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.
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References
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
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
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
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
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
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
BSL (2018) Descriptive variety list. Cereal, maize, large grained pulse crops, root crops (except potato, in German). Bundesortenamt, Hannover
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
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
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
Development Core Team (2018) R: a language and environment for statistical computing. https://www.r-project.org. Accessed 22 June 2018
CNR InterOmics (2017) CNR InterOmics Consortium. https://www.interomics.eu/wild-emmer-wheat-genome. Accessed 15 June 2017
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
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
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
Flath K, Schmitt AK, Miedaner T (2018b) Vorsicht: Getreideroste schlafen nie. Land Forst 20:25–27
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
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
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
Lancashire PD, Bleiholder H, Boom TVD et al (1991) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601
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
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
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
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
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
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
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
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
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
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
McGill R, Tukey JW, Larsen WA (1978) Variations of box plots. Am Stat 32:12–16
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
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
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
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
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
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
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
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
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
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
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
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 809–811
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
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
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
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
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
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 116:395–408
Stram DO, Lee JW (1994) Variance components testing in the longitudinal mixed effects model. Biometrics 50:1171–1177
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
Williams E, Piepho H-P, Whitaker D (2011) Augmented p-rep designs. Biom J 53:19–27. https://doi.org/10.1002/bimj.201000102
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
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
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
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
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
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
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
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
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.
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Miedaner, T., Rapp, M., Flath, K. et al. Genetic architecture of yellow and stem rust resistance in a durum wheat diversity panel. Euphytica 215, 71 (2019). https://doi.org/10.1007/s10681-019-2394-5
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DOI: https://doi.org/10.1007/s10681-019-2394-5