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Identification of marker-trait associations in the German winter barley breeding gene pool (Hordeum vulgare L.)

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Abstract

A genome-wide association mapping approach for grain yield and traits of high agronomic relevance was carried out on basis of a set of 61 six-rowed and 48 two-rowed German winter barley (Hordeum vulgare L.) cultivars representing breeding progress in the period 1959–2003. Extensive phenotyping was conducted in field trials carried out at 12 locations in 3 years. Heritability was estimated at between 0.45 for grain yield and 0.94 for grains per spike. By using the Illumina Golden Gate Bead Array technology, 833 single nucleotide polymorphisms with an allele frequency higher than 5% were obtained. Linkage disequilibrium on the whole genome extends to 7.35 cM. Based on a mixed linear model approach taking into account the population structure estimated on the basis of 72 simple sequence repeat markers covering the whole barley genome, 91 significant marker-trait associations were detected, corresponding to 48 different genomic regions.

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References

  • Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356

    Article  Google Scholar 

  • Beattie AD, Edney MJ, Scoles GJ, Rossnagel BG (2010) Association mapping of malting quality data from western Canadian two-row barley cooperative trails. Crop Sci 50:1649–1663

    Article  Google Scholar 

  • Brantestam AK, von Bothmer R, Dayteg C, Rashal I, Tuvesson S, Weibull J (2007) Genetic diversity changes and relationships in spring barley (Hordeum vulgare L.) germplasm of nordic and baltic areas as shown by SSR markers. Genet Resour Crop Evol 54:749–758

    Article  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed  Google Scholar 

  • Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172:557–567

    Article  PubMed  CAS  Google Scholar 

  • Cardon LR, Bel JI (2001) Association study designs for complex diseases. Nat Rev Genet 2:91–99

    Article  PubMed  CAS  Google Scholar 

  • Chaabane R, El Felah M, Salah HB, Naceur MB, Abdelly C, Ramla D, Nada A, Saker M (2009) Molecular characterization of tunisian barley (Hordeum vulgare L.) genotypes using microsatellites (SSRs) markers. Eur J Sci Res 36:6–15

    Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szűcs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, De Young J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582

    Article  PubMed  Google Scholar 

  • Cockram J, White J, Leigh FJ, Lea VJ, Chiapparino E, Laurie DA, Mackay IJ, Powell W, O’Sullivan DM (2008) Association mapping of partitioning loci in barley. BMC Genet 9:16

    Article  PubMed  Google Scholar 

  • Cockram J, White J, Zuluaga DL, Smith D, Comadran J, Macaulay M, Luo Z, Kearsey MJ, Werner P, Harrap D, Tapsell C, Liu H, Hedley PE, Stein N, Schulte D, Steuernagel B, Marshall DF, Thomas WTB, Ramsay L, Mackay I, Balding DJ, The AGOUEB Consortium, Waugh R, O’Sullivan DM (2010) Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci USA 107:21611–21616

    Article  PubMed  CAS  Google Scholar 

  • Comadran J, Thomas WTB, van Eeuwijk FÁ, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A, Benbelkacem A, Ouabbou H, Bort J, Romagosa I, Hackett CA, Russell JR (2009) Patterns of genetic diversity and linkage disequilibrium in a highly structured Hordeum vulgare association-mapping population for the Mediterranean basin. Theor Appl Genet 119:175–187

    Article  PubMed  CAS  Google Scholar 

  • Dice LR (1945) Measures of the amount of ecological association between species. Ecology 26:297–302

    Article  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  PubMed  CAS  Google Scholar 

  • Friedt W, Ordon F (2008) Molecular markers for gene pyramiding and resistance breeding in barley. In: Varshney R, Tuberosa R (eds) Genomics-assisted crop improvement, vol 2. Genomics applications in crops. Springer, Berlin, pp 81–101

    Google Scholar 

  • Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S (2005) Genetic structure and diversity in Oryza sativa L. Genetics 169:1631–1638

    Article  PubMed  CAS  Google Scholar 

  • Hamblin MT, Close TJ, Bhat PR, Chao S, Kling JG, Abraham KJ, Blake T, Brooks WS, Cooper B, Griffey CA, Hayes PM, Hole DJ, Horsley RD, Obert DE, Smith KP, Ullrich SE, Muehlbauer GJ, Jannink J-L (2009) Population structure and linkage disequilibrium in US barley germplasm: implications for association mapping. Crop Sci 50:556–566

    Article  Google Scholar 

  • Hayes P, Szucs P (2006) Disequilibrium and association in barley: thinking outside the glass. Proc Natl Acad Sci USA 103:18385–18386

    Article  PubMed  CAS  Google Scholar 

  • Igartua E, Casas AM, Ciudadà F, Montoyaà JL, Romagosa I (1999) RFLP markers associated with major genes controlling heading date evaluated in a barley germ plasm pool. Heredity 83:551–559

    Article  PubMed  Google Scholar 

  • Inostroza L, del Pozo A, Matus I, Castillo D, Hayes P, Machado S, Corey A (2009) Association mapping of plant height, yield, and yield stability in recombinant chromosome substitution lines (RCSLs) using Hordeum vulgare subsp. spontaneum as a source of donor alleles in a Hordeum vulgare subsp. vulgare background. Mol Breed 23:365–376

    Article  Google Scholar 

  • Ivandic V, Thomas WTB, Nevo E, Zhang Z, Forster BP (2003) Associations of simple sequence repeats with quantitative trait variation including biotic and abiotic stress tolerance in Hordeum spontaneum. Plant Breed 122:300–304

    Article  CAS  Google Scholar 

  • Jannink J-L, Bink MCAM, Jansen RC (2001) Using complex plant pedigrees to map valuable genes. Trends Plant Sci 6:337–342

    Article  PubMed  CAS  Google Scholar 

  • Jun T-H, Van K, Kim MY, Lee S-H, Walker DR (2008) Association analysis using SSR markers to find QTL for seed protein content in soybean. Euphytica 162:179–191

    Article  CAS  Google Scholar 

  • Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 104:1424–1429

    Article  PubMed  CAS  Google Scholar 

  • Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446

    Article  PubMed  CAS  Google Scholar 

  • Kraakman ATW, Martinez F, Mussiraliev B, van Eeuwijk FA, Niks RE (2006) Linkage disequilibrium mapping of morphological, resistance, and other agronomically relevant traits in modern spring barley cultivars. Mol Breed 17:41–58

    Article  CAS  Google Scholar 

  • Kraft T, Hansen M, Nilsson N-O (2000) Linkage disequilibrium and fingerprinting in sugar beet. Theor Appl Genet 101:323–326

    Article  Google Scholar 

  • Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L.) cross. Genome 38:575–585

    Article  PubMed  CAS  Google Scholar 

  • Malysheva-Otto LV, Ganal MW, Röder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet 7:6

    Article  PubMed  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman M, Sanchez JG, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084

    Article  PubMed  CAS  Google Scholar 

  • Matthies IE, Weise S, Roeder M (2009a) Association of haplotype diversity in the a-amylase gene amy1 with malting quality parameters in barley. Mol Breed 23:139–152

    Article  CAS  Google Scholar 

  • Matthies IE, Weise S, Foerster J, Roeder M (2009b) Association mapping and marker development of the candidate genes (1 → 3), (1 → 4)-β-d-glucan-4-glucanohydrolase and (1 → → → 4)-β-xylan-endohydrolase 1 for malting quality in barley. Euphytica 170:109–122

    Article  CAS  Google Scholar 

  • Mohlke KL, Lange EM, Valle TT, Ghosh S, Magnuson VL, Silander K, Watanabe RM, Chines PS, Bergman RN, Tuomilehto J, Collins FS, Boehnke M (2010) Linkage disequilibrium between microsatellite markers extends beyond 1 cM on chromosome 20 in finns. Genome Res 11:1221–1226

    Article  Google Scholar 

  • Morrell PL, Toleno DM, Lundy KE, Clegg MT (2005) Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilization. Proc Natl Acad Sci USA 102:2442–2447

    Article  PubMed  CAS  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:1360–1385

    Article  Google Scholar 

  • Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193

    Article  PubMed  CAS  Google Scholar 

  • Oliphant A, Barker DL, Stuelpnagel JR, Chee MS (2002) BeadArray technology: enabling an accurate, cost-effective approach to high-throughput genotyping. Biotechniques 32:56–61

    Google Scholar 

  • Ordon F, Ahlemeyer J, Werner K, Koehler W, Friedt W (2005) Molecular assessment of genetic diversity in winter barley and its use in breeding. Euphytica 146:21–28

    Article  CAS  Google Scholar 

  • Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Przeworski M (2001) Linkage disequilibrium in humans: models and data. Am J Hum Genet 69:1–14

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pswarayi A, van Eeuwijk FA, Ceccarelli S, Grando S, Comadran J, Russell JR, Pecchioni N, Tondelli A, Akar T, Al-Yassin A, Benbelkacem A, Ouabbou H, Thomas WTB, Romagosa I (2008) Changes in allele frequencies in landraces, old and modern barley cultivars of marker loci close to QTL for grain yield under high and low input conditions. Euphytica 163:435–447

    Article  Google Scholar 

  • Qi X, Niks RE, Stam P, Lindhout P (1998) Identification of QTLs for partial resistance to leaf rust (Puccinia hordei) in barley. Theor Appl Genet 96:1205–1215

    Article  CAS  Google Scholar 

  • Ramsay L, Macaulay M, Degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh R (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005

    PubMed  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuola Y, Wilson LM, Whitt SR (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ (2000) NTSYS-pc: numerical taxonomy and multivariate analysis system, version 2.1. Exeter Software, Setauket

    Google Scholar 

  • Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF, Graner A, Close TJ, Waugh R (2006) Recent history of artificial outcrossing facilitates whole genome association mapping in elite crop varieties. Proc Natl Acad Sci USA 103:18656–18661

    Article  PubMed  CAS  Google Scholar 

  • Roy JK, Smith KP, Muehlbauer GJ, Chao S, Close TJ, Steffenson BJ (2010) Association mapping of spot blotch resistance in wild barley. Mol Breed 26:243–256

    Article  PubMed  Google Scholar 

  • SAS Institute (2004) SAS® 9.1.2 qualification tools user’s guide. SAS Institute, Cary

    Google Scholar 

  • Schmalenbach I, Léon J, Pillen K (2009) Identification and verification of QTLs for agronomic traits using wild barley introgression lines. Theor Appl Genet 118:483–497

    Article  PubMed  CAS  Google Scholar 

  • Skøt L, Humphreys MO, Armstead I, Heywood S, Skøt KP, Sanderson R, Thomas ID, Chorlton KH, Hamilton NRS (2005) An association mapping approach to identify flowering time genes in natural populations of Lolium perenne (L.). Mol Breed 15:233–245

    Article  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. W.H. Freeman, San Francisco

    Google Scholar 

  • Stein N, Herren G, Keller B (2001) A new DNA extraction method for high-throughput marker analysis in a large-genome species such as Triticum aestivum. Plant Breed 120:354–356

    Article  CAS  Google Scholar 

  • Stracke S, Prester T, Stein N, Perovic D, Ordon F, Graner A (2007) Effects of introgression and recombination on haplotype structure and linkage disequilibrium surrounding a locus encoding bymovirus resistance in barley. Genetics 175:805–817

    Article  PubMed  CAS  Google Scholar 

  • Stracke S, Haseneyer G, Veyrieras J-B, Geiger HH, Sauer S, Graner A, Piepho HP (2009) Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet 118:259–273

    Article  PubMed  CAS  Google Scholar 

  • Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yan L, von Zitzewitz J, Skinner JS, Hayes PM, Dubcovsky J (2005) Molecular characterization of the duplicated meristem identity genes HvAP1a and HvAP1b in barley. Genome 48:905–912

    Article  PubMed  CAS  Google Scholar 

  • Zhang LY, Marchand S, Tinker NA, Belzile F (2009) Population structure and linkage disequilibrium in barley assessed by DArT markers. Theor Appl Genet 119:43–52

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank the co-operating breeding companies Deutsche Saatveredelung AG, Dieckmann GmbH & Co. KG, Limagrain GmbH, KWS Lochow GmbH, Nordsaat Saatzucht GmbH, Pflanzenzucht Oberlimpurg, Saatzucht Bauer GmbH & Co. KG, Lantmännen SW Seed GmbH, Saatzucht Josef Breun GmbH & Co. KG, Saatzucht Streng GmbH & Co. KG, Secobra Saatzucht GmbH and W. von Borries-Eckendorf GmbH & Co. KG for their support. This work is financed by the German Research Foundation (DFG) as part of the Collaborative Research Centre (SFB) 299 at the University of Giessen and by the Federal Ministry of Education and Research (BMBF) within the framework of GABI-GENOBAR (FKZ 03115066 A–E).

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Rode, J., Ahlemeyer, J., Friedt, W. et al. Identification of marker-trait associations in the German winter barley breeding gene pool (Hordeum vulgare L.). Mol Breeding 30, 831–843 (2012). https://doi.org/10.1007/s11032-011-9667-6

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