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Genome-wide association study for septoria tritici blotch resistance reveals the occurrence and distribution of Stb6 in a historic Swiss landrace collection

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Abstract

Septoria tritici blotch (STB), caused by the fungus Zymoseptoria tritici, is a major constraint in global wheat production. The lack of genetic diversity in modern elite wheat cultivars largely hinders the improvement of STB resistance. Wheat landraces are reservoirs of untapped genetic diversity, which can be exploited to find novel STB resistance genes or alleles. Here, we characterized 188 Swiss wheat landraces for resistance to STB using four Swiss Z. tritici isolates. We used a genome-wide association study (GWAS) to identify genetic variants associated with the amount of lesion and pycnidia production by the fungus. The majority of the landraces were highly resistant for both traits to the isolate 1E4, indicating a gene-for-gene relationship, while higher phenotypic variability was observed against other isolates. GWAS detected a significant SNP on chromosome 3A that was associated with both traits in the isolate 1E4. The resistance response against 1E4 was likely controlled by the Stb6 gene. Sanger sequencing revealed that the majority of these ~ 100-year-old landraces carry the Stb6 resistance allele. This indicates the importance of this gene in Switzerland during the early 1900s for disease control in the field. Our study demonstrates the importance of characterizing historic landrace collections for STB resistance to provide valuable information on resistance variability and contributing alleles. This will help breeders in the future to make decisions on integrating such germplasms in STB resistance breeding.

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References

  • Arraiano LS, Kirby J, Brown JKM (2007) Cytogenetic analysis of the susceptibility of the wheat line Hobbit sib (Dwarf A) to Septoria tritici blotch. Theor Appl Genet 116(1):113–122

    Article  CAS  PubMed  Google Scholar 

  • Ballini E, Tavaud M, Ducasse A, Sanchez D, Paux E, Kitt J, Charmet G, Audigeos D, Roumet P, David J, Morel JB (2020) Genome wide association mapping for resistance to multiple fungal pathogens in a panel issued from a broad composite cross-population of tetraploid wheat Triticum turgidum. Euphytica 216:1–17

    Article  CAS  Google Scholar 

  • Bhullar NK, Street K, Mackay M, Yahiaoui N, Keller B (2009) unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Natl Acad Sci USA 106(23):9519–9524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhullar NK, Zhang Z, Wicker T, Keller B (2010) Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Biol 10(1):1–13

    Article  CAS  Google Scholar 

  • Brown JKM, Chartrain L, Zuber PL, Saintenac C (2015) Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genet Biol 79:33–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K et al (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci USA 110(20):8057–8062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chartrain L, Brading PA, Brown JK (2005) Presence of the Stb6 gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol 54(2):134–43

    Article  CAS  Google Scholar 

  • Cowger C, Hoffer ME, Mundt CC (2000) Specific adaptation by mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathol 49(4):445–451

    Article  Google Scholar 

  • Croll D, Zala M, McDonald BA (2013) Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet 9:e1003567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estep LF, Torriani SFF, Zala M, Anderson NP, Flowers MD, McDonald BA, Mundt CC, Brunner PC (2015) Emergence and early evolution of fungicide resistance in North American populations of Zymoseptoria tritici. Plant Pathol 64(4):961–971

    Article  CAS  Google Scholar 

  • Fones H, Gurr S (2015) The impact of septoria tritici blotch disease on wheat: an EU perspective. Fungal Genet Biol 79:3–7

    Article  PubMed  PubMed Central  Google Scholar 

  • Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156(1):1–13

    Article  Google Scholar 

  • Hall D, Tegström C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 9(2):157–165

    Article  CAS  PubMed  Google Scholar 

  • Hayes LE, Sackett KE, Anderson NP, Flowers MD, Mundt CC (2016) Evidence of selection for fungicide resistance in Zymoseptoria tritici populations on wheat in Western Oregon. Plant Dis 100(2):483–489

    Article  CAS  PubMed  Google Scholar 

  • International Wheat Genome Sequencing Consortium (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 36(6403)

  • Islam MT, Croll D, Gladieux P, Soanes DM, Persoons A, Bhattacharjee P, Hossain MS et al (2016) Emergence of wheat blast in bangladesh was caused by a south american lineage of Magnaporthe oryzae. BMC Biol 14(1):84

    Article  PubMed  PubMed Central  Google Scholar 

  • Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4:297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jørgensen LN, Hovmøller MS, Hansen JG, Lassen P, Clark B et al (2014) IPM Strategies and Their Dilemmas Including an Introduction to www.eurowheat.org. J Integr Agric 13(2):265–281

  • Karisto P, Hund A, Yu K, Anderegg J, Walter A, Mascher F, McDonald BA, Mikaberidze A (2018) Ranking quantitative resistance to septoria tritici blotch in elite wheat cultivars using automated image analysis. Phytopathology 108(5):568–581

    Article  PubMed  Google Scholar 

  • Kema GHJ, Lange W, Silfhout CHV (1995) Differential suppression of stripe rust resistance in synthetic wheat hexaploids derived from Triticum turgidum subsp. dicoccoides and Aegilops squarrosa. Phytopathology (USA)

  • Kidane YG, Hailemariam BN, Mengistu DK, Fadda C, Pè ME, Dell'Acqua M (2017) Genome-wide association study of Septoria tritici blotch resistance in Ethiopian durum wheat landraces. Front Plant Sci 14(8):1586

    Article  Google Scholar 

  • Kollers S, Rodemann B, Ling J, Korzun V, Ebmeyer E, Argillier O, Hinze M et al (2013) Genetic architecture of resistance to septoria tritici blotch (Mycosphaerella graminicola) in European Winter Wheat. Mol Breeding 33(2):411–423

    Article  CAS  Google Scholar 

  • Kolmer JA, Singh RP, Garvin DF, Viccars L, William HM, Huerta‐Espino J, Ogbonnaya FC, Raman H, Orford S, Bariana HS, Lagudah ES (2008) Analysis of the Lr34/Yr18 rust resistance region in wheat germplasm. Crop Sci 48(5):1841–1852

    Article  CAS  Google Scholar 

  • Krattinger SG, Jordan DR, Mace ES, Raghavan C, Luo MC, Keller B, Lagudah ES (2013) Recent emergence of the wheat Lr34 multi-pathogen resistance: insights from haplotype analysis in wheat, rice, sorghum and Aegilops tauschii. Theoret Appl Genet 126(3):663-672

    Article  CAS  Google Scholar 

  • Lendenmann MH, Croll D, Stewart EL, McDonald BA (2014) Quantitative Trait Locus Mapping of Melanization in the Plant Pathogenic Fungus Zymoseptoria tritici. G3: Genes, Genomes, Genetics 4(12):2519–2533

    Article  Google Scholar 

  • Liu J, Rasheed A, He Z, Imtiaz M, Arif A, Mahmood T, Ghafoor A, Siddiqui SU, Ilyas MK, Wen W, Gao F (2019) Genome-wide variation patterns between landraces and cultivars uncover divergent selection during modern wheat breeding. Theoret Appl Genet 132(9):2509–2523

    Article  CAS  Google Scholar 

  • Liu Y, Wang H, Jiang Z, Wang W, Xu R, Wang Q, Zhang Z, Li A, Liang Y, Ou S, Liu X (2021) Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 1–6

  • McDonald BA, Mundt CC (2016) How knowledge of pathogen population biology informs management of septoria tritici blotch. Phytopathology 106(9):948–955

    Article  PubMed  Google Scholar 

  • Meile L, Croll D, Brunner PC, Plissonneau C, Hartmann FE, McDonald BA, Vallet AS (2018) A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch. New Phytol 219(3):1048–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mengistu DK, Kidane YG, Catellani M, Frascaroli E, Fadda C, Pè ME, Acqua MD (2016) High-density molecular characterization and association mapping in ethiopian durum wheat landraces reveals high diversity and potential for wheat breeding. Plant Biotechnol J 14(9):1800–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miedaner T, Zhao Y, Gowda M, Longin CFH, Korzun V, Ebmeyer E, Kazman E, Reif JC (2013) Genetic architecture of resistance to septoria tritici blotch in European Wheat. BMC Genomics 14(1):1–8

    Article  CAS  Google Scholar 

  • Milner SG, Jost M, Taketa S, Mazón E, Himmelbach A, Oppermann M, Weise S et al (2019) Genebank genomics highlights the diversity of a global barley collection. Nat Genet 51(2):319–326

    Article  CAS  PubMed  Google Scholar 

  • Müller T, Viret BS, Fossati D, Brabant C, Schori A, Keller B, Krattinger SG (2018) Unlocking the diversity of genebanks: whole-genome marker analysis of swiss bread wheat and spelt. Theor Appl Genet 131(2):407–416

    Article  PubMed  CAS  Google Scholar 

  • Muqaddasi QH, Zhao Y, Rodemann B, Plieske J, Ganal MW, Röder MS (2019) Genome-wide association mapping and prediction of adult stage septoria tritici blotch infection in European Winter Wheat via high-density marker arrays. Plant Genome 12(1):1–13

    Article  Google Scholar 

  • Nelson JC, Singh RP, Autrique JE, Sorrells ME (1997) Mapping genes conferring and suppressing leaf rust resistance in wheat. Crop Sci 37(6):1928–1935

    Article  CAS  Google Scholar 

  • Pang Y, Liu C, Wang D, Amand PS, Bernardo A, Li W, He F et al (2020) High-resolution genome-wide association study identifies genomic regions and candidate genes for important agronomic traits in Wheat. Mol Plant 13(9):1311–1327

    Article  CAS  PubMed  Google Scholar 

  • Ponomarenko A, Goodwin SB, Kema GHJ (2011) Septoria Tritici Blotch (STB) of Wheat

  • Ray DK, Mueller ND, West PC, Foley JA (2013) Yield Trends Are Insufficient to Double Global Crop Production by 2050. PloS One 8(6):

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reif JC, Zhang P, Dreisigacker S, Warburton ML, Ginkel MV, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. Theor Appl Genet 5:859–864

    Article  Google Scholar 

  • Ren SX, McIntosh RA, Lu ZJ (1997) Genetic suppression of the cereal rye-derived gene Pm8 in wheat. Euphytica 93(3):353–360

    Article  Google Scholar 

  • Saintenac C, Lee WS, Cambon F, Rudd JJ, King RC, Marande W, Powers SJ et al (2018) Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat Genet 50(3):368–374

    Article  CAS  PubMed  Google Scholar 

  • Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3(3):430–439

    Article  PubMed  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464

    Article  Google Scholar 

  • Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, Bhavani S, Rouse MN et al (2015) Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105(7):872–884

    Article  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry, 4th Edn New York. WH Freeman and Company, NY

    Google Scholar 

  • Stephens C, Olmez F, Blyth H, McDonald M, Bansal A, Turgay EB, Hahn F, Saintenac C, Nekrasov V, Solomon P et al (2020) Remarkable recent changes in genetic diversity of the avirulence gene AvrStb6 in global populations of the wheat pathogen Zymoseptoria tritici. bioRxiv. January 1

  • Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE, Palma-Guerrero J, Ma X, McDonald BA (2018) Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol Plant Pathol 19(1):201–216

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Liu X, Wang J, Li M, Wang Q, Tian F, Su Z et al (2016) GAPIT Version 2: An Enhanced Integrated Tool for Genomic Association and Prediction. Plant Genome 9(2)

  • Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277(5329):1063–1066

    Article  CAS  PubMed  Google Scholar 

  • Turner SD (2014) qqman: an R package for visualizing GWAS results using QQ and manhattan plots. Biorxiv 005165

  • Vagndorf N, Nielsen NH, Edriss V, Andersen JR, Orabi J, Jørgensen LN, Jahoor A (2017) Genomewide association study reveals novel quantitative trait loci associated with resistance towards septoria tritici blotch in North European Winter Wheat. Plant Breeding 136(4):474–482

    Article  CAS  Google Scholar 

  • VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91(11):4414–4423

    Article  CAS  PubMed  Google Scholar 

  • UN (2015) The World Population Prospects: 2015 Revision [Online]. Available: http://www.un.org/en/development/desa/publications/world-population-prospects-2015-revision.html (Accessed September 1, 2018).

  • Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Xia X, Rosewarne GM, Zhu H, Li S, Zhang Z, He Z (2015) Stripe rust resistance gene Yr18 and its suppressor gene in Chinese wheat landraces. Plant Breeding 134(6):634–640

    Article  CAS  Google Scholar 

  • Yates S, Mikaberidze A, Krattinger SG, Abrouk M, Hund A, Yu K, Studer B, Fouche S, Meile L, Pereira D, Karisto P et al (2019) Precision phenotyping reveals novel loci for quantitative resistance to septoria tritici blotch. Plant Phenomics 2019:3285904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17(2):155–160

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208

    Article  CAS  PubMed  Google Scholar 

  • Zeller FJ, Hsam SLK (1996) Chromosomal location of a gene suppressing powdery mildew resistance genes Pm8 and Pm17 in common wheat (Triticum aestivum L. em. Thell.). Theoret Appl Genet 93(1–2):38–40

    Article  CAS  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42(4):355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan J, Linde CC, Jürgens T, Merz U, Steinebrunner F, McDonald BA (2005) Variation for neutral markers is correlated with variation for quantitative traits in the plant pathogenic fungus Mycosphaerella graminicola. Mol Ecol 14(9):2683–2693

    Article  CAS  PubMed  Google Scholar 

  • Zhan J, Pettway RE, McDonald BA (2003) The global genetic structure of the wheat pathogen Mycosphaerella graminicola Is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genet Biol 38(3):286–297

    Article  CAS  PubMed  Google Scholar 

  • Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C, Zala M, Ducasse A et al (2017) A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol 214(2):619–631

    Article  CAS  PubMed  Google Scholar 

  • Zogg H, Horber E, Salzmann R (1950) Bericht uber die Tatigkeit der Eidg. Landwirtschaftlichen Versuchsanstalt Zurich-Oerlikon pro 1948/1949. 8. Pflanzenschutz Annu Agric Suisse 51:432–442

    Google Scholar 

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Acknowledgements

This work was funded by the Swiss Federal Office for Agriculture (BLW) in the framework of NAP‐PGREL (National Plan of Action for the Conservation and Sustainable Utilization of Plant Genetic Resources) Project Nr. 627000640. We are thankful to Dr. Fabio Mascher, Dr. Dario Fossati, and Beate Schierscher for providing valuable discussions on the history of these landraces in STB resistance breeding. We thank Dr. Danilo Dos Santos Pereira, Alessio Bernasconi, Dr. Petteri Karisto, Maria Zwyssig and Susanne Dora for help in collecting phenotypic data.

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  1. Plant Pathology, Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland

    Anik Dutta & Bruce A. McDonald

  2. Laboratory of Evolutionary Genetics, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland

    Daniel Croll

  3. Center for Desert Agriculture, Biological and Environmental Science and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    Simon G. Krattinger

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  1. Anik Dutta
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AD, DC, BAM and SK conceived the idea of this study. AD conducted the experiment, collected phenotypic data, performed data analysis and wrote the first manuscript draft. BAM provided funding. All co-authors edited and approved the final version of the manuscript.

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Correspondence to Simon G. Krattinger.

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Dutta, A., Croll, D., McDonald, B.A. et al. Genome-wide association study for septoria tritici blotch resistance reveals the occurrence and distribution of Stb6 in a historic Swiss landrace collection. Euphytica 217, 108 (2021). https://doi.org/10.1007/s10681-021-02843-7

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