahir Eyal was an enthusiastic supporter of the septoria workshops and the international exchange of ideas. He will be missed. We would like to express our appreciation for the efforts of Ravi Singh, Maarten van Ginkel, and Linda Ainsworth, who organized the workshop. We wish to thank Diana Godínez, María Luisa Varela, and Laura Rodríguez for managing the logistical support. We also recognize the efforts of Arnoldo Amaya, María Garay, Lucy Gilchrist, Monique Henry, Gilberto Hernández, Reynaldo Villareal, Juan José Joven, Marcelo Ortíz, Eliot Sánchez, Kelly Cassaday, Miguel Mellado, Wenceslao Almazán, and Antonio Luna, as well as many other members of CIMMYT staff who contributed to the success of this event. The International Organizing Committee September 21, 1999 1 Opening Remarks Historical Aspects and Future Challenges of an International Wheat Program S. Rajaram Wheat Program, CIMMYT, El Batan, Mexico I am immensely honored and grateful to the organizing committee of the 5th International Septoria Workshop for asking me to deliver this lecture in the opening session. Even though my presentation is very broad and covers many issues, I assure you that I have been involved in breeding for resistance to septoria tritici blotch for at least 25 years, with some remarkable success. In this attempt, I would like to recognize the contribution of Prof. Zahir Eyal, who served as a consultant on septoria issues to CIMMYT in the 1970s and 1980s. Indeed, he and I have some common intellectual roots through Prof. Ralph Caldwell of Purdue University. Prof. Eyal’s untimely death and departure from the scientific community is a loss to us all. I dedicate this opening lecture to him. Wheat is the most widely The formidable challenge to contributed to this decrease grown and consumed food crop in meet this demand is not new to (Pingali and Heisey, 1997). Whether the world. It is the staple food of agricultural scientists who have production constraints are affected nearly 35% of the world been involved in the development by physiological or genetic limits is population, and demand for wheat of improved wheat production hotly debated, but future increases will grow faster than for any other technologies for the past half in food productivity will require major crop. The forecasted global century. For all developing substantial research and demand for wheat in the year 2020 countries, wheat yields have grown development investment to varies between 840 (Rosegrant et at an average annual rate of over improve the profitability of wheat al., 1995) to 1050 million tons 2% between 1961 and 1994 production systems through (Kronstad, 1998). To reach this (CIMMYT, 1996). In Western enhancing input efficiencies. Due to target, global production will need Europe and North America the a continuing necessity for multi- to increase 1.6 to 2.6% annually annual rate of growth for wheat disciplinary team efforts in plant from the present production level yield was 2.7% from 1977 to 1985, breeding, and the rapidly changing of 560 million tons. Increases in falling to 1.5% from 1986 to 1995. development of technologies, three realized grain yield have provided Recent data have indicated a overlapping avenues can be about 90% of the growth in world decrease in the productivity gains considered for raising the yield cereal production since 1950 being achieved by major wheat frontier in wheat: continued (Mitchell et al., 1997) and by the producing countries (Brown, 1997). investments in “conventional first decade of the next century In Western Europe, where the breeding” methods; use of current most of the increase needed in highest average wheat grain yield and expanded genetic diversity; world food production must come is obtained in the Netherlands and investigation and from higher absolute yields (8.6t/ha), yield increased from 5 to implementation of biotechnology (Ruttan, 1993). For wheat, the 6t/ha in five years, but it took assisted plant breeding. global average grain yield must more than a decade to raise yields increase from the current 2.5 t/ha from 6 to 7 t/ha. Worldwide, Conventional Wheat to 3.8t/ha. In 1995, only 18 annual wheat grain yield growth Breeding countries world worldwide had decreased from 3.0% between 1977- average wheat grain yields of more 1985, to 1.6% from 1986-1995, It is likely that gains to be than 3.8 t/ha, the majority located excluding the USSR (CIMMYT, achieved from conventional in Northern Europe (CIMMYT, 1996). Degradation of the land breeding will continue to be 1996). resource base, together with a significant for the next two decades slackening of research investment or more (Duvick, 1996), but these and infrastructure, have 2 Opening Remarks — S. Rajaram are likely to come at a higher by breeders through introgression to the adoption of new Mexican research cost than in the past. In of one or more genes controlling semidwarf wheat cultivars (Byerlee recent surveys of wheat breeders disease resistance. and Moya, 1993). In 1990, an (Braun et al., 1998; Rejesus et al., estimated 93% of the total spring 1996), more than 80% of Adoption of CIMMYT- bread wheat production in respondents expressed concern that Based Germplasm developing countries, excluding plant variety protection (PVP) and China, came from semidwarf plant or gene patents will restrict spring wheats, which covered CIMMYT’s breeding access to germplasm. This may about 83% of the total spring bread methodology is tailored to develop have deleterious consequences for wheat area in developing countries widely adapted, disease resistant future breeding success. (Byerlee and Moya, 1993). germplasm with high and stable Rasmusson (1996) has stated that yield across a wide range of nearly half of the progress made by Table 1. Origin of spring bread wheat varieties in environments. The impact of this developing countries. breeders in the past can be approach has been significant. attributed to germplasm exchange. The total spring bread wheat NARS cross Regional and international (Triticum aestivum L.) area in CIMMYT CIMMYT CIMMYT No nurseries have been an efficient cross parents ancestor CIMMYT developing countries, excluding means of gathering data from 1966-90 45% 28% 3% 24%* China, is around 63 million ha, of varied environments and exposing 1991-97 58% 30% 3% 9% which 36 million ha or 58% are germplasm to diverse pathogen * Estimated. planted to varieties derived from Note: Excluding China. NARS=national agricultural selection pressures, while CIMMYT germplasm (Table 1) research system. providing access and exchange of (Byerlee and Moya, 1993; germplasm. Breeders utilize these The cornerstone of CIMMYT’s Rajaram, 1995). During the 1966-90 cooperative nurseries extensively breeding methodology is targeted period, 1317 bread wheat cultivars in their crossing programs (Braun breeding for the mega- were released by developing et al., 1998). However, the number environments, the use of a diverse countries, of which 70% were either of cooperatively distributed wheat gene pool for crossing, shuttle direct releases from CIMMYT yield and screening nurseries has breeding, selection for yield under advanced lines or had at least one been greatly reduced during the optimum conditions, and multi- CIMMYT parent (Byerlee and past decade. locational testing to identify Moya, 1993). For the 1986-90 superior germplasm with good period, 84% of all bread wheat Investments needed for disease resistance. In this paper we cultivars released in developing breeding efforts will increase with would like to present some recent countries had CIMMYT germplasm increasing yield levels. Further, developments in CIMMYT’s Wheat in their pedigrees. Simultaneously progress to develop higher yielding Program. the use of dwarfing genes has cultivars is reduced with every continued to increase over time. objective added to a breeding Targeted breeding: The Today, regardless of the type of program. Though the list of mega-environment concept wheat, more than 90% of all wheat important traits may get longer and To address the needs of diverse varieties released in developing longer, little if any assistance has wheat growing areas, CIMMYT countries are semidwarfs, which been provided by economists to introduced in 1988 the concept of covered 70% of the total wheat area prioritize breeding objectives. mega-environments (ME) (Rajaram in developing countries by the end Considering that a wheat breeding et al., 1994). Mega-environments of 1990 (Byerlee and Moya, 1993). program like CIMMYT allocates are defined as a broad, not The continuous adoption of around 60% of its resources to necessarily contiguous areas, semidwarf spring wheat cultivars durable resistance breeding, the occurring in more than one country in the post-Green Revolution need for research in this field is and frequently transcontinental, period (1977-90) resulted in about obvious. Due to high costs, we see defined by similar biotic and 15.5 million tons of additional durable resistance breeding as one abiotic stresses, cropping system wheat production in 1990, valued of the first fields where requirements, consumer at about US$ 3 billion, of which transformation should be applied preferences, and, for convenience, 50%, or US$ 1.5 billion, is attributed 3 Historical Aspects and Future Challenges of an International Wheat Program by volume of production. Use of diverse genepools to Broad-based plant germplasm Germplasm generated for a given maintain genetic diversity resources are imperative for a ME is useful throughout that Recent surveys conducted by sound and successful breeding environment, accommodating the CIMMYT Economics Program program. Utmost attention is given major stresses but perhaps not all have found that 58% of all wheat to the genetic diversity within the significant secondary stresses. varieties in developing countries CIMMYT germplasm to minimize Within an ME, millions of hectares derive from CIMMYT germplasm; the risk of genetic vulnerability, are addressed with a certain degree this percentage rises to more than since it is grown on large areas and of homogeneity as relates to wheat. 80%, if varieties with parents of is widely used by national By 1993, 12 ME had been defined, 6 CIMMYT origin are also included programs. I believe that the use of for spring wheats (ME1-ME6), 3 for (Table 1). This spectacular success genetically diverse material is facultative wheats (ME7-ME9), and puts an enormous burden on mandatory to increase yield 3 for winter wheats (ME9-ME12). CIMMYT to continually diversify potential and yield stability in the Details of each ME are given in its germplasm base for resistance future. In any year 500-800 parental Table 2. and stability parameters. lines are considered for crossing. Table 2. Classification of megaenvironments (MEs) used by the CIMMYT Wheat Program. Year Major Representative breeding Area Moisture Temperature Growth breeding locations/ began at ME Latitudea (m ha)b regimec regimed habit Sowne objectivesf, g regions CIMMYT SPRING WHEAT 1 Low 32.0 Low rainfall, Temperate Spring A Resistance to Yaqui Valley, 1945 irrigated lodging, SR, LR, YR Mexico; Indus Valley, Pakistan; Gangetic Valley, India; Nile Valley, Egypt 2 Low 10.0 High rainfall Temperate Spring A As for ME1 + North African 1972 resistance to Coast, Highlands of YR, Septoria East Africa, Andes, spp., sprouting and Mexico 3 Low 1.7 High rainfall Temperate Spring A As for ME2 + Passo Fundo, 1974 acid soil Brazil tolerance 4A Low 10.0 Low rainfall, Temperate Spring A Resistance to Aleppo, Syria; 1974 winter drought, Settat, Morocco dominant Septoria spp., YR 4B Low 5.8 Low rainfall, Temperate Spring A Resistance to Marcos Juárez, 1974 summer drought, Argentina dominant Septoria spp., Fusarium spp., LR, SR 4C Low 5.8 Mostly Hot Spring A Resistance to Indore, India 1974 residual drought, and moisture heat in seedling stage 5A Low 3.9 High rainfall Hot Spring A Resistance to Joydepur, 1981 / irrigated, heat, Helmin- Bangladesh; humid thosporium Londrina, Brazil spp., Fusarium spp., sprouting 5B Low 3.2 Irrigated , Hot Spring A Resistance to Gezira, Sudan; 1975 low humidity heat and SR Kano, Nigeria 6 High 5.4 Moderate Temperate Spring S Resistance to Harbin, China 1989 rainfall/ SR, LR, Helmin- summer thosporium spp., dominant Fusarium spp., sprouting, photoperiod sensitivity (cont’d.)
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