Molecular Breeding

, 35:170 | Cite as

QTL mapping of adult plant resistance to Ug99 stem rust in the spring wheat population RB07/MN06113-8

  • Prabin Bajgain
  • Matthew N. Rouse
  • Sridhar Bhavani
  • James A. Anderson


The emergence and spread of the Ug99 race group of the stem rust pathogen (Puccinia graminis Pers. f. sp. tritici) in the past decade have exposed the vulnerability of wheat (Triticum aestivum L.) to this disease. Discovery of novel and effective sources of resistance is vital for breeding resistant varieties to avert losses. The experimental breeding line MN06113-8 and cultivar RB07 developed by the University of Minnesota wheat breeding program exhibited adult plant resistance (APR) to the Ug99 race group in field tests in Kenya and Ethiopia. Both lines were found to be susceptible at the seedling stage to isolates of the race TTKSK, TTKST, and TTTSK. To dissect the genetic mechanism of resistance present in these lines, MN06113-8 was crossed to RB07 to generate 141 F6 recombinant inbred lines (RILs). The RIL population was evaluated for APR to Ug99 in Kenya and Ethiopia over three seasons and for resistance to North American stem rust pathogen races in St. Paul, MN, in one season. The population was genotyped using high-throughput SNP genotyping assays. Composite interval mapping detected six quantitative trait loci (QTL) involved in APR to African stem rust races and three QTLs involved in stem rust resistance to North American stem rust races. One QTL located on chromosome 2B was associated with APR to stem rust races in all environments. Development of diagnostic markers linked to this gene will facilitate marker-assisted selection of resistant lines to develop varieties with enhanced levels of stem rust resistance.


Linkage mapping Recombinant inbred lines Stem rust Ug99 Genotyping by sequencing Resistance breeding 



We thank the University of Minnesota Genomics Center, University of Minnesota Supercomputing Institute, the Microbial & Plant Genomics Institute, the University of Minnesota Graduate School, Kenya Agriculture and Livestock Research Organization, Ethiopia Institute of Agricultural Research, USDA-ARS Cereal Disease Laboratory personnel, and Anderson Wheat Lab for their help and support during various phases of the project. Funding for this work was provided by the United States Department of Agriculture, Agriculture and Food Research Initiative and 2011-68002-30029 (Triticeae Coordinated Agricultural Project,, the Borlaug Global Rust Initiative Durable Rust Resistance in Wheat Project (administered by Cornell University with a grant from the Bill & Melinda Gates Foundation), and the UK Department for International Development.

Author contribution

P.B. supervised planting of the RIL population in St. Paul, MN; recorded the phenotype of the RIL population in St. Paul, MN; carried out genotyping of the plant materials and data analysis; and drafted the manuscript. M.N.R. recorded the phenotype in East African nurseries and assisted in preparing the manuscript. S.B. supervised planting of and disease inoculation on the population in East African rust nurseries. J.A.A. conceived the study, developed the population, supervised the project, and assisted in preparing the manuscript. All authors contributed to and approved the final manuscript.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Human participants and/or animals statement

Not applicable.

Informed consent

Not applicable.

Supplementary material

11032_2015_362_MOESM1_ESM.xlsx (82 kb)
Supplementary material 1 (XLSX 81 kb)


  1. Anderson JA, Busch RH, Mcvey DV, Kolmer JA, Linkert GL, Wiersma JV, Dill-Macky R, Wiersma JJ, Hareland GA (2005) Registration of ‘Oklee’ wheat. Crop Sci 45:784–785CrossRefGoogle Scholar
  2. Anderson JA, Linkert GL, Busch RH, Wiersma JJ, Kolmer JA, Jin Y, Dill-Macky R, Wiersma JV, Hareland GA, McVey DV (2009) Registration of ‘RB07’ wheat. J Plant Regist 3(2):175–180. doi: 10.3198/jpr2008.08.0478crc CrossRefGoogle Scholar
  3. 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 Regist 6(2):180–185. doi: 10.3198/jpr2011.06.0339crc CrossRefGoogle Scholar
  4. Ayliffe M, Singh R, Lagudah E (2008) Durable resistance to wheat stem rust needed. Curr Opin Plant Biol 11(2):187–192. doi: 10.1016/j.pbi.2008.02.001 CrossRefPubMedGoogle Scholar
  5. Bansal U, Bariana H, Wong D, Randhawa M, Wicker T, Hayden M, Keller B (2014) Molecular mapping of an adult plant stem rust resistance gene Sr56 in winter wheat cultivar Arina. Theor Appl Genet 127(6):1441–1448. doi: 10.1007/s00122-014-2311-1 CrossRefPubMedGoogle Scholar
  6. Bhavani S, Singh RP, Argillier O, Huerta-Espino J, Singh S, Njau P, Brun S, Lacam S, Desmouceaux N (2011) Mapping durable adult plant stem rust resistance to the race Ug99 group in six CIMMYT wheats. In: McIntosh RA (ed) Proceedings of the Borlaug Global Rust Initiative 2011 technical workshop, June 13–16, 2011, Saint Paul, Minnesota. Borlaug Global Rust Initiative, Ithaca, NY, pp 43–53Google Scholar
  7. Bonnett DG, Rebetzke GJ, Spielmeyer W (2005) Strategies for efficient implementation of molecular markers in wheat breeding. Mol Breed 15(1):75–85. doi: 10.1007/s11032-004-2734-5 CrossRefGoogle Scholar
  8. Burdon JJ, Barrett LG, Rebetzke G, Thrall PH (2014) Guiding deployment of resistance in cereals using evolutionary principles. Evol Appl 7:609–624PubMedCentralCrossRefPubMedGoogle Scholar
  9. Busch RH, McVey DV, Linkert GL, Wiersma JV, Warnes DO, Wilcoxson RD, Hareland GA, Edwards I, Schmidt H (1996) Registration of ‘Verde’ wheat. Crop Sci 36:1418CrossRefGoogle Scholar
  10. Busch RH, McVey DV, Linkert GL, Wiersma JV, Dill-Macky R, Hareland GA, Edwards I, Schmidt HJ (2000) Registration of ‘HJ98’ wheat. Crop Sci 40:296–297CrossRefGoogle Scholar
  11. Carter AH, Chen XM, Garland-Campbell K, Kidwell KK (2009) Identifying QTL for high-temperature adult-plant resistance to stripe rust (Puccinia striiformis f. sp. tritici) in the spring wheat (Triticum aestivum L.) cultivar ‘Louise’. Theor Appl Genet 119(6):1119–1128. doi: 10.1007/s00122-009-1114-2 CrossRefPubMedGoogle Scholar
  12. Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci. doi: 10.1073/pnas.1217133110 Google Scholar
  13. Crossa J, Burgueño J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177(3):1889–1913. doi: 10.1534/genetics.107.078659 PubMedCentralCrossRefPubMedGoogle Scholar
  14. Dyck PL (1992) Transfer of a gene for stem rust resistance from Triticum araraticum to hexaploid wheat. Genome 35(5):788–792. doi: 10.1139/g92-120 CrossRefGoogle Scholar
  15. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6(5):e19379. doi: 10.1371/journal.pone.0019379 PubMedCentralCrossRefPubMedGoogle Scholar
  16. Evanega SD, Singh RP, Coffman R, Pumphrey MO (2014) The Borlaug Global Rust Initiative: reducing the genetic vulnerability of wheat to rust. In: Tuberosa R, Graner A, Frison E (eds) Genomics of plant genetic resources. Springer, Netherlands, pp 317–331. doi: 10.1007/978-94-007-7575-6_13 CrossRefGoogle Scholar
  17. Ghazvini H, Hiebert C, Zegeye T, Liu S, Dilawari M, Tsilo T, Anderson J, Rouse M, Jin Y, Fetch T (2012) Inheritance of resistance to Ug99 stem rust in wheat cultivar Norin 40 and genetic mapping of Sr42. Theor Appl Genet 125(4):817–824. doi: 10.1007/s00122-012-1874-y CrossRefPubMedGoogle Scholar
  18. Hare RA, McIntosh RA (1979) Genetic and cytogenetic studies of durable adult-plant resistances in Hope and related cultivars to wheat rusts. Zeitschrift für Pflanzenzüchtung 83:350–367Google Scholar
  19. Hayes HK, Ausemus ER, Stakman EC, Bailey CH, Wilson HK, Bamberg RH, Morkley MC, Crim RF, Levine MN (1936) Thatcher wheat. Stn Bull Minn Agric Exp Stn 325:1–36Google Scholar
  20. Herrera-Foessel S, Singh R, Lillemo M, Huerta-Espino J, Bhavani S, Singh S, Lan C, Calvo-Salazar V, Lagudah E (2014) Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor Appl Genet 127(4):781–789. doi: 10.1007/s00122-013-2256-9 CrossRefPubMedGoogle Scholar
  21. Hiebert C, Fetch T Jr, Zegeye T (2010) Genetics and mapping of stem rust resistance to Ug99 in the wheat cultivar Webster. Theor Appl Genet 121(1):65–69. doi: 10.1007/s00122-010-1291-z CrossRefPubMedGoogle Scholar
  22. Hodson DP, Nazari K, Park RF, Hansen J, Lassen P, Arista J, Fetch T, Hovmøller M, Jin Y, Pretorius ZA, Sonder K (2011) Putting Ug99 on the map: an update on current and future monitoring. In: McIntosh RA (ed) Borlaug Global Rust Initiative 2011 technical workshop. Borlaug Global Rust Initiative, St Paul, pp 3–13Google Scholar
  23. Jin Y, Singh RP, Ward RW, Wanyera R, Kinyua M, Njau P, Fetch T, 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(9):1096–1099. doi: 10.1094/PDIS-91-9-1096 CrossRefGoogle Scholar
  24. Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92(6):923–926. doi: 10.1094/PDIS-92-6-0923 CrossRefGoogle Scholar
  25. Jin Y, Szabo LJ, Rouse MN, Fetch T, 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
  26. Kaur J, Bansal U, Khanna R, Saini R, Bariana H (2009) Molecular mapping of stem rust resistance in HD2009/WL711 recombinant inbred line population. Int J Plant Breed 3:28–33Google Scholar
  27. Kerber ER, Dyck PL (1990) Transfer to hexaploid wheat of linked genes for adult-plant leaf rust and seedling stem rust resistance from an amphiploid of Aegilops speltoides × Triticum monococcum. Genome 33(4):530–537. doi: 10.1139/g90-079 CrossRefGoogle Scholar
  28. Kidwell K, Osborn T (1992) Simple plant DNA isolation procedures. In: Beckmann JS, Osborn TC (eds) Plant genomes: methods for genetic and physical mapping. Springer, Netherlands, pp 1–13. doi: 10.1007/978-94-011-2442-3_1 CrossRefGoogle Scholar
  29. Kislev ME (1982) Stem rust of wheat 3300 years old found in Israel. Science 216(4549):993–994. doi: 10.1126/science.216.4549.993 CrossRefPubMedGoogle Scholar
  30. 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: Genes|Genomes|Genetics 2(6):665–673. doi: 10.1534/g3.112.002386
  31. Knott DR (1968) The inheritance of resistance to stem rust races 56 and 15B-IL (Can.) in the wheat varieties Hope and H-44. Can J Genet Cytol 10(2):311–320. doi: 10.1139/g68-043 CrossRefGoogle Scholar
  32. Knott DR (1982) Multigenic inheritance of stem rust resistance in wheat. Crop Sci 22(2):393–399. doi: 10.2135/cropsci1982.0011183X002200020045x CrossRefGoogle Scholar
  33. Knott DR (1989) The wheat rusts—breeding for resistance. Theor Appl Genet 12:1–201. doi: 10.1007/978-3-642-83641-1 CrossRefGoogle Scholar
  34. Knott DR (2001) The relationship between seedling and field resistance to two races of stem rust in Thatcher wheat. Can J Plant Sci 81(3):415–418. doi: 10.4141/P00-027 CrossRefGoogle Scholar
  35. 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
  36. Kosambi DD (1943) The estimation of map distance from recombination values. Ann Eugenics 12(1):172–175. doi: 10.1111/j.1469-1809.1943.tb02321.x CrossRefGoogle Scholar
  37. 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(1):21–30. doi: 10.1007/s00122-006-0406-z CrossRefPubMedGoogle Scholar
  38. Liu W, Rouse M, Friebe B, Jin Y, Gill B, Pumphrey M (2011) 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(5):669–682. doi: 10.1007/s10577-011-9226-3 CrossRefPubMedGoogle Scholar
  39. Lorieux M (2012) MapDisto: fast and efficient computation of genetic linkage maps. Mol Breed 30(2):1231–1235. doi: 10.1007/s11032-012-9706-y CrossRefGoogle Scholar
  40. Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9(1):e1003215. doi: 10.1371/journal.pgen.1003215 PubMedCentralCrossRefPubMedGoogle Scholar
  41. Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen X, Pumphrey M, Dubcovsky J (2015) A genome-wide association study of resistance to stripe rust (Puccinia striiformis f. sp. tritici) in a worldwide collection of hexaploid spring wheat (Triticum aestivum L.). G3 Genes|Genomes|Genetics 5(3):449–465. doi: 10.1534/g3.114.014563
  42. Mago R, Lawrence G, Ellis J (2011) The application of DNA marker and doubled-haploid technology for stacking multiple stem rust resistance genes in wheat. Mol Breed 27(3):329–335. doi: 10.1007/s11032-010-9434-0 CrossRefGoogle Scholar
  43. McIntosh RA, Gyarfas J (1971) Triticum timopheevi as a source of resistance to wheat stem rust. Zeitschrift für Pflanzenzüchtung 66:240–248Google Scholar
  44. McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO Publications, VictoriaCrossRefGoogle Scholar
  45. McIntosh RA, Yamazaki Y, Devos KM, Dubcovsky J, Rogers WJ, Appels R (2003) Catalogue of gene symbols for wheat. In: Pogna NE, Romano M, Pogna EA, Galterio (eds) Proceedings of the 10th international wheat genetics symposium, 1–6 September, 2003, Paestum, Italy. Istituto Sperimentale per la Cerealicoltura, Rome, pp 1–34Google Scholar
  46. Mundt CC (2014) Durable resistance: a key to sustainable management of pathogens and pests. Infect Genet Evol 27:446–455. doi: 10.1016/j.meegid.2014.01.011 CrossRefPubMedGoogle Scholar
  47. Nazareno NRX, Roelfs AP (1981) Adult plant resistance of Thatcher wheat to stem rust. Phytopathology 71:181–185CrossRefGoogle Scholar
  48. 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 187:1011–1021. doi: 10.1534/genetics.110.123588 PubMedCentralCrossRefPubMedGoogle Scholar
  49. 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(4):413–419. doi: 10.1094/PDIS-94-4-0413 CrossRefGoogle Scholar
  50. Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity of leaves and stem of cereals. Can J Res 26c(5):496–500. doi: 10.1139/cjr48c-033
  51. Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a aovel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7(2):e32253. doi: 10.1371/journal.pone.0032253 PubMedCentralCrossRefPubMedGoogle Scholar
  52. Pozniak CJ, Reimer S, Fetch T, Clarke JM, Clarke FR, Somers DJ, Knox RE, Singh AK (2008) Association mapping of Ug99 resistance in diverse durum wheat population. In: Rudi A, Russell E, Peter L, Michael M, Lynne M, Peter S (eds) Proceedings of the 11th international wheat genetics symposium, 24–29 August, 2008, Brisbane, Australia. Sydney University Press, Sydney, pp 809–811Google Scholar
  53. 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 84:203Google Scholar
  54. 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(4):590. doi: 10.1094/PDIS-12-11-1027-PDN CrossRefGoogle Scholar
  55. Prins R, Pretorius ZA, Bender CM, Lehmensiek A (2011) QTL mapping of stripe, leaf and stem rust resistance genes in a Kariega × Avocet S doubled haploid wheat population. Mol Breed 27(2):259–270. doi: 10.1007/s11032-010-9428-y CrossRefGoogle Scholar
  56. Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J, Hensel G, Viccars LA, Richardson TM, Buesing G, Troller A, Lagudah ES, Keller B (2013) The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnol J 11(7):847–854. doi: 10.1111/pbi.12077 CrossRefPubMedGoogle Scholar
  57. Roelfs AP (1985) Wheat and rye stem rust. In: Roelfs AP, Bushnell WR (eds) The cereal rusts, vol 2. Academic Press, Orlando, pp 3–37Google Scholar
  58. Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat: concepts and methods of disease management. CIMMYT, MexicoGoogle Scholar
  59. Rouse MN, Jin Y (2011) Stem rust resistance in A-genome diploid relatives of wheat. Plant Dis 95:941–944CrossRefGoogle Scholar
  60. Rouse M, Nava I, Chao S, Anderson J, 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(5):877–885. doi: 10.1007/s00122-012-1879-6 CrossRefPubMedGoogle Scholar
  61. Rouse MN, Nirmala J, Jin Y, Chao S, Fetch TG Jr, Pretorius ZA, Hiebert CW (2014a) Characterization of Sr9h, a wheat stem rust resistance allele effective to Ug99. Theor Appl Genet 127(8):1681–1688. doi: 10.1007/s00122-014-2330-y CrossRefPubMedGoogle Scholar
  62. Rouse MN, Talbert LE, Singh D, Sherman JD (2014b) Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in Thatcher wheat (Triticum aestivum L.). Theor Appl Genet 127(7):1549–1559. doi: 10.1007/s00122-014-2319-6 CrossRefPubMedGoogle Scholar
  63. Singh RP (2012) Pros and cons of utilizing major, race-specific resistance genes versus partial resistance in breeding rust resistant wheat. In: McIntosh RA (ed) Borlaug Global Rust Initiative 2012 technical workshop. International Maize and Wheat Improvement Center (CIMMYT), Beijing, pp 57–65Google Scholar
  64. Singh RP, Huerta EJ, Manilal HM (2005) Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric For 29:121–127Google Scholar
  65. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, Wanyera R, Herrera-Foessel SA, Ward RW (2008) Will stem rust destroy the world’s wheat crop? In: Donald LS (ed) Advances in agronomy, vol 98. Academic Press, pp 271–309. doi: 10.1016/S0065-2113(08)00205-8
  66. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49(1):465–481. doi: 10.1146/annurev-phyto-072910-095423 CrossRefPubMedGoogle Scholar
  67. 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(8):1951–1964. doi: 10.1007/s00122-013-2109-6 PubMedCentralCrossRefPubMedGoogle Scholar
  68. 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 Breed 31(2):405–418. doi: 10.1007/s11032-012-9798-4 PubMedCentralCrossRefPubMedGoogle Scholar
  69. Singh RP, Herrera-Foessel SA, Huerta-Espino J, Lan CX, Basnet BR, Bhavani S, Lagudah ES (2013c) Pleiotropic gene Lr46/Yr29/Pm39/Ltn2 confers slow rusting, adult plant resistance to wheat stem rust fungus. In: Borlaug Global Rust Initiative 2013 technical workshop. New Delhi, India, p 17Google Scholar
  70. Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. US Dep Agric Agric Res Serv E 6/7Google Scholar
  71. Stubbs RW, Prescott JM, Saari EE, Dubin HJ (1986) Cereal disease methodology manual. CIMMYT, MexicoGoogle Scholar
  72. Stuthman DD, Leonard KJ, Miller‐Garvin J (2007) Breeding crops for durable resistance to disease. In: Donald LS (ed) Advances in agronomy, vol 95. Academic Press, pp 319–367. doi: 10.1016/S0065-2113(07)95004-X
  73. Suenaga K, Singh RP, Huerta-Espino J, William HM (2003) Microsatellite markers for genes Lr34/Yr18 and other quantitative trait Loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology 93(7):881–890. doi: 10.1094/phyto.2003.93.7.881 CrossRefPubMedGoogle Scholar
  74. 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(1):253–261. doi: 10.2135/cropsci2007.04.0204 CrossRefGoogle Scholar
  75. Tsilo TJ, Kolmer JA, Anderson JA (2014) Molecular mapping and improvement of leaf rust resistance in wheat breeding lines. Phytopathology 104(8):865–870. doi: 10.1094/PHYTO-10-13-0276-R PubMedGoogle Scholar
  76. Wang S, Basten CJ, Zeng Z-B (2012) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NCGoogle Scholar
  77. 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(1):113. doi: 10.1094/PD-90-0113A CrossRefGoogle Scholar
  78. William M, Singh RP, Huerta-Espino J, Islas SO, Hoisington D (2003) Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology 93(2):153–159. doi: 10.1094/phyto.2003.93.2.153 CrossRefPubMedGoogle Scholar
  79. Wu S, Pumphrey M, Bai G (2009) Molecular mapping of stem-rust-resistance gene Sr40 in wheat. Crop Sci 49(5):1681–1686. doi: 10.2135/cropsci2008.11.0666 CrossRefGoogle Scholar
  80. Yu L-X, Lorenz A, Rutkoski J, Singh R, Bhavani S, Huerta-Espino J, Sorrells M (2011) Association mapping and gene–gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theor Appl Genet 123(8):1257–1268. doi: 10.1007/s00122-011-1664-y CrossRefPubMedGoogle Scholar
  81. Yu L-X, Morgounov A, Wanyera R, Keser M, Singh S, Sorrells M (2012) Identification of Ug99 stem rust resistance loci in winter wheat germplasm using genome-wide association analysis. Theor Appl Genet 125(4):749–758. doi: 10.1007/s00122-012-1867-x CrossRefPubMedGoogle Scholar
  82. Yu L-X, Barbier H, Rouse M, Singh S, Singh R, Bhavani S, Huerta-Espino J, Sorrells M (2014) A consensus map for Ug99 stem rust resistance loci in wheat. Theor Appl Genet 127(7):1561–1581. doi: 10.1007/s00122-014-2326-7 PubMedCentralCrossRefPubMedGoogle Scholar
  83. Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14(6):415–421. doi: 10.1111/j.1365-3180.1974.tb01084.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of Agronomy and Plant GeneticsUniversity of MinnesotaSt. PaulUSA
  2. 2.Cereal Disease LaboratoryUnited States Department of Agriculture-Agricultural Research Service (USDA-ARS)St. PaulUSA
  3. 3.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA
  4. 4.International Maize and Wheat Improvement Center (CIMMYT)ICRAF HouseNairobiKenya

Personalised recommendations