Abstract
Stripe rust disease is caused by the fungus Puccinia striiformis f. sp. tritici and severely threatens wheat worldwide, repeatedly breaking resistance conferred by resistance genes and evolving more aggressive strains. Wild emmer wheat, Triticum dicoccoides, is an important source for novel stripe rust resistance (Yr) genes. Yr15, a major gene located on chromosome 1BS of T. dicoccoides, was previously reported to confer resistance to a broad spectrum of stripe rust isolates, at both seedling and adult plant stages. Introgressions of Yr15 into cultivated T. aestivum bread wheat and T. durum pasta wheat that began in the 1980s are widely used. In the present study, we aimed to validate SSR markers from the Yr15 region as efficient tools for marker-assisted selection (MAS) for introgression of Yr15 into wheat and to compare the outcome of gene introgression by MAS and by conventional phenotypic selection. Our findings establish the validity of MAS for introgression of Yr15 into wheat. We show that the size of the introgressed segment, defined by flanking markers, varies for both phenotypic selection and MAS. The genetic distance of the MAS marker from Yr15 and the number of backcross steps were the main factors affecting the length of the introgressed donor segments. Markers Xbarc8 and Xgwm493, which are the nearest flanking markers studied, were consistent and polymorphic in all 34 introgressions reported here and are therefore the most recommended markers for the introgression of Yr15 into wheat cultivars. Introgression directed by markers, rather than by phenotype, will facilitate simultaneous selection for multiple stripe rust resistant genes and will help to avoid escapees during the selection process.
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References
Aaronsohn A (1910) Agricultural and botanical explorations in Palestine. Bureau of Plant Industry Bulletin 180, USDA
Bariana H, Brown G, Bansal U, Miah H, Standen G, Lu M (2007) Breeding triple rust resistant wheat cultivars for Australia using conventional and marker-assisted selection technologies. Crop Pasture Sci 58:576–587
Brennan JP, Murray GM (1998) Economic importance of wheat diseases in Australia. Wagga Wagga, NSW Agriculture
Brouwer DJ, St Clair DA (2004) Fine mapping of three quantitative trait loci for late blight resistance in tomato using near isogenic lines (NILs) and sub-NILs. Theor Appl Genet 108:628–638
Cavanagh CR, Taylor J, Larroque O, Coombes N, Verbyla AP, Nath Z, Kutty I, Rampling L, Butow B, Ral JP, Tomoskozi S, Balazs G, Bekes F, Mann G, Quail KJ, Southan M, Morell MK, Newberry M (2010) Sponge and dough bread making: genetic and phenotypic relationships with wheat quality traits. Theor Appl Genet 121:815–828
Chen XM (2005) Epidemiology and control of stripe rust [Puccinia striiformis f. sp tritici] on wheat. Can J Plant Pathol 27:314–337
Chen XM (2007) Challenges and solutions for stripe rust control in the United States. Aust J Agric Res 58:648–655
Chen XM, Moore M, Milus EA, Long DL, Line RF, Marshall D, Jackson L (2002) Wheat stripe rust epidemics and races of Puccinia striiformis f. sp. tritici in the United States in 2000. Plant Dis 86:39–46
Chen XM, Penmanb L, Wanb A, Cheng P (2010) Virulence races of Puccinia striiformis f. sp. tritici in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Can J Plant Pathol 32:315–333
Cheng J, Yan J, Sela H, Manisterski J, Lewinsohn D, Nevo E, Fahima T (2010) Pathogen race determines the type of resistance response in the stripe rust—Triticum dicoccoides pathosystem. Physiol Plantarum 139:269–279
Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 363:557–572
Fahima T, Röder M, Grama A, Nevo E (1998) Microsatellite DNA polymorphism divergence in Triticum dicoccoides accessions highly resistant to yellow rust. Theor Appl Genet 96:187–195
Ganal MW, Röder MS (2007) Microsatellite and SNP markers in wheat breeding. In: Varshney RK, Tuberosa R (eds) Genomics-assisted crop improvement, vol 2. Springer Verlag, Heidelberg, pp 1–24. ISBN 978-1-4020-6296-4
Gerechter-Amitai ZK, van Silfhout CH, Grama A, Kleitman F (1989) Yr15—a new gene for resistance to Puccinia striiformis in Triticum dicoccoides sel. G25. Euphytica 43:187–190
Gerechter-Amitai ZK, Grama A, Kleitman F, Daos A (1992) Improvement of cultivated wheat by transfer of high protein potential and resistance to powdery mildew and yellow rust from wild emmer wheat. The Netherlands Ministry of Development Cooperation, The Hague
Grama A, Gerechter-Amitai ZK (1974) Inheritance of resistance to stripe rust (Puccinia striiformis) in crosses between wild emmer (Triticum dicoccoides) and cultivated tetraploid and hexaploid wheats. II. Triticum aestivum. Euphytica 23:393–398
Grama A, Gerechter-Amitai ZK, Blum A, Rubenthaler GL (1982) Breeding bread wheat cultivars for high protein content by transfer of protein genes from Triticum dicoccoides. In: Proceedings of the seed protein improvement by nuclear techniques, Research Coordination Meetings, IAEA, Vienna, December 1982
Gupta PK, Varshney RK (2000) The development and use of microsatellite markers for genetic analysis and plant breeding with emphasis on bread wheat. Euphytica 113:163–185
Gupta PK, Varshney RK, Sharma PC, Ramesh B (1999) Molecular markers and their applications in wheat breeding. Plant Breed 118:369–390
Hammond-Kosack KE, Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607
He Y, Li X, Zhang J, Jiang G, Liu S, Chen S, Tu J, Xu C, Zhang Q (2004) Gene pyramiding to improve hybrid rice by molecular marker techniques. In: Proceedings of the 4th international crop science congress, Brisbane, Australia
Hill CB, Taylor JD, Edwards J, Mather D, Bacic A, Langridge P, Roessner U (2013) Whole-genome mapping of agronomic and metabolic traits to identify novel quantitative trait loci in bread wheat grown in a water-limited environment. Plant Physiol 162:1266–1281s
Holland JB (2004) Implementation of molecular markers for quantitative traits in breeding programs—challenges and opportunities. In: Proceedings of the 4th international crop science congress, Brisbane, Australia
Hospital F (2001) Size of donor chromosome segments around introgressed loci and reduction of linkage drag in marker-assisted backcross programs. Genetics 158:1363–1380
Jacobsen E, Schouten HJ (2007) Cisgenesis strongly improves introgression breeding and induced translocation breeding of plants. Trends Biotechnol 25:219–223
Joshi RK, Nayak S (2010) Gene pyramiding-A broad spectrum technique for developing durable stress resistance in crops. Biotechnol Mol Biol Rev 5:51–60
Kidwell KK, Osborn TC (1992) Simple plant DNA isolation procedures. In: Beckmann JS, Osborn TC (eds) Plant genomes: methods for genetic and physical mapping. Kluwer Academic Publishers, Dordrecht, pp 1–13
Koebner R, Summers RW (2003) 21st century wheat breeding: plot selection or plate detection? Trends Biotechnol 21:59–63
Li GQ, Li ZF, Yang WY, Zhang Y, He ZH, Xu SC, Singh RP, Qu YY, Xia XC (2006) Molecular mapping of stripe rust resistance gene YrCH42 in Chinese wheat cultivar Chuanmai 42 and its allelism with Yr24 and Yr26. Theor Appl 112:1434–1440
Lin F, Chen XM (2007) Genetics and molecular mapping of genes for race-specific all-stage resistance and non-race-specific high-temperature adult-plant resistance to stripe rust in spring wheat cultivar Alpowa. Theor Appl Genet 114:1277–1287
Line RF, Qayoum A (1992) Virulence, aggressiveness, evolution, and distribution of races of Puccinia striiformis (the cause of stripe rust of wheat) in North America, 1968–87. US Dep Agric Agric Res Serv Tech Bull 1788
McDonald BA, Linden C (2002) The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica 124:163–180
McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212–222
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO, Melbourne, Australia
McIntosh RA, Silk J, The TT (1996) Cytogentic studies in wheat. XVII. Monosomic analysis and linkage relationships of the gene Yr15 for resistance to stripe rust. Euphytica 89:395–399
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Somers DJ, Appels R, Devos KM (2008) Catalogue of gene symbols for wheat. In: Proceedings of the 11th international wheat genetics symposium, pp 1–59
Mester D, Ronin Y, Minkov D, Nevo E, Korol AB (2003) Constructing large-scale genetic maps using an evolutionary strategy algorithm. Genetics 165:2269–2282
Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130
Murphy LR, Santra D, Kidwell K, Yan G, Chen X, Campbell KG (2009) Linkage maps of wheat stripe rust resistance genes Yr5 and Yr15 for use in marker-assisted selection. Crop Sci 49:1786–1790
Nevo E, Korol AB, Beiles A, Fahima T (2002) Evolution of wild emmer and wheat improvement. Springer, Heidelberg. ISBN 978-1-4020-6297-1
Niks RE, Parlevliet JE, Lindhout P, Bai Y (2011) Breeding crops with resistance to diseases and pests. Wageningen Academic Publishers, Wageningen, p 198
Niu YC, Qiao Q, Wu LR (2000) Postulation of resistance genes to stripe rust in commercial wheat cultivars from Henan, Shandong and Anhui provinces. Acta Phytopathol Sin 30:122–128
Panigrahi J, Mishra RR, Sahu AR, Rath SC, Seth S, Mishra SP (2013) Marker-assisted breeding for simple inherited traits conferring stress resistance in crop plants. The Ecoscan 02/2013; III(Special):217–233
Peleg Z, Saranga Y, Suprunova T, Ronin Y, Röder MS, Kilian A, Korol AB, Fahima T (2008) High-density genetic map of durum wheat × wild emmer wheat based on SSR and DArT markers. Theor Appl Genet 117:103–115
Peng JH, Fahima T, Röder MS, Huang OY, Dahan A, Li YC, Grama A, Nevo E (2000) High-density molecular map of chromosome region harboring stripe-rust resistance gene YrH52 and Yr15 derived from wild emmer wheat, Triticum dicoccoides. Genetica 109:199–210
Qayoum A, Line RF (1985) High-temperature, adult-plant resistance to stripe rust of wheat. Phytopathology 75:1121–1125
Randhawa M, Bansal U, Valárik M, Klocová B, Doležel J, Bariana H (2014) Molecular mapping of stripe rust resistance gene Yr51 in chromosome 4AL of wheat. Theor Appl Genet 127:317–324
Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023
Sharp PJ, Johnston S, Brown G, McIntosh RA, Pallotta M, Carter M, Jones MGK (2001) Validation of molecular markers for wheat breeding. Crop Pasture Sci 52:1357–1366
Simko I, Pechenick DA, McHale LK, Truco MJ, Ochoa OE, Michelmore RW, Scheffler BE (2009) Association mapping and marker-assisted selection of the lettuce dieback resistance gene Tvr1. BMC Plant Biol 9:135
Singh S, Sidhu JS, Huang N, Vikal Y, Li Z, Brar DS, Dhaliwal HS, Khush GS (2001) Pyramiding three bacterial blight resistance genes (xa5, xa13 and Xa21) using marker-assisted selection into indica rice cultivar PR106. Theor Appl Genet 102:1011–1015
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Song QJ, Fickus EW, Cregan PB (2002) Characterization of trinucleotide SSR motifs in wheat. Theor Appl Genet 104:286–293
Sourdille P, Singh S, Cadalen T, Brown-Guedira G, Gay G, Qi L, Qi LL, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25
Spielmeyer W, Sharpb PJ, Lagudaha ES (2003) Identification and validation of markers linked to broad-spectrum stem rust resistance gene Sr2 in wheat (Triticum aestivum L.). Crop Sci 43:333–336
Stam P, Zeven AC (1981) The theoretical proportion of the donor genome in near-isogenic lines of self-fertilizers bred by backcrossing. Euphytica 30:227–238
Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268:661–667
Stubbs RW (1985) Stripe rust. In: Roelfs AP, Bushnell WR (eds) The cereal rusts, vol 2., Diseases, distribution, epidemiology, and controlAcademic Press, Orlando, FL, USA, pp 61–101
Stuber CW (1991) Biochemical and molecular markers in plant breeding. Plant Breed Rev 9:37–61
Sun GL, Fahima T, Korol AB, Turpeinen T, Grama A, Ronin YI, Nevo E (1997) Identification of molecular markers linked to the Yr15 stripe rust resistance gene of wheat originated in wild emmer wheat, Triticum dicoccoides. Theor Appl Genet 95:622–628
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822
Timonova EM, Leonova IN, Röder MS, Salina EA (2013) Marker-assisted development and characterization of a set of Triticum aestivum lines carrying different introgressions from the T. timopheevii genome. Mol Breed 31:123–136
Tyrka M, Perovic D, Wardynska A, Ordon F (2008) A new diagnostic SSR marker for selection of the Rym4/Rym5 locus in barley breeding. J Appl Genet 49:127–134
van Silfhout CH, Grönewegen LJM (1984) The use of T. dicoccoides in winter wheat breeding. Vle conf. eur. et méditerr. Sur les rouilles des cereals. Grignon, 4–7 Septembre 1984. Ed. INRA Publ., 1984 (Les colloques de l’INRA, nr 25). Dissertation
Xie W, Ben-David R, Zeng B, Dinoor A, Xie C, Sun Q, Röder MS, Fahoum A, Fahima T (2012) Suppressed recombination rate on 6VS/6AL translocation region carrying the Pm21 locus introgressed from Haynaldia villosa into hexaploid wheat. Mol Breed 29:399–412
Yang ZP, Gilbert J, Somers DJ, Fedak G, Procunier JD, McKenzie IH (2003) Marker assisted selection of fusarium head blight resistance genes in two doubled- haploid populations of wheat. Mol Breed 12:309–317
Young ND, Tanksley SD (1989) RFLP analysis of the size of chromosomal segments retained around the Tm-2 locus of tomato during backcross breeding. Theor Appl Genet 77:353–359
Zakari A, McIntosh RA, Hovmoller MS, Wellings CR, Shariflou MR, Hayden M, Bariana HS (2003) Recombination of Yr15 and Yr24 in chromosome 1BS. In: Pogna NE, Romano N, Pogna EA, Galterio G (eds) Proc 10th Int Wheat Genet Symp, vol 1. Instituto Sperimentale per la Cerealcoltura, Rome, pp 417–420
Zhou R, Zhu Z, Kong X, Huo N, Tian Q, Li P, Jia J (2005) Development of wheat near-isogenic lines for powdery mildew resistance. Theor Appl Genet 110:640–648
Acknowledgments
This work was supported by grants from Sixth Framework Programme (FP6) of the European Union through the BioExploit project (CT-2005-513949), the United States—Israel Binational Agricultural Research and Development Fund (BARD), Grant IS-4628-13, and the Israel Science Foundation equipment Grant 1719/08. Dina Raats is grateful for the Eshkol Fellowship awarded by the Israeli Ministry of Science. Dr. J. Dubcovsky acknowledges support from HHMI, GBMF, and USDA-NIFA Grant 2011-68002-30029. The authors would like to acknowledge the help of the late Dr. Z. Gerechter-Amitai from the Agricultural Research Organization, Beit Dagan, Israel, Dr. X. Zhang from the University of California, and Drs. R. McIntosh and T. The from the University of Sydney, Australia, in providing us with the Yr15 introgression lines and the corresponding recipient lines, together with their pedigree information. The authors thank Dr. J. Manisterski and P. Ben-Yehuda from Tel Aviv University for providing spores of Puccinia striiformis isolate 5006 (race 38E134). The authors would like to thank O. Gurevich and T. Kis-Papo from the University of Haifa, Israel for their skillful technical assistance.
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Elitsur Yaniv and Dina Raats have contributed equally to this work.
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Yaniv, E., Raats, D., Ronin, Y. et al. Evaluation of marker-assisted selection for the stripe rust resistance gene Yr15, introgressed from wild emmer wheat. Mol Breeding 35, 43 (2015). https://doi.org/10.1007/s11032-015-0238-0
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DOI: https://doi.org/10.1007/s11032-015-0238-0