Skip to main content
Log in

Genome-wide association mapping for seedling and field resistance to Puccinia striiformis f. sp. tritici in elite durum wheat

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Genome-wide association analysis in tetraploid wheat revealed novel and diverse loci for seedling and field resistance to stripe rust in elite spring durum wheat accessions from worldwide.

Abstract

Improving resistance to stripe rust, caused by Puccinia striiformis f. sp. tritici, is a major objective for wheat breeding. To identify effective stripe rust resistance loci, a genome-wide association study (GWAS) was conducted using 232 elite durum wheat (Triticum turgidum ssp. durum) lines from worldwide breeding programs. Genotyping with the 90 K iSelect wheat single nucleotide polymorphism (SNP) array resulted in 11,635 markers distributed across the genome. Response to stripe rust infection at the seedling stage revealed resistant and susceptible accessions present in rather balanced frequencies for the six tested races, with a higher frequency of susceptible responses to United States races as compared to Italian races (61.1 vs. 43.1% of susceptible accessions). Resistance at the seedling stage only partially explained adult plant resistance, which was found to be more frequent with 67.7% of accessions resistant across six nurseries in the United States. GWAS identified 82 loci associated with seedling stripe rust resistance, five of which were significant at the false discovery rate adjusted P value <0.1 and 11 loci were detected for the field response at the adult plant stages in at least two environments. Notably, Yrdurum-1BS.1 showed the largest effect for both seedling and field resistance, and is therefore considered as a major locus for resistance in tetraploid wheat. Our GWAS study is the first of its kind for stripe rust resistance in tetraploid wheat and provides an overview of resistance in elite germplasm and reports new loci that can be used in breeding resistant cultivars.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Able J, Atienza S (2014) Durum wheat for the future: challenges, research and prospects in the 21st century. Crop Pasture Sci 65:1–124

    Google Scholar 

  • Agenbag G, Pretorius Z, Boyd L, Bender C, Prins R (2012) Identification of adult plant resistance to stripe rust in the wheat cultivar Cappelle–Desprez. Theor Appl Genet 125:109–120

    Article  CAS  PubMed  Google Scholar 

  • Atlija M, Arranz J-J, Martinez-Valladares M, Gutiérrez-Gil B (2016) Detection and replication of QTL underlying resistance to gastrointestinal nematodes in adult sheep using the ovine 50 K SNP array. Genet Sel Evol 48:1

    Article  Google Scholar 

  • Badebo A, Gelalcha S, Ammar K, Nachit M, Abdalla O, McIntosh R (2009) Overview of durum wheat research in Ethiopia: challenges and prospects. Proceedings, oral papers and posters, 2009 Technical Workshop, Borlaug Global Rust Initiative, Cd Obregón, Sonora, Mexico, 17–20 March, 2009. Borlaug Global Rust Initiative, 143–149

  • Bansal UK, Kazi AG, Singh B, Hare RA, Bariana HS (2014) Mapping of durable stripe rust resistance in a durum wheat cultivar Wollaroi. Mol Breed 33:51–59

    Article  CAS  Google Scholar 

  • Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265

    Article  CAS  PubMed  Google Scholar 

  • Berger GL, Liu S, Hall MD, Brooks WS, Chao S, Muehlbauer GJ, Baik B-K, Steffenson B, Griffey CA (2013) Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 126:693–710

    Article  CAS  PubMed  Google Scholar 

  • Bulli P, Zhang J, Chao S, Chen X, Pumphrey M (2016) Genetic architecture of resistance to stripe rust in a global winter wheat germplasm collection. G3: Genes| Genomes| Genet 116:028407

    Google Scholar 

  • Bůžková P (2013) Linear regression in genetic association studies. PLoS One 8:e56976

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci 110:8057–8062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Can J Plant Pathol 27:314–337

    Article  Google Scholar 

  • Chen X (2007) Challenges and solutions for stripe rust control in the United States. Crop Pasture Sci 58:648–655

    Article  Google Scholar 

  • Chen X (2013) High-temperature adult-plant resistance, key for sustainable control of stripe rust. Am J Plant Sci 4:608–627

    Article  Google Scholar 

  • Chen X (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Can J Plant Pathol 36:311–326

    Article  CAS  Google Scholar 

  • Chen X, Jones SS, Line RF (1996) Chromosomal location of genes for resistance to Puccinia striiformis in seven wheat cultivars with resistance genes at the Yr3 and Yr4 loci. Phytopathology 86:1228–1233

    Article  CAS  Google Scholar 

  • Chen X, 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

    Article  Google Scholar 

  • Chen J, Chu C, Souza EJ, Guttieri MJ, Chen X, 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 29:791–800

    Article  CAS  Google Scholar 

  • Cheng P, Chen X (2010) Molecular mapping of a gene for stripe rust resistance in spring wheat cultivar IDO377s. Theor Appl Genet 121:195–204

    Article  CAS  PubMed  Google Scholar 

  • Cheng P, Xu L, Wang M, See D, Chen X (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 127:2267–2277

    Article  CAS  PubMed  Google Scholar 

  • Christopher MD, Liu S, Hall MD, Marshall DS, Fountain MO, Johnson JW, Milus EA, Garland-Campbell KA, Chen X, Griffey CA (2013) Identification and mapping of adult plant stripe rust resistance in soft red winter wheat VA00 W-38. Crop Sci 53:871–879

    Article  Google Scholar 

  • Cordell HJ (2009) Detecting gene–gene interactions that underlie human diseases. Nat Rev Genet 10:392–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 99:968–973

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Uauy C, Fahima T, Dubcovsky J (2006) Physical map of the wheat high-grain protein content gene Gpc-B1 and development of a high-throughput molecular marker. New Phytol 169:753–763

    Article  CAS  PubMed  Google Scholar 

  • Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014) The past, present and future of breeding rust resistant wheat. Front Plant Sci 5:641

    Article  PubMed  PubMed Central  Google Scholar 

  • Etzel C, Shete S, Beasley T, Fernandez J, Allison D, Amos C (2003) Effect of Box–Cox transformation on power of Haseman–Elston and maximum-likelihood variance components tests to detect quantitative trait loci. Hum Hered 55:108–116

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang DD, Hinze LL, Percy RG, Li P, Deng D, Thyssen G (2013) A microsatellite-based genome-wide analysis of genetic diversity and linkage disequilibrium in Upland cotton (Gossypium hirsutum L.) cultivars from major cotton-growing countries. Euphytica 191:391–401

    Article  CAS  Google Scholar 

  • Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghavami F, Elias EM, Mamidi S, Ansari O, Sargolzaei M, Adhikari T, Mergoum M, Kianian SF (2011) Mixed model association mapping for Fusarium head blight resistance in Tunisian-derived durum wheat populations. G3: Genes| Genomes|Genet 1:209–218

    Article  CAS  PubMed Central  Google Scholar 

  • Gower JC (1987) Introduction to ordination techniques. In: Legendre P, Legendre L (eds) Developments in numerical ecology. NATO ASI Series, vol 14. Springer, Berlin, pp 3–64

    Chapter  Google Scholar 

  • McIntosh RA, Hart GE, Devos KM, Gale MD, and Rogers WJ (1998) Catalogue of gene symbols for wheat. In: Slinkard AE (ed) in Proceedings of the nineth International wheat genetics symposium. Slinkard. University Extension Press, University of Saskatchewan, Saskatoon, Sask., pp 1–235

  • Hovmøller MS, Yahyaoui AH, Milus EA, Justesen AF (2008) Rapid global spread of two aggressive strains of a wheat rust fungus. Mol Ecol 17:3818–3826

    Article  PubMed  Google Scholar 

  • Hovmøller MS, Sørensen CK, Walter S, Justesen AF (2011) Diversity of Puccinia striiformis on cereals and grasses. Annu Rev Phytopathol 49:197–217

    Article  PubMed  Google Scholar 

  • Hovmøller MS, Walter S, Bayles RA, Hubbard A, Flath K, Sommerfeldt N, Leconte M, Czembor P, Rodriguez-Algaba J, Thach T (2016) Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near Himalayan region. Plant Pathol 65:402–411

    Article  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Hubbard A, Lewis CM, Yoshida K, Ramirez-Gonzalez RH, de Vallavieille-Pope C, Thomas J, Kamoun S, Bayles R, Uauy C, Saunders DG (2015) Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol 16:1

    Article  Google Scholar 

  • Korzun V, Röder M, Wendehake K, Pasqualone A, Lotti C, Ganal M, Blanco A (1999) Integration of dinucleotide microsatellites from hexaploid bread wheat into a genetic linkage map of durum wheat. Theor Appl Genet 98:1202–1207

    Article  CAS  Google Scholar 

  • 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 126:1237–1256

    Article  PubMed  Google Scholar 

  • Letta T, Olivera P, Maccaferri M, Jin Y, Ammar K, Badebo A, Salvi S, Noli E, Crossa J, Tuberosa R (2014) Association mapping reveals novel stem rust resistance loci in durum wheat at the seedling stage. Plant Genome. doi:10.3835/plantgenome2013.08.0026

    Google Scholar 

  • Li G, Li Z, Yang W, Zhang Y, He Z, Xu S, Singh R, Qu Y, Xia X (2006) Molecular mapping of stripe rust resistance gene YrCH42 in Chinese wheat cultivar Chuanmai 42 and its allelism with Yr24 and Yr26. Theor Appl Genet 112:1434–1440

    Article  CAS  PubMed  Google Scholar 

  • Lin F, Chen X (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

    Article  CAS  PubMed  Google Scholar 

  • Lin F, Chen X (2009) Quantitative trait loci for non-race-specific, high-temperature adult-plant resistance to stripe rust in wheat cultivar express. Theor Appl Genet 118:631–642

    Article  CAS  PubMed  Google Scholar 

  • Line RF (2002) Stripe rust of wheat and barley in North America: a retrospective historical review 1. Annu Rev Phytopathol 40:75–118

    Article  CAS  PubMed  Google Scholar 

  • 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, 1968–1987. US Dep Agric Agric Res Serv Tech Bull 1788:44

    Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Locatelli A, Cuesta-Marcos A, Gutiérrez L, Hayes PM, Smith KP, Castro AJ (2013) Genome-wide association mapping of agronomic traits in relevant barley germplasm in Uruguay. Mol Breed 31:631–654

    Article  CAS  Google Scholar 

  • Lotti C, Salvi S, Pasqualone A, Tuberosa R, Blanco A (2000) Integration of AFLP markers into an RFLP-based map of durum wheat. Plant Breed 119:393–401

    Article  CAS  Google Scholar 

  • 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 123:143–157

    Article  PubMed  PubMed Central  Google Scholar 

  • Lumley T, Diehr P, Emerson S, Chen L (2002) The importance of the normality assumption in large public health data sets. Annu Rev Publ Health 23:151–169

    Article  Google Scholar 

  • Luo PG, Hu XY, Ren ZL, Zhang HY, Shu K, Yang ZJ (2008) Allelic analysis of stripe rust resistance genes on wheat chromosome 2BS. Genome 51:922–927

    Article  CAS  PubMed  Google Scholar 

  • Lupton F, Macer R (1962) Inheritance of resistance to yellow rust (Puccinia glumarum) in seven varieties of wheat. Trans Br Mycol Soc 45:21–45

    Article  Google Scholar 

  • Ma J, Zhou R, Dong Y, Wang L, Wang X, Jia J (2001) Molecular mapping and detection of the yellow rust resistance gene Yr26 in wheat transferred from Triticum turgidum L. using microsatellite markers. Euphytica 120:219–226

    Article  CAS  Google Scholar 

  • Maccaferri M, Sanguineti MC, Natoli V, Ortega JLA, Salem MB, Bort J, Chenenaoui C, De Ambrogio E, del Moral LG, De Montis A (2006) A panel of elite accessions of durum wheat (Triticum durum Desf.) suitable for association mapping studies. Plant Genet Resour 4:79–85

    Article  CAS  Google Scholar 

  • Maccaferri M, Sanguineti MC, Xie C, Smith JSC, Tuberosa R (2007) Relationships among durum wheat accessions. II. A comparison of molecular and pedigree information. Genome 50:385–399

    Article  CAS  PubMed  Google Scholar 

  • Maccaferri M, Sanguineti MC, Mantovani P, Demontis A, Massi A, Ammar K, Kolmer JA, Czembor JH, Ezrati S, Tuberosa R (2010) Association mapping of leaf rust response in durum wheat. Mol Breed 26:189–228

    Article  CAS  Google Scholar 

  • Maccaferri M, Sanguineti MC, Demontis A, El-Ahmed A, del Moral LG, Maalouf F, Nachit M, Nserallah N, Ouabbou H, Rhouma S (2011) Association mapping in durum wheat grown across a broad range of water regimes. J Exp Bot 62:409–438

    Article  CAS  PubMed  Google Scholar 

  • Maccaferri M, Ricci A, Salvi S, Milner SG, Noli E, Martelli PL, Casadio R, Akhunov E, Scalabrin S, Vendramin V (2015a) A high-density, SNP-based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotechnol J 13:648–663

    Article  CAS  PubMed  Google Scholar 

  • Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen X, Pumphrey M, Dubcovsky J (2015b) 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| Genet 114:014563

    Google Scholar 

  • Mallard S, Gaudet D, Aldeia A, Abelard C, Besnard A, Sourdille P, Dedryver F (2005) Genetic analysis of durable resistance to yellow rust in bread wheat. Theor Appl Genet 110:1401–1409

    Article  CAS  PubMed  Google Scholar 

  • Mantovani P, Maccaferri M, Sanguineti MC, Tuberosa R, Catizone I, Wenzl P, Thomson B, Carling J, Huttner E, DeAmbrogio E (2008) An integrated DArT-SSR linkage map of durum wheat. Mol Breed 22:629–648

    Article  CAS  Google Scholar 

  • Marone D, Laido G, Gadaleta A, Colasuonno P, Ficco DB, Giancaspro A, Giove S, Panio G, Russo MA, De Vita P (2012) A high-density consensus map of A and B wheat genomes. Theor Appl Genet 125:1619–1638

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayer KF, Rogers J, Doležel J, Pozniak C, Eversole K, Feuillet C, Gill B, Friebe B, Lukaszewski AJ, Sourdille P (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788

    Article  Google Scholar 

  • McGrann GRD, Smith PH, Burt C, Mateos GR, Chama TN, MacCormack R, Wessels E, Agenbag G, Boyd LA (2014) Genomic and genetic analysis of the wheat race-specific yellow rust resistance gene Yr5. J Plant Sci Mol Breed 3:2

    Article  Google Scholar 

  • McIntosh AR (1988) Catalogue of gene symbols for wheat. In: T.E. M, R.M.D. K (eds) the seventh International wheat genetics symposium. Institute of Plant Science Research, Cambridge, pp 1225–1323

  • McIntosh R, Lagudah E (2000) Cytogenetical studies in wheat. XVIII. Gene Yr24 for resistance to stripe rust. Plant Breed 119:81–93

    Article  CAS  Google Scholar 

  • McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2014) Catalogue of gene symbols for wheat: 2013–2014 supplement. Komugi—wheat genetic resources database. (http://www.shigen.nig.ac.jp/wheat/komugi/)

  • Naruoka Y, Garland-Campbell K, Carter A (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 128:1083–1101

    Article  CAS  PubMed  Google Scholar 

  • Need A, Ahmadi K, Spector T, Goldstein D (2006) Obesity is associated with genetic variants that alter dopamine availability. Ann Hum Genet 70:293–303

    Article  CAS  PubMed  Google Scholar 

  • Ordoñez M, Kolmer J (2007) Virulence phenotypes of a worldwide collection of Puccinia triticina from durum wheat. Phytopathology 97:344–351

    Article  PubMed  Google Scholar 

  • Pascual L, Albert E, Sauvage C, Duangjit J, Bouchet J-P, Bitton F, Desplat N, Brunel D, Le Paslier M-C, Ranc N (2016) Dissecting quantitative trait variation in the resequencing era: complementarity of bi-parental, multi-parental and association panels. Plant Sci 242:120–130

    Article  CAS  PubMed  Google Scholar 

  • Piepho HP, Möhring J, Melchinger AE, Büchse A (2008) BLUP for phenotypic selection in plant breeding and variety testing. Euphytica 161:209–228

    Article  Google Scholar 

  • Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rajaram S, Saari EE, Hettel GP (1992) Durum wheats: challenges and opportunities. Wheat Special Report No. 9; International Maize and Wheat Improvement Center (CIMMYT): Mexico City, Mexico, 1992

  • Ren R, Wang M, Chen X, Zhang Z (2012a) Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theor Appl Genet 125:847–857

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, He Z, Li J, Lillemo M, Wu L, Bai B, Lu Q, Zhu H, Zhou G, Du J (2012b) QTL mapping of adult-plant resistance to stripe rust in a population derived from common wheat cultivars Naxos and Shanghai 3/Catbird. Theor Appl Genet 125:1211–1221

    Article  PubMed  Google Scholar 

  • Ren Y, Li Z, He Z, Wu L, Bai B, Lan C, Wang C, Zhou G, Zhu H, Xia X (2012c) QTL mapping of adult-plant resistances to stripe rust and leaf rust in Chinese wheat cultivar Bainong 64. Theor Appl Genet 125:1253–1262

    Article  CAS  PubMed  Google Scholar 

  • Rexroad CE, Vallejo RL (2009) Estimates of linkage disequilibrium and effective population size in rainbow trout. BMC Genet 10:83

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosewarne G, Singh R, Huerta-Espino J, Herrera-Foessel S, Forrest K, Hayden M, Rebetzke G (2012) Analysis of leaf and stripe rust severities reveals pathotype changes and multiple minor QTLs associated with resistance in an Avocet × Pastor wheat population. Theor Appl Genet 124:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Huerta-Espino J, William HM (2005) Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk J Agric For 29:121–127

    CAS  Google Scholar 

  • Singh A, Pandey M, Singh A, Knox R, Ammar K, Clarke J, Clarke F, Singh R, Pozniak C, DePauw R (2013) Identification and mapping of leaf, stem and stripe rust resistance quantitative trait loci and their interactions in durum wheat. Mol Breed 31:405–418

    Article  CAS  PubMed  Google Scholar 

  • Solh M NK, Tadesse W, Wellings CR (2012) The growing threat of stripe rust worldwide. Borlaug Global Rust Initiative (BGRI) conference, Beijing, China

  • Stich B, Möhring J, Piepho H-P, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754

    Article  PubMed  PubMed Central  Google Scholar 

  • Tuberosa R, Pozniak C (2014) Durum wheat genomics comes of age. Introduction to the special issue on durum wheat genomics. Mol Breed 34:527–1530

    Article  Google Scholar 

  • Uauy C, Brevis JC, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J (2005) High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theor Appl Genet 112:97–105

    Article  CAS  PubMed  Google Scholar 

  • Vazquez MD, Peterson CJ, Riera-Lizarazu O, Chen X, Heesacker A, Ammar K, Crossa J, Mundt CC (2012) Genetic analysis of adult plant, quantitative resistance to stripe rust in wheat cultivar ‘Stephens’ in multi-environment trials. Theor Appl Genet 124:1–11

    Article  CAS  Google Scholar 

  • Wan A, Chen X (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 98:1534–1542

    Article  Google Scholar 

  • Wan A, Chen X, 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 100:966–975

    Article  Google Scholar 

  • 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 12:787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • William H, Singh R, 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 49:977–990

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Wang M, Cheng P, Kang Z, Hulbert S, Chen X (2013) Molecular mapping of Yr53, a new gene for stripe rust resistance in durum wheat accession PI 480148 and its transfer to common wheat. Theor Appl Genet 126:523–533

    Article  CAS  PubMed  Google Scholar 

  • Yildirim A, Karadag Y, Sakin MA, Gokmen S, Kandemir N, Akkaya MS, Yildirim F (2004) Transfer of stripe rust resistance gene Yr26 to Turkish wheats using microsatellite markers. Cereal Res Commun 32:25–30

    CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB (2005) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genet 38:203–208

    Article  PubMed  Google Scholar 

  • 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 123:1257–1268

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Han D, Chen X, Gou H, Guo S, Rong L, Wang Q, Huang L, Kang Z (2014a) Characterization and molecular mapping of stripe rust resistance gene Yr61 in winter wheat cultivar Pindong 34. Theor Appl Genet 127:2349–2358

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Wang M, Chen X, Lu Y, Kang Z, Jing J (2014b) Identification of Yr59 conferring high-temperature adult-plant resistance to stripe rust in wheat germplasm PI 178759. Theor Appl Genet 127:935–945

    Article  CAS  PubMed  Google Scholar 

  • Zhu H, Gilchrist L, Hayes P, Kleinhofs A, Kudrna D, Liu Z, Prom L, Steffenson B, Toojinda T, Vivar H (1999) Does function follow form? Principal QTLs for Fusarium head blight (FHB) resistance are coincident with QTLs for inflorescence traits and plant height in a doubled-haploid population of barley. Theor Appl Genet 99:1221–1232

    Article  CAS  Google Scholar 

  • Zwart RS, Thompson JP, Milgate AW, Bansal UK, Williamson PM, Raman H, Bariana HS (2010) QTL mapping of multiple foliar disease and root-lesion nematode resistances in wheat. Mol Breed 26:107–124

    Article  Google Scholar 

Download references

Acknowledgements

This project was partially supported by the Durable Rust Resistance in Wheat Project managed by Cornell University with funds from the Bill and Melinda Gates Foundation, the Department for International Development of the United Kingdom and the AGER Agroalimentare e Ricerca—Project ‘From seed to pasta—Multidisciplinary approaches for a more sustainable and high-quality durum wheat production’. Support for Weizhen Liu was provided by the China Scholarship Council, the Washington Grain Commission, and by Washington State University. We thank our colleagues John Kuehner, Wycliffe Nyongesa, Victor Demacon and Kent Evans for maintaining stripe rust screening nurseries, Anmin Wan and Yumei Liu for assisting in greenhouse tests, Simona Corneti and Sandra Stefanelli for assisting in laboratory analysis and stripe rust field sampling. We also appreciate Shiaoman Chao in USDA-ARS Cereal Crops Research for genotyping this panel using 90 K wheat SNP chip.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Weizhen Liu or Michael Pumphrey.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Communicated by Frank Ordon.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, W., Maccaferri, M., Bulli, P. et al. Genome-wide association mapping for seedling and field resistance to Puccinia striiformis f. sp. tritici in elite durum wheat. Theor Appl Genet 130, 649–667 (2017). https://doi.org/10.1007/s00122-016-2841-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-016-2841-9

Keywords

Navigation