Dynamic QTL for adult plant resistance to powdery mildew in common wheat (Triticum aestivum L.)
Agriculture will benefit from a rigorous characterization of genes for adult plant resistance (APR) since this gene class was recognized to provide more durable protection from plant diseases. The present study reports the identification of APR loci to powdery mildew in German winter wheat cultivars Cortez and Atlantis. Cortez was previously shown to carry all-stage resistance gene Pm3e. To avoid interference of Pm3e in APR studies, line 6037 that lacked Pm3e but showed field resistance from doubled-haploid (DH) population Atlantis/Cortez was used in two backcrosses to Atlantis for the establishment of DH population 6037/Atlantis//Atlantis. APR was assessed in the greenhouse 10, 15, and 20 days after inoculation (dai) from the 4-leaf stage onwards and combined with single-nucleotide polymorphism data in a genome-wide association study (GWAS) and a linkage map-based quantitative trait loci (QTL) analysis. In GWAS, two QTL were detected: one on chromosome 1BL 10 dai, the other on chromosome 2BL 20 dai. In conventional QTL analysis, both QTL were detected with all three disease ratings: the QTL on chromosome 1BL explained a maximum of 35.2% of the phenotypic variation 10 dai, whereas the QTL on chromosome 2BL explained a maximum of 43.5% of the phenotypic variation 20 dai. Compared with GWAS, linkage map-based QTL analysis allowed following the dynamics of QTL action. The two large-effect QTL for APR to powdery mildew with dynamic gene action can be useful for the enhancement of wheat germplasm.
KeywordsBlumeria graminis f. sp. tritici Disease resistance Genome-wide association study Linkage map-based QTL analysis
We thank Lorenz Hartl for his continuous support of the study and Adalbert Bund for population development. Technical assistance provided by Sabine Schmidt (crossing work), Martin Müller and team (DH production), Petra Greim (DNA isolation), and the staff of working group Wheat and Oat Breeding Research (set-up and maintenance of field trial) of the Bavarian State Research Center for Agriculture is gratefully acknowledged.
VM conceived the research and performed QTL analysis. MS designed the GH experiment, scored disease response, analyzed the phenotypic and genotypic data, and performed GWAS. VM drafted the manuscript and MS commented on it.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Acevedo-Garcia J, Spencer D, Thieron H, Reinstadler A, Hammond-Kosack K, Phillips AL, Panstruga R (2017) mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnol J 15:367–378. https://doi.org/10.1111/pbi.12631 CrossRefPubMedGoogle Scholar
- Anonymous (2004) Beschreibende Sortenliste. Deutscher Landwirtschaftsverlag GmbH, HannoverGoogle Scholar
- Anonymous (2018) Judgment of the court of justice in case C-528/16. https://curia.europa.eu/jcms/upload/docs/application/pdf/2018-07/cp180111en.pdf. Accessed 11 Feb 2019
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x CrossRefGoogle Scholar
- Buerstmayr H, Mohler V, Kohli M (2017) Advances in control of wheat diseases: Fusarium head blight, wheat blast and powdery mildew. In: Langridge P (ed) Achieving sustainable cultivation of wheat, Breeding, quality traits, pests and diseases, vol 1. Burleigh Dodds Science Publishing Limited, Cambridge, pp 345–370CrossRefGoogle Scholar
- Chen J, Upadhyaya NM, Ortiz D, Sperschneider J, Li F, Bouton C, Breen S, Dong C, Xu B, Zhang X, Mago R, Newell K, Xia X, Bernoux M, Taylor JM, Steffenson B, Jin Y, Zhang P, Kanyuka K, Figueroa M, Ellis JG, Park RF, Dodds PN (2017) Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science 358:1607–1610. https://doi.org/10.1126/science.aao4810 CrossRefPubMedGoogle 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. https://doi.org/10.1094/phyto-99-8-0968 CrossRefPubMedGoogle Scholar
- Hwang JU, Song WY, Hong D, Ko D, Yamaoka Y, Jang S, Yim S, Lee E, Khare D, Kim K, Palmgren M, Yoon HS, Martinoia E, Lee Y (2016) Plant ABC transporters enable many unique aspects of a terrestrial plant’s lifestyle. Mol Plant 9:338–355. https://doi.org/10.1007/s11103-017-0632-6 CrossRefPubMedGoogle Scholar
- International Wheat Genome Sequencing Consortium (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361: eaar7191. https://doi.org/10.1126/science.aar7191
- Klahr A, Zimmermann G, Wenzel G, Mohler V (2007) Effects of environment, disease progress, plant height and heading date on the detection of QTLs for resistance to Fusarium head blight in an European winter wheat cross. Euphytica 154:17–28. https://doi.org/10.1007/s10681-006-9264-7 CrossRefGoogle Scholar
- Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363. https://doi.org/10.1126/science.1166453 CrossRefPubMedGoogle Scholar
- Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, Bjørnstad Å (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116:1155–1166. https://doi.org/10.1007/s00122-008-0743-1 CrossRefPubMedGoogle Scholar
- Lu Q, Bjørnstad Å, Ren Y, Asad MA, Xia X, Chen X, Ji F, Shi J, Lillemo M (2012) Partial resistance to powdery mildew in German spring wheat ‘Naxos’ is based on multiple genes with stable effects in diverse environments. Theor Appl Genet 125:297–309. https://doi.org/10.1007/s00122-012-1834-6 CrossRefPubMedGoogle Scholar
- Luo PG, Luo HY, Chang ZJ, Zhang HY, Zhang M, Ren ZL (2009) Characterization and chromosomal location of Pm40 in common wheat: a new gene for resistance to powdery mildew derived from Elytrigia intermedium. Theor Appl Genet 118:1059–1064. https://doi.org/10.1007/s00122-009-0962-0 CrossRefPubMedGoogle Scholar
- Marone D, Russo MA, Laidò G, De Vita P, Papa R, Blanco A, Mastrangelo AM (2013) Genetic basis of qualitative and quantitative resistance to powdery mildew in wheat: from consensus regions to candidate genes. BMC Genomics 14:562. https://doi.org/10.1186/1471-2164-14-562 CrossRefPubMedPubMedCentralGoogle Scholar
- 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/download.jsp. Accessed 11 Feb 2019
- Muranty H, Pavoine M-T, Jaudeau B, Radek W, Doussinault G, Barloy D (2009) Two stable QTL involved in adult plant resistance to powdery mildew in the winter wheat line RE714 are expressed at different times along the growing season. Mol Breed 23:445–461. https://doi.org/10.1007/s11032-008-9248-5 CrossRefGoogle Scholar
- Petre B, Morin E, Tisserant E, Hacquard S, Da Silva C, Poulain J, Delaruelle C, Martin F, Rouhier N, Kohler A (2012) RNA-Seq of early-infected poplar leaves by the rust pathogen Melampsora larici-populina uncovers PtSultr3;5, a fungal-induced host sulfate transporter. PLoS One 7:e44408. https://doi.org/10.1371/journal.pone.0044408 CrossRefPubMedPubMedCentralGoogle Scholar
- Poppe S, Dorsheimer L, Happel P, Stukenbrock EH (2015) Rapidly evolving genes are key players in host specialization and virulence of the fungal wheat pathogen Zymoseptoria tritici (Mycosphaerella graminicola). PLoS Pathog 11:e1005055. https://doi.org/10.1371/journal.ppat.1005055 CrossRefPubMedPubMedCentralGoogle Scholar
- Pretorius ZA, Park RF, Wellings CR (2000) An accelerated method for evaluating adult-plant resistance to leaf and stripe rust in spring wheat. Acta Phytopathol Entomol Hung 35:359–364Google Scholar
- Salcedo A, Rutter W, Wang S, Akhunova A, Bolus S, Chao S, Anderson N, De Soto MF, Rouse M, Szabo L, Bowden RL, Dubcovsky J, Akhunov E (2017) Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science 358:1604–1606. https://doi.org/10.1126/science.aao7294 CrossRefPubMedPubMedCentralGoogle Scholar
- Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111:731–735. https://doi.org/10.1007/s00122-005-2058-9 CrossRefPubMedGoogle Scholar
- Tucker DM, Griffey CA, Liu S, Saghai Maroof MA (2006) Potential for effective marker-assisted selection of three quantitative trait loci conferring adult plant resistance to powdery mildew in elite wheat breeding populations. Plant Breed 125:430–436. https://doi.org/10.1111/j.1439-0523.2006.01233.x CrossRefGoogle Scholar
- Turner SD (2014) qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. biorRxiv 005165. https://doi.org/10.1101/005165
- Vales MI, Schön CC, Capettini F, Chen XM, Corey AE, Mather DE, Mundt CC, Richardson KL, Sandoval-Islas JS, Utz HF, Hayes PM (2005) Effect of population size on the estimation of QTL: a test using resistance to barley stripe rust. Theor Appl Genet 111:1260–1270. https://doi.org/10.1007/s00122-005-0043-y CrossRefPubMedGoogle Scholar
- Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Consortium, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo M-C, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014b) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796. https://doi.org/10.1111/pbi.12183 CrossRefPubMedPubMedCentralGoogle Scholar
- Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, King J, West C, Griffiths S, King I, Bentley AR, Edwards KJ (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206. https://doi.org/10.1111/pbi.12485 CrossRefPubMedGoogle Scholar