Theoretical and Applied Genetics

, Volume 127, Issue 7, pp 1549–1559 | Cite as

Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.)

  • Matthew N. Rouse
  • Luther E. Talbert
  • Davinder Singh
  • Jamie D. Sherman
Original Paper

Abstract

Key message

Quantitative trait loci conferring adult plant resistance to Ug99 stem rust in Thatcher wheat display complementary gene action suggesting multiple quantitative trait loci are needed for effective resistance.

Abstract

Adult plant resistance (APR) in wheat (Triticum aestivum L.) to stem rust, caused by Puccinia graminis f. sp. tritici (Pgt), is desirable because this resistance can be Pgt race non-specific. Resistance derived from cultivar Thatcher can confer high levels of APR to the virulent Pgt race TTKSK (Ug99) when combined with stem rust resistance gene Sr57 (Lr34). To identify the loci conferring APR in Thatcher, we evaluated 160 RILs derived from Thatcher crossed to susceptible cultivar McNeal for field stem rust reaction in Kenya for two seasons and in St. Paul for one season. All RILs and parents were susceptible as seedlings to race TTKSK. However, adult plant stem rust severities in Kenya varied from 5 to 80 %. Composite interval mapping identified four quantitative trait loci (QTL). Three QTL were inherited from Thatcher and one, Sr57, was inherited from McNeal. The markers closest to the QTL peaks were used in an ANOVA to determine the additive and epistatic effects. A QTL on 3BS was detected in all three environments and explained 27–35 % of the variation. The peak of this QTL was at the same location as the Sr12 seedling resistance gene effective to race SCCSC. Epistatic interactions were significant between Sr12 and QTL on chromosome arms 1AL and 2BS. Though Sr12 cosegregated with the largest effect QTL, lines with Sr12 were not always resistant. The data suggest that Sr12 or a linked gene, though not effective to race TTKSK alone, confers APR when combined with other resistance loci.

Keywords

Quantitative Trail Locus Stem Rust Adult Plant Resistance Significant Quantitative Trail Locus Stem Rust Resistance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Funding for this research was provided by the USDA-ARS National Plant Disease Recovery System, the Durable Rust Resistance in Wheat project (funded by the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development), and the USDA-AFRI Triticeae Coordinated Agricultural Project (2011-68002-30029). We acknowledge the Computational Genetics Laboratory of the University of Minnesota Supercomputing Institute for computational support. We are grateful to staff at the Kenya Agricultural Research Institute and at the USDA-ARS Cereal Disease Laboratory for maintenance of field experiments. Mention of trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA, and does not imply its approval to the exclusion of other products and vendors that might also be suitable.

Conflict of interest

The authors declare that there are no conflict of interest.

Ethical standards

The authors declare that the experiments comply with the current laws of the countries in which the experiments were performed.

References

  1. Anderson JA, Wiersma JJ, Linkert GL, Kolmer JA, Jin Y, Dill-Macky R, Wiersma JV, Hareland GA, Busch RH (2012) Registration of ‘Tom’ wheat. J Plant Reg 6:180–185CrossRefGoogle Scholar
  2. Faris JD, Xu SS, Cai X, Friesen TL, Jin Y (2008) Molecular and cytogenetic characterization of a durum wheat-Aegilops speltoides chromosome translocation conferring resistance to stem rust. Chromosome Res 16:1097–1105PubMedCrossRefGoogle Scholar
  3. Gavin Vanegas CD, Garvin DF, Kolmer JA (2008) Genetics of stem rust resistance in the spring wheat cultivar Thatcher and the enhancement of resistance by Lr34. Euphytica 159:391–401CrossRefGoogle Scholar
  4. Ghazvini H, Hiebert CW, Zegeye T, Fetch T (2012a) Inheritance of stem rust resistance derived from Aegilops triuncialis in wheat line Tr129. Can J Plant Sci 92:1037–1041CrossRefGoogle Scholar
  5. Ghazvini H, Hiebert CW, Zegeye T, Liu S, Dilawari M, Tsilo T, Anderson JA, Rouse MN, Jin Y, Fetch T (2012b) Inheritance of resistance to Ug99 stem rust in wheat cultivar Norin 40 and genetic mapping of Sr42. Theor Appl Genet 125:817–824PubMedCrossRefGoogle Scholar
  6. Green GJ, Dyck PL (1975) The reaction of Thatcher wheat to Canadian races of stem rust. Can Plant Dis Surv 55:85–86Google Scholar
  7. Haile JK, Nachit MM, Hammer K, Badebo A, Roder MS (2012) QTL mapping of resistance to race Ug99 of Puccinia graminis f. sp. tritici in durum wheat (Triticum durum Desf.). Mol Breeding 30:1479–1493CrossRefGoogle Scholar
  8. Hayes HK, Ausemus ER, Stakman EC, Bailey CH, Wilson HK, Bamberg RH, Markley MC, Crim RF, Levine MN (1936) Thatcher wheat. Minn Agric Exp Stn Tech Bull 325Google Scholar
  9. Hiebert CW, Fetch T Jr, Zegeye T (2010) Genetics and mapping of stem rust resistance to Ug99 in the wheat cultivar Webster. Theor Appl Genet 121:65–69PubMedCrossRefGoogle Scholar
  10. Hiebert CW, Fetch TG, Zegeye T, Thomas JB, Somers DJ, Humphreys DG, McCallum BD, Cloutier S, Singh D, Knott DR (2011) Genetics and mapping of seedling resistance to Ug99 stem rust in Canadian wheat cultivars ‘Peace’ and ‘AC Cadillac’. Theor Appl Genet 122:143–149PubMedCrossRefGoogle Scholar
  11. Jin Y, Singh RP (2006) Resistance in US wheat to recent Eastern African isolates of Puccinia graminis f. sp. tritici with virulence to resistance gene Sr31. Plant Dis 90:476–480CrossRefGoogle Scholar
  12. Jin Y, Singh RP, Ward RW, Wanyera R, Kinyua M, Njau P, Fetch T Jr, Pretorius ZA, Yahyaoui A (2007) Characterization of seedling infection types and adult plant infection responses of monogenic Sr gene lines to race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 91:1096–1099CrossRefGoogle Scholar
  13. Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T Jr (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926CrossRefGoogle Scholar
  14. Jin Y, Szabo LJ, Rouse MN, Fetch T Jr, Pretorius ZA, Wanyera R, Njau P (2009) Detection of virulence to resistance gene Sr36 within the TTKS race lineage of Puccinia graminis f. sp. tritici. Plant Dis 93:367–370CrossRefGoogle Scholar
  15. Klindworth DL, Niu Z, Chao S, Friesen TL, Jin Y, Faris JD, Cai X, Xu SS (2012) Introgression and characterization of a goatgrass gene for a high level of resistance to Ug99 stem rust in tetraploid wheat. G3 2:665–673PubMedCentralPubMedCrossRefGoogle Scholar
  16. Knott DR (2000) The inheritance of stem rust resistance in Thatcher wheat. Can J Plant Sci 80:53–63CrossRefGoogle Scholar
  17. Knott DR (2001) The relationship between seedling and field resistance to two races of stem rust in Thatcher wheat. Can J Plant Sci 81:415–418CrossRefGoogle Scholar
  18. Kolmer JA, Dyck PL, Roelfs AP (1991) An appraisal of stem and leaf rust resistance in North American hard red spring wheats and the probability of multiple mutations to virulence in populations of cereal rust fungi. Phytopathology 81:237–239Google Scholar
  19. Kolmer JA, Garvin DF, Jin Y (2011) Expression of a Thatcher wheat adult plant stem rust resistance QTL on chromosome arm 2BL is enhanced by Lr34. Crop Sci 51:526–533CrossRefGoogle Scholar
  20. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Heurta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363PubMedCrossRefGoogle Scholar
  21. Lagudah ES, McFadden H, Singh RP, Huerta-Espino J, Bariana HS, Spielmeyer W (2006) Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor Appl Genet 114:21–30PubMedCrossRefGoogle Scholar
  22. Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brown-Guedira G, Selter LL, Keller B (2009) Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor Appl Genet 119:889–898PubMedCrossRefGoogle Scholar
  23. Lanning SP, Talbert LE, McGuire CF, Bowman HF, Carlson GR, Jackson GD, Eckhoff JL, Kushnak GD, Stougaard RN, Stallknecht GF, Wichman DM (1994) Registration of ‘McNeal’ wheat. Crop Sci 34:1126–1127CrossRefGoogle Scholar
  24. Letta T, Maccaferri M, Badebo A, Ammar K, Ricci A, Crossa J, Tuberosa R (2013) Searching for novel sources of field resistance to Ug99 and Ethiopian stem rust races in durum wheat via association mapping. Theor Appl Genet 126:1237–1256PubMedCrossRefGoogle Scholar
  25. Liu S, Yu L, Singh RP, Jin Y, Sorrells ME, Anderson JA (2010) Diagnostic and co-dominant PCR markers for wheat stem rust resistance genes Sr25 and Sr26. Theor Appl Genet 120:691–697PubMedCrossRefGoogle Scholar
  26. Liu W, Jin Y, Rouse M, Friebe B, Gill B, Pumphrey MO (2011a) Development and characterization of wheat-Ae. searsii Robertsonian translocations and a recombinant chromosome conferring resistance to stem rust. Theor Appl Genet 122:1537–1545PubMedCrossRefGoogle Scholar
  27. Liu W, Rouse M, Friebe B, Jin Y, Gill B, Pumphrey MO (2011b) Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from Aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosome Res 19:669–682PubMedCrossRefGoogle Scholar
  28. Lorieux M, Goffinet B, Perrier X, De Gonzales Leon D, Laaud C (1995) Maximum likelihood models for mapping genetic markers showing segregation distortion. 1. Backcross populations. Theor Appl Genet 90:73–80PubMedGoogle Scholar
  29. Lowe I, Jankuloski L, Chao S, Chen X, See D, Dubcovsky J (2011) Mapping and validation of QTL which confer partial resistance to broadly virulent post-2000 North American races of stripe rust in hexaploid wheat. Theor Appl Genet 123:143–157PubMedCrossRefGoogle Scholar
  30. Luig NH (1983) A survey of virulence genes in wheat stem rust, Puccinia graminis f. sp. tritici. Advances in plant breeding, Supplement 11 to Journal of Plant Breeding. Paul Parey, BerlinGoogle Scholar
  31. Mago R, Spielmeyer W, Lawrence GJ, Lagudah ES, Ellis JG, Pryor A (2002) Identification and mapping of molecular markers linked to rust resistance genes located on chromosome 1RS of rye using wheat-rye translocation lines. Theor Appl Genet 104:1317–1324PubMedCrossRefGoogle Scholar
  32. Mago R, Bariana HS, Dundas IS, Spielmeyer W, Lawrence GJ, Pryor AJ, Ellis JG (2005) Development of PCR markers for the selection of wheat stem rust resistance genes Sr24 and Sr26 in diverse wheat germplasm. Theor Appl Genet 111:496–504PubMedCrossRefGoogle Scholar
  33. Mago R, Brown-Geudira G, Dreisigacker S, Breen J, Jin Y, Singh R, Appels R, Lagudah ES, Ellis J, Spielmeyer W (2011) An accurate DNA marker assay for stem rust resistance gene Sr2 in wheat. Theor Appl Genet 122:735–744PubMedCrossRefGoogle Scholar
  34. McIntosh RA, Dubcovsky J, Rogers WJ, Morris CF, Appels R, Xia XC (2012) Catalogue of gene symbols for wheat: 2012 supplement. Annu Wheat Newslett 58:259–279Google Scholar
  35. Naruoka Y, Talbert LE, Lanning SP, Blake NK, Martin JM, Sherman JD (2011) Identification of quantitative trait loci for productive tiller number and its relationship to agronomic traits in spring wheat. Theor Appl Genet 123:1043–1053PubMedCrossRefGoogle Scholar
  36. Nazari K, Mafi M, Yahyaoui A, Singh RP, Park RF (2009) Detection of wheat stem rust (Puccinia graminis f. sp. tritici) race TTKSK (Ug99) in Iran. Plant Dis 93:317CrossRefGoogle Scholar
  37. Niu Z, Klindworth DL, Friesen TL, Chao S, Jin Y, Cai X, Xu SS (2011) Targeted introgression of a wheat stem rust resistance gene by DNA marker-assisted chromosome engineering. Genetics 187:1011–1021PubMedCentralPubMedCrossRefGoogle Scholar
  38. Njau PN, Jin Y, Huerta-Espino J, Keller B, Singh RP (2010) Identification and evaluation of sources of resistance to stem rust race Ug99 in wheat. Plant Dis 94:413–419CrossRefGoogle Scholar
  39. Njau PN, Bhavani S, Huerta-Espino J, Keller B, Singh RP (2013) Identification of QTL associated with durable adult plant resistance to stem rust race Ug99 in wheat cultivar ‘Pavon 76’. Euphytica 190:33–44CrossRefGoogle Scholar
  40. Olson EL, Brown-Geudira G, Marshall D, Stack E, Bowden RL, Jin Y, Rouse M, Pumphrey MO (2010) Development of wheat lines having a small introgressed segment carrying stem rust resistance gene Sr22. Crop Sci 50:1823–1830CrossRefGoogle Scholar
  41. Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity of leaves and stem of cereals. Can J Res Sect C 26:496–500CrossRefGoogle Scholar
  42. Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84:203CrossRefGoogle Scholar
  43. Pretorius ZA, Bender CM, Visser B, Terefe T (2010) First report of a Puccinia graminis f. sp. tritici race virulent to the Sr24 and Sr31 wheat stem rust resistance genes in South Africa. Plant Dis 94:784CrossRefGoogle Scholar
  44. Pretorius ZA, Szabo LJ, Boshoff WHP, Herselman L, Visser B (2012) First report of a new TTKSF race of wheat stem rust (Puccinia graminis f. sp. tritici) in South Africa and Zimbabwe. Plant Dis 96:590CrossRefGoogle Scholar
  45. Qi LL, Pumphrey MO, Friebe B, Zhang P, Qian C, Bowden RL, Rouse MN, Jin Y, Gill BS (2011) A novel Robertsonian translocation event leads to transfer of a stem rust resistance gene (Sr52) effective against race Ug99 from Dasypyrum villosum into bread wheat. Theor Appl Genet 123:159–167PubMedCrossRefGoogle Scholar
  46. Roelfs AP (1978) Estimated losses caused by rust in small grain cereals in the United States: 1918–76. USDA Miscellaneous Publication, USA 1363Google Scholar
  47. Roelfs AP, Martens JW (1988) An international system of nomenclature for Puccinia graminis f. sp. tritici. Phytopathology 78:526–533CrossRefGoogle Scholar
  48. Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat: concepts and methods of disease management. CIMMYT, MexicoGoogle Scholar
  49. Rouse MN, Wanyera R, Njau P, Jin Y (2011) Sources of resistance to stem rust race Ug99 in spring wheat germplasm. Plant Dis 95:762–766CrossRefGoogle Scholar
  50. Rouse MN, Nava IC, Chao SM, Anderson JA, Jin Y (2012) Identification of markers linked to the race Ug99 effective stem rust resistance gene Sr28 in wheat (Triticum aestivum L.). Theor Appl Genet 125:877–885PubMedCrossRefGoogle Scholar
  51. Saal B, Wricke G (1999) Development of simple sequence repeat markers in rye (Secale cereale L.). Genome 42:964–972PubMedCrossRefGoogle Scholar
  52. Sambasivam PK, Bansal UK, Hayden MJ, Dvorak J, Lagudah ES, Bariana HS (2008) Identification of markers linked with stem rust resistance genes Sr33 and Sr45. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds) Proceedings of 11th international wheat genetics symposium. Sydney University Press, Australia, pp 351–353Google Scholar
  53. Sherman JD, Martin JM, Blake NK, Lanning SP, Talbert LE (2014) Genetic basis of agronomic differences between a modern and a historical spring wheat cultivar. Crop Sci 54:1–13CrossRefGoogle Scholar
  54. Simons K, Abate Z, Chao S, Zhang W, Rouse M, Jin Y, Elias E, Dubcovsky J (2011) Genetic mapping of stem rust resistance gene Sr13 in tetraploid (Triticum turgidum ssp. durum L.). Theor Appl Genet 122:649–658PubMedCrossRefGoogle Scholar
  55. Singh RP, McIntosh RA (1987) Genetics of resistance to Puccinia graminis tritici in ‘Chris’ and ‘W3746’ wheats. Theor Appl Genet 73:846–855PubMedCrossRefGoogle Scholar
  56. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011a) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481PubMedCrossRefGoogle Scholar
  57. Singh RP, Huerta-Espino J, Bhavani S, Herrera-Foessel SA, Singh D, Singh PK, Velu G, Mason RE, Jin Y, Njau P, Crossa J (2011b) Race non-specific resistance to rust diseases in CIMMYT spring wheats. Euphytica 179:175–186CrossRefGoogle Scholar
  58. Singh A, Knox RE, DePauw RM, Singh AK, Cuthbert RD, Campbell HL, Singh D, Bhavani S, Fetch T, Clarke F (2013a) Identification and mapping in spring wheat of genetic factors controlling stem rust resistance and the study of their epistatic interactions across multiple environments. Theor Appl Genet 126:1951–1964PubMedCentralPubMedCrossRefGoogle Scholar
  59. Singh A, Pandey MP, Singh AK, Knox RE, Ammar K, Clarke JM, Clarke FR, Singh RP, Pozniak CJ, DePauw RM, McCallum BD, Cuthbert RD, Randhawa HS, Fetch TG Jr (2013b) Identification and mapping of leaf, stem and stripe rust resistance quantitative trait loci and their interactions in durum wheat. Mol Breeding 31:405–418CrossRefGoogle Scholar
  60. Singh S, Singh RP, Bhavani S, Huerta-Espino J, Lopez-Vera EE (2013c) QTL mapping of slow-rusting, adult plant resistance to race Ug99 of stem rust fungus in PBW343/Muu RIL population. Theor Appl Genet 126:1367–1375PubMedCrossRefGoogle Scholar
  61. Snape JW, Riggs TJ (1975) Genetical consequences of single seed descent in the breeding of self-pollinating crops. Heredity 35:211–219CrossRefGoogle Scholar
  62. Stakman EC, Steward DM, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. USDA Agric Res Serv E-617Google Scholar
  63. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org
  64. Tsilo TJ, Jin Y, Anderson JA (2007) Microsatellite markers linked to stem rust resistance allele Sr9a in wheat. Crop Sci 47:2013–2020CrossRefGoogle Scholar
  65. Tsilo TJ, Jin Y, Anderson JA (2008) Diagnostic microsatellite markers for the detection of stem rust resistance gene Sr36 in diverse genetic backgrounds of wheat. Crop Sci 48:253–261CrossRefGoogle Scholar
  66. Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
  67. Wanyera R, Kinyua MG, Jin Y, Singh RP (2006) The spread of stem rust caused by Puccinia graminis f. sp. tritici, with virulence on Sr31 in wheat in Eastern Africa. Plant Dis 90:113CrossRefGoogle Scholar
  68. Wu S, Pumphrey M, Bai G (2009) Molecular mapping of stem-rust-resistance gene Sr40 in wheat. Crop Sci 49:1682–1686CrossRefGoogle Scholar
  69. Young ND (1996) QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 34:479–501PubMedCrossRefGoogle Scholar
  70. Yu L, Lorenz A, Rutkoski J, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2011) Association mapping and gene–gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123:1257–1268PubMedCrossRefGoogle Scholar
  71. Yu L, Morgounov A, Wanyera R, Keser M, Singh SK, Sorrells M (2012) Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor Appl Genet 125:749–758PubMedCrossRefGoogle Scholar
  72. Yu L, Barbier H, Rouse MN, Singh S, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2014) A consensus map for Ug99 stem rust resistance loci in wheat. Theor Appl Genet. doi: 10.1007/s00122-014-2326-7 (companion paper)
  73. Zhang W, Olson EL, Saintenac C, Rouse M, Abate Z, Jin Y, Akhunov E, Pumphrey MO, Dubcovsky J (2010) Genetic maps of stem rust resistance gene Sr35 in diploid and hexaploid wheat. Crop Sci 50:2464–2474CrossRefGoogle Scholar
  74. Zheng ZB (1993) Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci USA 90:10972–10976CrossRefGoogle Scholar
  75. Zheng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2014

Authors and Affiliations

  • Matthew N. Rouse
    • 1
    • 2
  • Luther E. Talbert
    • 3
  • Davinder Singh
    • 4
    • 5
  • Jamie D. Sherman
    • 3
  1. 1.Cereal Disease Laboratory, United States Department of Agriculture-Agricultural Research Service (USDA-ARS)St. PaulUSA
  2. 2.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA
  3. 3.Department of Plant Sciences and Plant PathologyMontana State UniversityBozemanUSA
  4. 4.International Maize and Wheat Improvement Center (CIMMYT)MexicoMexico
  5. 5.Plant Breeding InstituteUniversity of SydneyNarellanAustralia

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