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Euphytica

, 215:71 | Cite as

Genetic architecture of yellow and stem rust resistance in a durum wheat diversity panel

  • Thomas MiedanerEmail author
  • Matthias Rapp
  • Kerstin Flath
  • C. Friedrich H. Longin
  • Tobias Würschum
Article

Abstract

Winter durum (Triticum turgidum var. durum) growing is favored in Germany, Austria, and Hungary. With the invasion of the aggressive Warrior race with a wider virulence spectrum of the yellow rust (YR) causing pathogen, YR came into focus of durum breeders. Accordingly, a local epidemic of stem rust in winter wheat 2013 gained much attention. Therefore, we aimed to analyze the genetic architecture of resistance to YR and stem rust (SR) in a diversity panel of 328 durum lines genotyped by 12,550 mapped markers. Infections were successful in three environments for YR and one environment for SR. Additionally, cumulative ratings of leaf and ear health were conducted in five and three environments, respectively. The genome-wide association analysis revealed six to eight quantitative trait loci (QTL) per trait with an explained total genotypic variance of 42% (YR) to 75% (ear health). Sequence comparison with a reference genome indicated that three YR (Yr10, Yr51, YrH9014) and two SR (Sr56, Sr8155B1) resistance genes might be present in the diversity panel. Other QTL with explained genotypic variances ranging from 1.5 to 21% were detected. The difference between marker-assisted selection and genomic prediction was the highest for those traits with lower explained genetic variance (YR, leaf health) indicating that an array of non-detected QTL was used for genomic prediction. Genomics-assisted breeding could greatly help in achieving complex resistances in cultivars.

Keywords

Durum Wheat Rust Puccinia striiformis Puccinia graminis MAS Genomic prediction 

Notes

Acknowledgements

The financial support of Deutsche Forschungsgemeinschaft (DFG), Bonn, is highly acknowledged (DFG LO 1816-4/1). We further thank Bianca Yildirim and Silvia Koch, University of Hohenheim, for their excellent technical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The experiments reported in this study comply with the current laws of Germany.

Supplementary material

10681_2019_2394_MOESM1_ESM.pdf (828 kb)
Supplementary material 1 (PDF 827 kb)

References

  1. Aoun M, Kolmer JA, Rouse MN, Chao S, Bulbula WD, Elias EM, Acevedo M (2017) Inheritance and bulked segregant analysis of leaf rust and stem rust resistance in durum wheat genotypes. Phytopathology 107:1496–1506.  https://doi.org/10.1094/PHYTO-12-16-0444-R CrossRefPubMedGoogle Scholar
  2. Avni R, Nave M, Barad O et al (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357:93–97.  https://doi.org/10.1126/science.aan0032 CrossRefPubMedGoogle Scholar
  3. Bansal UK, Kazi AG, Singh B, Hare RA, Bariana HS (2014a) Mapping of durable stripe rust resistance in a durum wheat cultivar Wollaroi. Mol Breed 33:51–59.  https://doi.org/10.1007/s11032-013-9933-x CrossRefGoogle Scholar
  4. Bansal U, Bariana H, Wong D, Randhawa M, Wicker T, Hayden M, Keller B (2014b) Molecular mapping of an adult plant stem rust resistance gene Sr56 in winter wheat cultivar Arina. Theor Appl Genet 127:1441–1488.  https://doi.org/10.1007/s00122-014-2311-1 CrossRefPubMedGoogle Scholar
  5. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635.  https://doi.org/10.1093/bioinformatics/btm308 CrossRefGoogle Scholar
  6. Brar GS, Graf R, Knox R, Campbell H, Kutcher HR (2017) Reaction of differential wheat and triticale genotypes to natural stripe rust [Puccinia striiformis f. sp. tritici] infection in Saskatchewan, Canada. Can J Plant Pathol 39:138–148.  https://doi.org/10.1080/07060661.2017.1341433 CrossRefGoogle Scholar
  7. BSL (2018) Descriptive variety list. Cereal, maize, large grained pulse crops, root crops (except potato, in German). Bundesortenamt, HannoverGoogle Scholar
  8. Chao S, Rouse MN, Acevedo M, Szabo-Hever A, Bockelman H, Bonman JM, Elias E, Klindworth D, Xu S (2017) Evaluation of genetic diversity and host resistance to stem rust in USDA NSGC durum wheat accessions. Plant Genome 10:2.  https://doi.org/10.3835/plantgenome2016.07.0071 CrossRefGoogle Scholar
  9. Chen X, Penman L, Anmin W, 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.  https://doi.org/10.1080/07060661.2010.499271 CrossRefGoogle Scholar
  10. 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 127:2267–2277.  https://doi.org/10.1007/s00122-014-2378-8 CrossRefPubMedGoogle Scholar
  11. Development Core Team (2018) R: a language and environment for statistical computing. https://www.r-project.org. Accessed 22 June 2018
  12. CNR InterOmics (2017) CNR InterOmics Consortium. https://www.interomics.eu/wild-emmer-wheat-genome. Accessed 15 June 2017
  13. Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255.  https://doi.org/10.3835/plantgenome2011.08.0024 CrossRefGoogle Scholar
  14. Endelman JB, Jannink JL (2012) Shrinkage estimation of the realized relationship matrix. G3 Genes Genomes Genet 2:1405–1413.  https://doi.org/10.1534/g3.112.004259 CrossRefGoogle Scholar
  15. Flath K, Miedaner T, Olivera PD, Rouse MN, Yue J (2018a) Genes for wheat stem rust resistance postulated in German cultivars and their efficacy in seedling and adult-plant field tests. Plant Breed 137:301–312.  https://doi.org/10.1111/pbr.12591 CrossRefGoogle Scholar
  16. Flath K, Schmitt AK, Miedaner T (2018b) Vorsicht: Getreideroste schlafen nie. Land Forst 20:25–27Google Scholar
  17. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, UK. https://www.vsni.co.uk/downloads/asreml/release3/UserGuide.pdf. Accessed 22 June 2018
  18. Hovmøller MS, Walter S, Bayles RA et al (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.  https://doi.org/10.1111/ppa.12433 CrossRefGoogle Scholar
  19. Huerta-Espino J, Singh RP (2017) First detection of virulence in Puccinia striiformis f. sp. tritici to wheat resistance genes Yr10 and Yr24 (= Yr26) in Mexico. Plant Dis 101:1676.  https://doi.org/10.1094/PDIS-04-17-0532-PDNLancashire CrossRefGoogle Scholar
  20. Lancashire PD, Bleiholder H, Boom TVD et al (1991) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601CrossRefGoogle Scholar
  21. Laroche A, Frick MM, Huel R, Nykiforuk C, Conner B, Kuzyk A (2000) Molecular identification of the wheat stripe rust resistance gene Yr10, the first full-length leucine zipper-nucleotide binding site-leucine-rich-repeat resistance gene in cereals (Unpublished). https://www.ncbi.nlm.nih.gov/entrez/viewer.fcgi?Db=nucleotide&val=11990496. Accessed 22 June 2018
  22. 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.  https://doi.org/10.1007/s00122-013-2050-8 CrossRefPubMedGoogle Scholar
  23. 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 7:1.  https://doi.org/10.3835/plantgenome2013.08.0026 CrossRefGoogle Scholar
  24. Li H, Vikram P, Singh RP et al (2015) A high density GBS map of bread wheat and its application for dissecting complex disease resistance traits. BMC Genom 16:216.  https://doi.org/10.1186/s12864-015-1424-5 CrossRefGoogle Scholar
  25. Lin X, N’Diaye A, Walkowiak S et al (2018) Genetic analysis of resistance to stripe rust in durum wheat (Triticum turgidum L. var. durum). PLoS ONE 13:e0203283.  https://doi.org/10.1371/journal.pone.0203283 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Liu T, Wan A, Liu D, Chen X (2017a) Changes of races and virulence genes in Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen, in the United States from 1968 to 2009. Plant Dis 101:1522–1532.  https://doi.org/10.1094/PDIS-12-16-1786-RE CrossRefPubMedGoogle Scholar
  27. Liu W, Maccaferri M, Bulli P, Rynearson S, Tuberosa R, Chen X, Pumphrey M (2017b) 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.  https://doi.org/10.1007/s00122-016-2841-9 CrossRefPubMedGoogle Scholar
  28. Liu W, Maccaferri M, Rynearson S, Letta T, Zegeye H, Tuberosa R, Chen X, Pumphrey M (2017c) Novel sources of stripe rust resistance identified by genome-wide association mapping in Ethiopian durum wheat (Triticum turgidum ssp. durum). Front Plant Sci 8:774.  https://doi.org/10.3389/fpls.2017.00774 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Losert D, Maurer HP, Leiser WL, Würschum T (2017) Defeating the Warrior: genetic architecture of triticale resistance against a novel aggressive yellow rust race. Theor Appl Genet 130:685–696.  https://doi.org/10.1007/s00122-016-2843-7 CrossRefPubMedGoogle Scholar
  30. Ma D-F, Hou L, Tang M-S, Wang H-G, Li Q, Jing J-X (2013) Genetic analysis and molecular mapping of a stripe rust resistance gene. YRH9014 in wheat line H9014-14-4-6-1. J Integr Agric 12:638–645.  https://doi.org/10.1016/S2095-3119(13)60271-3 CrossRefGoogle Scholar
  31. McGill R, Tukey JW, Larsen WA (1978) Variations of box plots. Am Stat 32:12–16Google Scholar
  32. McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers J, Morris C, Appels R, Xia XC (2013) Catalogue of gene symbols for wheat. https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/2013/GeneSymbol.pdf. Accessed 22 June 2018
  33. McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of gene symbols for wheat: 2017 supplement. https://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2017.pdf. Accessed 23 January 2019
  34. Miedaner T, Lieberherr B, Koch S, Scholz M, Ebmeyer E (2014) Combined inoculation of wheat pathogens Zymoseptoria tritici and Fusarium culmorum as a tool for increasing selection intensity in resistance breeding. Plant Breed 133:543–547.  https://doi.org/10.1111/pbr.12191 CrossRefGoogle Scholar
  35. Miedaner T, Sieber A-N, Desaint H, Buerstmayr H, Longin CFH, Würschum T (2017) The potential of genomic-assisted breeding to improve Fusarium head blight resistance in winter durum wheat. Plant Breed 136:610–619.  https://doi.org/10.1111/pbr.12515 CrossRefGoogle Scholar
  36. Miedaner T, Schmid JE, Flath K, Koch S, Jacobi A, Ebmeyer E, Taylor M (2018) A multiple disease test for field-based phenotyping of resistances to Fusarium head blight, yellow rust and stem rust in wheat. Eur J Plant Pathol 151:451–461.  https://doi.org/10.1007/s10658-017-1386-3 CrossRefGoogle Scholar
  37. Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong GY, Myles S (2015) LinkImpute: fast and accurate genotype imputation for non-model organisms. G3 Genes Genomes Genet 5:2383–2390.  https://doi.org/10.1534/g3.115.021667 CrossRefGoogle Scholar
  38. Nirmala J, Saini J, Newcomb M, Olivera P, Gale S, Klindworth D, Elias E, Talbert L, Chao S, Faris J, Xu S, Jin Y, Rouse MN (2017) Discovery of a novel stem rust resistance allele in durum wheat that exhibits differential reactions to Ug99 isolates. G3 Genes Genomes Genet 7:3481–3490.  https://doi.org/10.1534/g3.117.300209 CrossRefGoogle Scholar
  39. Olivera Firpo PD, Newcomb M, Flath K, Sommerfeldt-Impe N, Szabo LJ, Carter M, Luster DG, Jin Y (2017) Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013. Plant Pathol 66:1258–1266.  https://doi.org/10.1111/ppa.12674 CrossRefGoogle Scholar
  40. Patpour M, Hovmøller MS (2016) Samples of stem rust infected wheat from Italy. GRRC report 01/2016. Aarhus Univ., Denmark. http://wheatrust.org/fileadmin/www.grcc.au.dk/International_Services/Pathotype_SR_Results/Country_report_Sicily_-_November2016.pdf. Accessed 22 June 2018
  41. Piepho H-P, Möhring J (2007) Computing heritability and selection response from unbalanced plant breeding trials. Genetics 177:1881–1888.  https://doi.org/10.1534/genetics.107.074229 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Poland J, Rutkoski J (2016) Advances and challenges in genomic selection for disease resistance. Annu Rev Phytopathol 54:79–98.  https://doi.org/10.1146/annurev-phyto-080615-100056 CrossRefPubMedGoogle Scholar
  43. 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
  44. Prat N, Buerstmayr M, Steiner B, Robert O, Buerstmayr H (2014) Current knowledge on resistance to Fusarium head blight in tetraploid wheat. Mol Breed 34:1689–1699.  https://doi.org/10.1007/s11032-014-0184-2R CrossRefGoogle Scholar
  45. 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.  https://doi.org/10.1007/s00122-013-2220-8 CrossRefPubMedGoogle Scholar
  46. Rosewarne G, Herrera-Foessel S, Singh R, Huerta-Espino J, Lan C, He Z (2013) Quantitative trait loci of stripe rust resistance in wheat. Theor Appl Genet 126:2427–2449.  https://doi.org/10.1007/s00122-013-2159-9 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Rutkoski JE, Heffner EL, Sorrells ME (2011) Genomic selection for durable stem rust resistance in wheat. Euphytica 179:161–173.  https://doi.org/10.1007/s10681-010-0301-1 CrossRefGoogle Scholar
  48. Shamanin V, Salina E, Wanyera R, Zelenskiy Y, Olivera P, Morgounov A (2016) Genetic diversity of spring wheat from Kazakhstan and Russia for resistance to stem rust Ug99. Euphytica 212:287–296.  https://doi.org/10.1007/s10681-016-1769-0 CrossRefGoogle Scholar
  49. Spindel JE, Begum H, Akdemir D, Collard B, Redoña E, Jannink J, McCouch S (2016) Genome-wide prediction models that incorporate de novo GWAS are a powerful new tool for tropical rice improvement. Heredity 116:395–408CrossRefGoogle Scholar
  50. Stram DO, Lee JW (1994) Variance components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177CrossRefGoogle Scholar
  51. Wan A, Muleta KT, Zegeye H, Hundie B, Pumphrey MO, Chen X (2017) Virulence characterization of wheat stripe rust fungus Puccinia striiformis f. sp. tritici in Ethiopia and evaluation of Ethiopian wheat germplasm for resistance to races of the pathogen from Ethiopia and the United States. Plant Dis 101:73–80.  https://doi.org/10.1094/PDIS-03-16-0371-RE CrossRefPubMedGoogle Scholar
  52. Williams E, Piepho H-P, Whitaker D (2011) Augmented p-rep designs. Biom J 53:19–27.  https://doi.org/10.1002/bimj.201000102 CrossRefPubMedGoogle Scholar
  53. Würschum T, Reif JC, Kraft T, Janssen G, Zhao Y (2013) Genomic selection in sugar beet breeding populations. BMC Genet 14:85.  https://doi.org/10.1186/1471-2156-14-85 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Würschum T, Abel S, Zhao Y (2014) Potential of genomic selection in rapeseed (Brassica napus L.) breeding. Plant Breed 133:45–51.  https://doi.org/10.1111/pbr.12137 CrossRefGoogle Scholar
  55. Würschum T, Langer SM, Longin CFH (2015) Genetic control of plant height in European winter wheat cultivars. Theor Appl Genet 128:865–874.  https://doi.org/10.1007/s00122-015-2476-2 CrossRefPubMedGoogle Scholar
  56. Würschum T, Leiser WL, Longin CFH (2017) Molecular genetic characterization and association mapping in spelt wheat. Plant Breed 136:214–223.  https://doi.org/10.1111/pbr.12462 CrossRefGoogle Scholar
  57. Xu LS, Wang MN, Cheng P, Kang ZS, Hulbert SH, Chen XM (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.  https://doi.org/10.1007/s00122-012-1998-0 CrossRefPubMedGoogle Scholar
  58. Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208.  https://doi.org/10.1038/ng1702 CrossRefGoogle Scholar
  59. Yuan C, Wu J, Yan B, Hao Q, Zhang C, Lyu B et al (2018) Remapping of the stripe rust resistance gene Yr10 in common wheat. Theor Appl Genet 131:1253–1262.  https://doi.org/10.1007/s00122-018-3075-9 CrossRefPubMedGoogle Scholar
  60. Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20.  https://doi.org/10.3835/plantgenome2008.02.0089 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.State Plant Breeding InstituteUniversity of HohenheimStuttgartGermany
  2. 2.Institute for Plant Protection in Field Crops and GrasslandJulius-Kuehn-Institut (JKI)KleinmachnowGermany

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