Abstract
Septoria tritici blotch (STB), caused by the ascomycete Mycosphaerella graminicola, is one of the most ubiquitous and important diseases of bread wheat worldwide. The aim of this study was to identify markers linked to loci conferring resistance to STB from seven biparental populations. Linkage analysis, meta-analysis and association mapping were combined to identify robust quantitative trait loci (QTLs) for resistance. Linkage analysis led to the detection of 115 QTLs for resistance to STB and 66 QTLs linked to plant height and/or earliness. Meta-analysis clustered these 115 QTLs into 27 Meta-QTLs (MQTLs) of pathogen resistance, of which 14 were found to be linked to plant height and/or earliness. Both the relationship between dwarfing and susceptibility to STB and the significant negative correlation between earliness and STB symptoms were confirmed. Eleven loci were linked to STB resistance by association mapping using a general linear model and/or a mixed linear model, of which eight co-located with STB MQTLs and two co-located with individual QTLs. Associated markers located in MQTL regions enhanced the relevance of the results and validated the potential of an association mapping approach. With several biparental populations, meta-analysis is the most relevant form of genetic analysis study, but association mapping can be used as a validation method. Regions linked to resistance in both methods should be relevant for use in breeding programs for improving resistance to STB in wheat varieties. The main interest in comparing both approaches is to detect robust loci that will be functional in many genetic backgrounds rather than just in one or a few specific backgrounds.
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References
Adhikari TB, Cavaletto JR, Dubcovsky J, Gieco JO, Schlatter AR, Goodwin SB (2004) Molecular mapping of the Stb4 gene for resistance to Septoria tritici blotch in wheat. Phytopathology 94:1198–1206
Allison DB, Heo M (1998) Meta-analysis of linkage data under worst-case conditions: a demonstration using the human OB region. Genetics 148:859–865
Arabi MIE, Jawhar M, Mir Ali N (2007) The effects of Mycosphaerella graminicola infection on wheat protein content and quality. Cereal Res Commun 35:81–88
Arama PF, Parlevliet JE, van Silfhout CH (1999) Heading date and resistance to Septoria tritici blotch in wheat not genetically associated. Euphytica 106:63–68
Arraiano LS, Chartrain L, Bossolini E, Slatter HN, Keller B, Brown JKM (2007) A gene in European wheat cultivars for resistance to an African isolate of Mycosphaerella graminicola. Plant Pathol 56:73–78
Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati W, Zhang X, Ali Amer M, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JDG, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631
Baltazar BM, Scharen AL, Kronstad WE (1990) Association between dwarfing genes’Rht1’ and’Rht2’ and resistance to Septoria tritici blotch in winter wheat (Triticum aestivum L. emThell). Theor Appl Genet 79:422–426
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265
Bodmer WF (1987) Human genetics: the molecular challenge. BioEssays 7:41–45
Bordes J, Ravel C, Le Gouis J, Lapierre A, Charmet G, Balfourier F (2011) Use of a global wheat core collection for association analysis of flour and dough quality traits. J Cereal Sci 54:137–147
Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6(5):e1000940
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
Brading PA, Verstappen ECP, Kema GHJ, Brown JKM (2002) A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92:439–445
Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111
Chartrain L, Brading PA, Widdowson JP, Brown JKM (2004) Partial resistance to Septoria tritici blotch (Mycosphaerella graminicola) in wheat cultivars Arina and Riband. Phytopathology 94:497–504
Chartrain L, Brading PA, Brown JKM (2005) Presence of the Stb6 gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol 54:134–143
Chartrain L, Sourdille P, Bernard M, Brown JKM (2009) Identification and location of Stb9, a gene for resistance to Septoria tritici blotch in wheat cultivars Courtot and Tonic. Plant Pathol 58:547–555
Cools HJ, Fraaije BA (2008) Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag Sci 64:681–684
Crossa J, Burgueno J, Dreisigacker S, Vargas M, Herrera-Foessel SA, Lillemo M, Singh RP, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch JH, Ortiz R (2007) Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics 177:1889–1913
Ellis M, Spielmeyer W, Gale KR, Rebetzke GJ, Richards RA (2002) “Perfect” markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor Appl Genet 105:1038–1042
Eriksen L, Munk L (2003) The occurrence of Mycosphaerella graminicola and its anamorph Septoria tritici in winter wheat during the growing season. Eur J Plant Pathol 109:253–259
Eriksen L, Shaw MW, Ostergard H (2001) A model of the effect of pseudothecia on genetic recombination and epidemic development in populations of Mycosphaerella graminicola. Phytopathology 91:240–248 (Erratum 519)
Eriksen L, Borum F, Jahoor A (2003) Inheritance and localisation of resistance to Mycosphaerella graminicola causing Septoria tritici blotch and plant height in the wheat (Triticum aestivum L.) genome with DNA markers. Theor Appl Genet 107:515–527
Etzel C, Guerra R (2003) Meta-analysis of genetic-linkage of quantitative trait loci. Am J Hum Genet 71:56–65
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Fraaije BA, Burnett FJ, Clark WS, Motteram J, Lucas JA (2005) Resistance development to QoI inhibitors in populations of Mycosphaerella graminicola in the UK. In: Dehne HW, Gisi U, Kuck KH, Russell PE, Lyr H (eds) Modern fungicides and antifungal compounds IV. BCPC, Alton, pp 63–71
Fraaije BA, Cools HJ, Kim SH, Motteram J, Clark WS, Lucas JA (2007) A novel substitution I381 V in the sterol 14α-demethylase (CYP51) of Mycosphaerella graminicola is differentially selected by azole fungicides. Mol Plant Pathol 8:245–254
Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473
Goodwin SB (2007) Back to basics and beyond: increasing the level of resistance to Septoria tritici blotch in wheat. Aust Plant Pathol 36:532–538
Goodwin SB, McDonald BA, Kema GHJ (2003) The Mycosphaerella sequencing initiative. In: Kema GHI, Van Ginkel M, Harrabi M (eds) Global insights into the Septoria and Stagonospora disease of cereals: proceedings of the sixth international symposium Septoria and Stagonospora diseases of cereals. Tunis, pp 149–151
Gupta PK, Balyan HS, Edwards KJ, Isaac P, Korzun V, Röder M, Gautier MF, Jourdrier P, Schlatter AR (2002) Genetic mapping of 66 new microsatellite (SSR) loci in bread wheat. Theor Appl Genet 105:413–422
Guyomarc’h H, Sourdille P, Charmet G, Edwards K, Bernard M (2002) Characterisation of polymorphic microsatellites markers from Aegilops tauschii and transferability to the D-genome of bread wheat. Theor Appl Genet 104:1164–1172
Hanocq E, Laperche A, Jaminon O, Lainé A-L, Le Gouis J (2007) Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis. Theor Appl Genet 114:569–584
Henderson CR (1975) Best linear unbiased estimation and prediction under a selection model. Biometrics 31:423–447
Hill WG, Robertson A (1968) The effects of inbreeding at loci with heterozygote advantage. Genetics 60:615–628
Hoogendoorn J, Rickson JM, Gale MD (1990) Differences in leaf and stem anatomy related to plant height of tall and dwarf wheat. J Plant Physiol 136:72–77
Jestin C, Lodé M, Vallée P, Domin C, Falentin C, Horvais R, Coedel S, Manzanares-Dauleux MJ, Delourme R (2010) Association mapping of quantitative resistance for Leptosphaeria maculans in oilseed rape (Brassica napus L.). Mol Breed 27:271–287
Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckermann D, Daly MJ, Eskin E (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723
Kearsey MJ, Farquhar AJ (1998) QTL analysis in plants: where are we now? Heredity 80:137–142
Kisana NS, Nkongolo KK, Quick JS, Johnson DL (1993) Production of double haploids by anther culture and wheat × maize method in wheat breeding programme. Plant Breed 110:96–102
Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Laurie DA, Bennett MD (1986) Wheat × maize hybridization. Can J Genet Cytol 28:313–316
Lewis CM (2002) Genetic association studies: design, analysis and interpretation. Brief Bioinform 3:146–153
Löffler M, Schön CC, Miedaner T (2009) Revealing the genetic architecture of FHB resistance in hexaploid wheat (Triticum aestivum L.) by QTL meta-analysis. Mol Breed 23:473–488
Lohmueller KE, Pearce CL, Pike M, Lander ES, Hirschhorn JN (2003) Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat Genet 33:177–182
Lorieux M (2006) MapDisto, A tool for easy mapping of genetic markers. Poster (P886) presented at the Plant and Animal Genome XIV Conf. http://mapdisto.free.fr/
Maenhout S, De Baets B, Haesaert G (2009) CoCoa: a software tool for estimating the coefficient of coancestry from multilocus genotype data. Bioinformatics 25:2753–2754
Manenti G, Galvan A, Pettinicchio A, Trincucci G, Spada E, Zolin A, Milani S, Gonzalez-Neira A, Dragani TA (2009) Mouse genome-wide association mapping needs linkage analysis to avoid false-positive loci. PLoS Genet 5(1):e1000331
Miedaner T, Risser P, Paillard S, Schnurbusch T, Keller B, Hartl L, Holzapfel J, Korzun V, Ebmeyer E, Utz HF (2012) Broad-spectrum resistance loci for three quantitatively inherited diseases in two winter wheat populations. Mol Breed 29:731–742
Neumann K, Kobiljski B, Dencic S, Varshney RK, Börner A (2010) Genome-wide association mapping: a case study in bread wheat (Triticum aestivum L.). Mol Breed 27:37–58
Paillotin G (2008) Rapport final du Président du comité opérationnel « Ecophyto 2018 » , Chantier 15 « Agriculture écologique et productive » , 17 juin 2008
Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA, Al-Kaff N, Korolev A, Boulton MI, Phillips AL, Hedden P, Nicholson P, Thomas SG (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831
Pestsova EG, Korzun V, Börner A (2008) Validation and utilisation of Rht dwarfing gene-specific markers. Cereal Res Comun 36:235–246
Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181
R Fundation for Statistical Computing (2007) R: A programming environment for data analysis and graphics version 2.6.0 (2007-10-03)
Risser P, Ebmeyer E, Korzun V, Hartl L, Miedaner T (2011) Quantitative trait loci for adult-plant resistance to Mycosphaerella graminicola in two winter wheat populations. Phytopathology 101:1209–1216
Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023
Saintenac C, Falque M, Martin O, Paux E, Feuillet C, Sourdille P (2009) Detailed recombination studies along chromosome 3B provide new insight into crossover distribution in wheat. Genetics 181:393–403
Sourdille P, Guyomarc’h H, Baron C, Gandon B, Chiquet V (2001) Improvement of the genetic maps of wheat using new microsatellite markers. Plant and animal genome IX. San Diego, pp. 167
Stich B, Melchinger AE (2009) Comparison of mixed-model approaches for association mapping in rapeseed, potato, sugar beet, maize, and Arabidopsis. BMC Genomics 10:94
Stich B, Möhring J, Piepho HP, Heckenberger M, Buckler ES, Melchinger AE (2008) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754
Tabib Ghaffary SM (2011c) Efficacy and mapping of resistance to Mycospaerella graminicola in wheat, 233 pp. PhD thesis, Wageningen University, Wageningen
Tabib Ghaffary SM, Robert O, Laurent V, Lonnet P, Margalé E, van der Lee TA, Visser RG, Kema GHJ (2011a) Genetic analysis of resistance to Septoria tritici blotch in the French winter wheat cultivars Balance and Apache. Theor Appl Genet 123:741–754
Tabib Ghaffary SM, Faris JD, Friesen TL, Visser RG, van der Lee TA, Robert O, Kema GHJ (2011b) New broad-spectrum resistance to Septoria tritici blotch derived from synthetic hexaploid wheat. Theor Appl Genet 124:125–142
Tavella CM (1978) Date of heading and plant height of wheat varieties, as related to septoria leaf blotch damage. Euphytica 27:577–580
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Veyrieras J-B, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinform 8:49
Voorrips RE (2002) MapChart: Software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Basten CJ, Zeng Z (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh
Wilhelm EP, Turner AS, Laurie DA (2009) Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet 118:285–294
Wilson LM, Whitt SR, Ibanez AM, Rocheford TR, Goodman MM, Buckler S (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotech 17:155–160
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Yu J, Zhang Z, Zhu C, Tabanao DA, Pressoir G, Tuinstra MR, Kresovich S, Buckler ES (2009) Simulation appraisal of the adequacy of number of background markers for relationship estimation in association mapping. The Plant Genome 2:63–77
Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Zhao KY, Aranzana MJ, Kim S, Lister C, Shindo C, Tang CL, Toomajian C, Zheng HG, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:71–82
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20
Zou J, Jiang C, Cao Z, Li R, Long Y, Chen S, Meng J (2010) Association mapping of seed oil content in Brassica napus and comparison with quantitative trait loci identified from linkage mapping. Genome 53:908–916
Acknowledgments
This research was carried out with the financial support of the French Fonds de Soutien à l’Obtention Végétale (FSOV) within the program FSOV 2008B “Exploitation de résistances durables aux septorioses et fusarioses de blé tendre” and with the financial contribution of the European Community within the project BioExploit (integrated project FOOD-CT-2005-513959) “exploitation of natural plant biodiversity for pesticide-free production of food”. We thank Drs. Steve Barnes and Glenda Willems, SESVanderHave Company, for their critical review of the manuscript.
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Goudemand, E., Laurent, V., Duchalais, L. et al. Association mapping and meta-analysis: two complementary approaches for the detection of reliable Septoria tritici blotch quantitative resistance in bread wheat (Triticum aestivum L.). Mol Breeding 32, 563–584 (2013). https://doi.org/10.1007/s11032-013-9890-4
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DOI: https://doi.org/10.1007/s11032-013-9890-4