Theoretical and Applied Genetics

, Volume 131, Issue 9, pp 1835–1849 | Cite as

Combination of all-stage and high-temperature adult-plant resistance QTL confers high-level, durable resistance to stripe rust in winter wheat cultivar Madsen

  • L. Liu
  • M. N. Wang
  • J. Y. Feng
  • D. R. See
  • S. M. Chao
  • X. M. ChenEmail author
Original Article


Key message

Wheat cultivar Madsen has a new gene on the short arm of chromosome 1A and two QTL for all-stage resistance and three QTL for high-temperature adult-plant resistance that in combination confer high-level, durable resistance to stripe rust.


Wheat cultivar Madsen has maintained a high-level resistance to stripe rust over 30 years. To map quantitative trait loci (QTL) underlying the high-level, durable resistance, 156 recombinant inbred lines (RILs) developed from cross Avocet S × Madsen were phenotyped with selected races of Puccinia striiformis f. sp. tritici in the greenhouse seedling tests, and in naturally infected fields during 2015–2017. The RILs were genotyped by SSR and SNP markers from genotyping by sequencing and the 90 K wheat SNP chip. Three QTL for all-stage resistance were mapped on chromosomes 1AS, 1BS and 2AS, and two QTL for high-temperature adult-plant (HTAP) resistance were mapped on 3BS and 6BS. The most effective QTL on 2AS, explaining 8.97–23.10% of the phenotypic variation in seedling tests and 8.60–71.23% in field tests, contained Yr17 for all-stage resistance and an additional gene for HTAP resistance. The 6BS QTL, detected in all field tests, was identified as Yr78. The 1AS QTL, conferring all-stage resistance, was identified as a new gene, which explained 20.45 and 30.23% of variation in resistance to races PSTv-37 and PSTv-40, respectively, and contributed significantly to field resistance at Pullman in 2015-2017, but was not detected at Mount Vernon. The interactions among QTL were mostly additive, and RILs with all five QTL had the highest level of resistance in the field, similar to Madsen. Genotyping 148 US Pacific Northwest wheat cultivars with markers for the 1AS, 2AS and 6BS QTL validated the genes and markers, and indicated their usefulness for marker-assisted selection.



This research was supported by the US Department of Agriculture, Agricultural Research Service (Project No. 2090-22000-018-00D), Vogel Foundation (Project No. 13Z-3061-6665), Washington Grain Commission (Project No. 13C-3061-5665) and Washington State University, Department of Plant Pathology, College of Agricultural, Human, and Natural Resource Sciences, Agricultural Research Center, HATCH Project Number WNP00461, Washington State University, Pullman, WA 99164-6430, USA. We would like to thank the International Wheat Genome Sequencing Consortium (IWGSC) for allowing us to use the online data. The China Scholarship Council scholarship to Lu Liu is highly appreciated. We thank Arron Carter, Dennis Johnson and Robert McIntosh for critical reviewing the manuscript.

Author contribution statement

LL developed the mapping population, extracted DNA, conducted all experiments of phenotyping and genotyping the mapping population, analyzed the data, validated markers, and drafted and revised the manuscript. MNW participated in the development of the mapping population, phenotyping and genotyping and revised the manuscript. JYF made the cross and developed the early generations. DRS provided equipment and guidance for SSR and KASP marker analyses and revised the manuscript. SMC performed the 90 K SNP genotyping and initial analysis. XMC developed the project, designed experiments, guided through the entire study, write and revised the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that there is no conflict of interest.

Ethical standards

All experiments and data analyses were conducted in Pullman and Mount Vernon, Washington, and the 90 K SNP genotype was done in Fargo, North Dakota, the USA. All authors have contributed to the study and approved the version for submission. The manuscript has not been submitted to any other journal.

Supplementary material

122_2018_3116_MOESM1_ESM.pptx (2.6 mb)
Seedling reactions of Madsen to different races of Puccinia striiformis f. sp. tritici and field reactions of AvS and Madsen (PPTX 2692 kb)
122_2018_3116_MOESM2_ESM.docx (23 kb)
Mean infection type (IT) and disease severity (DS) of AvS and Madsen at different growth stages tested in fields subjected to natural infection by Puccinia striiformis f. sp. tritici (DOCX 22 kb)
122_2018_3116_MOESM3_ESM.docx (292 kb)
Molecular markers mapped to chromosomes in AvS × Madsen (DOCX 292 kb)
122_2018_3116_MOESM4_ESM.docx (22 kb)
T test statistics for relative area under the disease progress curve (rAUDPC) and infection type (IT) data of spring and winter wheat lines in all environments (DOCX 21 kb)
122_2018_3116_MOESM5_ESM.docx (79 kb)
Alleles (bp) of SSR and PCR markers and haplotypes of SNP markers within the regions of QYrMa.wgp-2AS (marker VENTRIUP/LN2, V/LN2), QYrMa.wgp-6BS (Xbarc146 and Xbarc136) and QYrMa.wgp-1AS (Xcfa2153, IWB54411, IWB12795 and IWA5150) locus in Madsen, AvS, Chinese Spring, and 148 US Pacific Northwest wheat cultivars and breeding lines (DOCX 78 kb)
122_2018_3116_MOESM6_ESM.docx (32 kb)
Putative resistance genes in the IWB7628-IWB12795 region covering QTL QYrMa.wgp-1AS and putative genes matching SNP markers in the region based on BLAST searching of the Zavitan genome sequences (the International Wild Emmer Wheat Genome Sequencing Consortium, WEWseq; (DOCX 31 kb)
122_2018_3116_MOESM7_ESM.docx (20 kb)
Co-segregating SNPs of the SNP markers within stripe rust resistance QTL on wheat chromosomes 1AS, 1BS, 2AS, 3BS and 6BS shown in Fig. 3 (DOCX 19 kb)


  1. Allan RE, Peterson CJ, Rubenthaler GL, Line RF, Roberts DE (1989) Registration of “Madsen’ wheat. Crop Sci 29:1575–1576CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Shäffer AA, Zhang JH, Zhang Z, Miller W, Lipman GJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedCentralPubMedGoogle Scholar
  3. Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan K, Golan G, Faris J, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97CrossRefPubMedGoogle Scholar
  4. Bariana HS, McIntosh RA (1993) Cytogenetic studies in wheat. XV. Location of rust resistance genes in VPM1 and their genetic linkage with other disease resistance genes in chromosome 2A. Genome 36:476–482CrossRefPubMedGoogle Scholar
  5. Bariana HS, Bansal UK, Schmidt A, Lehmensiek A, Kaur J, Miah H, Howes N, McIntyre CL (2010) Molecular mapping of adult plant stripe rust resistance in wheat and identification of pyramided QTL genotypes. Euphytica 176:251–260CrossRefGoogle Scholar
  6. Case AJ, Naruoka Y, Chen X, Garland-Campbell KA, Zemetra RS, Carter AH (2014) Mapping stripe rust resistance in a Brundage × Coda winter wheat recombinant inbred line population. PLoS ONE 9:e91758CrossRefPubMedCentralPubMedGoogle Scholar
  7. Chen XM (2005) Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can J Plant Pathol 27:314–337CrossRefGoogle Scholar
  8. Chen XM (2013) High-temperature adult-plant resistance, key for sustainable control of stripe rust. Am. J. Plant Sci 4:608–627CrossRefGoogle Scholar
  9. Chen XM (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Can J Plant Pathol 36:311–326CrossRefGoogle Scholar
  10. Chen XM, Line RF (1992) Inheritance of stripe rust resistance in wheat cultivars used to differentiate races of Puccinia striiformis in North America. Phytopathology 82:633–637CrossRefGoogle Scholar
  11. Chen XM, Line RF (1995) Gene action in wheat cultivars for durable high-temperature adult-plant resistance and interactions with race-specific, seedling resistance to stripe rust caused by Puccinia striiformis. Phytopathology 85:567–572CrossRefGoogle Scholar
  12. Chen JL, Chu C, Souza EJ, Guttieri MJ, Chen XM, Xu S, Hole D, Zemetra R (2012) Genome-wide identification of QTL conferring high-temperature adult-plant (HTAP) resistance to stripe rust (Puccinia striiformis f. sp. tritici) in wheat. Mol Breed 29:791–800CrossRefGoogle Scholar
  13. Chen XM, Evans KC, Liu YM (2014) Control of stripe rust on winter wheat cultivars with foliar fungicide in 2013. Plant Dis Manag Rep 8:CF35Google Scholar
  14. Chen XM, Evans CK, Liu YM, Heath M (2015) Effects of fungicide application on control of stripe rust on winter wheat cultivars in 2014. Plant Dis Manag Rep 9:CF017Google Scholar
  15. Chen XM, Evans CK, Liu YM (2016) Responses of winter wheat cultivars to fungicide application for control of stripe rust in 2015. Plant Dis Manag Rep 10:C023Google Scholar
  16. Cheng P, Xu LS, Wang MN, See DR, Chen XM (2014) Molecular mapping of genes Yr64 and Yr65 for stripe rust resistance in hexaploid derivatives of durum wheat accessions PI 331260 and PI 480016. Theor Appl Genet 127:2267–2277CrossRefPubMedGoogle Scholar
  17. Churchill G, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedCentralPubMedGoogle Scholar
  18. Clarke JD (2002) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. In: Weigel D, Glazebrook J (eds) Arabidopsis: A Laboratory Manual. CSHL Press. Cold Spring Harbor, NY, USAGoogle Scholar
  19. Dedryver F, Paillard S, Mallard S, Robert O, Trottet M, Nègre S, Verplancke G, Jahier J (2009) Characterization of genetic components involved in durable resistance to stripe rust in the bread wheat “Renan”. Phytopathology 99:968–973CrossRefPubMedGoogle Scholar
  20. Dong ZZ, Hegarty JM, Zhang JL, Zhang WJ, Chao SM, Chen XM, Zhou YH, Dubcovsky J (2017) Validation and characterization of a QTL for adult plant resistance to stripe rust on wheat chromosome arms 6BS (Yr78). Theor Appl Genet 130:2127–2137CrossRefPubMedCentralPubMedGoogle Scholar
  21. Godoy J, Rynearson S, Chen XM, Pumphrey M (2018) Genome-wide association mapping of loci for resistance to stripe rust in North American elite spring wheat germplasm. Phytopathology. CrossRefPubMedGoogle Scholar
  22. Helguera M, Khan IA, Kolmer J, Lijavetzky D, Zhong-qi L, Dubcovsky J (2003) PCR assays for the Lr37-Yr17-Sr38 cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Sci 43:1839–1847CrossRefGoogle Scholar
  23. Hou L, Chen XM, Wang MN, See DR, Chao SM, Bulli P, Jing JX (2015) Mapping a large number of QTL for durable resistance to stripe rust in winter wheat Druchamp using SSR and SNP markers. PLoS ONE 10:e0126794CrossRefPubMedCentralPubMedGoogle Scholar
  24. Kandel JS, Krishnan V, Jiwan D, Chen XM, Skinner DZ, See DR (2017) Mapping genes for resistance to stripe rust in spring wheat landrace PI 480035. PLoS ONE 12:e0177898CrossRefGoogle Scholar
  25. Lan CX, Liang SS, Zhou XC, Zhou G, Lu QL, Xia XC, He ZH (2010) Identification of genomic regions controlling adult-plant stripe rust resistance in Chinese landrace Pingyuan 50 through bulked segregant analysis. Phytopathology 100:313–318CrossRefPubMedGoogle Scholar
  26. Lan CX, Zhang YL, Herrera-Foessel SA, Basnet BR, Huerta-Espino J, Lagudah ES, Singh RP (2015) Identification and characterization of pleiotropic and co-located resistance loci to leaf rust and stripe rust in bread wheat cultivar Sujata. Theor Appl Genet 128:549–561CrossRefPubMedGoogle Scholar
  27. Lin F, Chen XM (2009) Quantitative trait loci for non-race-specific, high-temperature adult-plant resistance to stripe rust in wheat cultivar Express. Theor Appl Genet 118:631–642CrossRefPubMedGoogle Scholar
  28. Line RF, Chen XM (1995) Successes in breeding for and managing durable resistance to wheat rusts. Plant Dis 79:1254–1255Google Scholar
  29. 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. U.S. Department of Agriculture Technical Bulletin No. 1788, the national Technical Information Service, Springfield, p 44Google Scholar
  30. Liu TL, Wan AM, Liu DC, Chen XM (2017) Changes of races and virulence genes of Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen, in the United States from 1968 to 2009. Plant Dis 101:1522–1532CrossRefGoogle Scholar
  31. Liu W, Naruoka Y, Miller K, Garland-Campbell KA, Carter AH (2018) Characterizing and validating stripe rust resistance loci in US Pacific Northwest winter wheat accessions (Triticum aestivum L.) by genome-wide association and linkage mapping. Plant. Genome 11:170087Google Scholar
  32. Lu Y, Wang MN, Chen XM, See D, Chao SM, Jing JX (2014) Mapping of Yr62 and a small-effect QTL for high-temperature adult-plant resistance to stripe rust in spring wheat PI 192252. Theor Appl Genet 127:1449–1459CrossRefPubMedGoogle Scholar
  33. Naruoka Y, Garland-Campbell KA, Carter AH (2015) Genome-wide association mapping for stripe rust (Puccinia striiformis f. sp. tritici) in US Pacific Northwest winter wheat (Triticum aestivum L.). Theor Appl Genet 128:1083–1101CrossRefPubMedGoogle Scholar
  34. Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:e32253CrossRefPubMedCentralPubMedGoogle Scholar
  35. Quan W, Hou GL, Chen J, Du ZY, Lin F, Guo Y, Liu S, Zhang ZJ (2013) Mapping of QTL lengthening the latent period of Puccinia striiformis in winter wheat at the tillering growth stage. Eur J Plant Pathol 136:715–727CrossRefGoogle Scholar
  36. Ramirez-Gonzalez RH, Segovia V, Bird N, Fenwick P, Holdgate S, Berry S, Jack P, Caccamo M, Uauy C (2014) RNA-Seq bulked segregant analysis enables the identification of high-resolution genetic markers for breeding in hexaploid wheat. Plant Biotechnol J 13:613–624CrossRefPubMedGoogle Scholar
  37. Santra DK, Chen XM, Santra M, Garland-Campbell KA, Kidwell KK (2008) Identification and mapping QTL for high-temperature adult-plant resistance to stripe rust in winter wheat (Triticum aestivum L.) cultivar ‘Stephens’. Theor Appl Genet 117:793–802CrossRefPubMedGoogle Scholar
  38. Santra DK, Santra M, Allan RE, Campbell KG, Kidwell KK (2009) Genetic and molecular characterization of vernalization genes Vrn-A1, Vrn-B1, and Vrn-D1 in spring wheat germplasm from the Pacific Northwest region of the USA. Plant Breed 128:576–584CrossRefGoogle Scholar
  39. Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114CrossRefPubMedGoogle Scholar
  40. Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V, WageningenGoogle Scholar
  41. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  42. Wan AM, Chen XM (2014) Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. Plant Dis 98:1534–1542CrossRefGoogle Scholar
  43. Wan AM, Chen XM, Yuen J (2016) Races of Puccinia striiformis f. sp. tritici in the United States in 2011 and 2012 and comparison with races in 2010. Plant Dis 100:966–975CrossRefGoogle Scholar
  44. Wang MN, Chen XM (2017) Stripe rust resistance. In: Chen XM, Kang ZS (eds) Stripe rust. Springer, Dordrecht, pp 39–444. CrossRefGoogle Scholar
  45. Wang S, Basten CJ, Zeng Z-B (2007) Windows QTL Cartographer 2.5. Department of Statistics. North Carolina State University, Raleigh, NC, USAGoogle Scholar
  46. Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796CrossRefPubMedCentralPubMedGoogle Scholar
  47. Wellings CR (2011) Global status of stripe rust: a review of historical and current threats. Euphytica 179:129–141CrossRefGoogle Scholar
  48. William HM, Singh RP, Huerta-Espino J, Palacios G, Suenaga K (2006) Characterization of genetic loci conferring adult plant resistance to leaf rust and stripe rust in spring wheat. Genome 49:977–990CrossRefPubMedGoogle Scholar
  49. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. PNAS 100:6263–6268CrossRefPubMedGoogle Scholar
  50. Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1458PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature (Outside the USA) 2018

Authors and Affiliations

  1. 1.Department of Plant PathologyWashington State UniversityPullmanUSA
  2. 2.Institute of Biotechnology and Nuclear Technology ResearchSichuan Academy of Agricultural SciencesChengduChina
  3. 3.Wheat Health, Genetics and Quality Research UnitUSDA-ARSPullmanUSA
  4. 4.Cereal Crops ResearchUSDA-ARSFargoUSA

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