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Haplotype diversity and population structure in cultivated and wild barley evaluated for Fusarium head blight responses

Abstract

Fusarium head blight (FHB) is a threat to barley (Hordeum vulgare L.) production in many parts of the world. A number of barley accessions with partial resistance have been reported and used in mapping experiments to identify quantitative trait loci (QTL) associated with FHB resistance. Here, we present a set of barley germplasm that exhibits FHB resistance identified through screening a global collection of 23,255 wild (Hordeum vulgare ssp. spontaneum) and cultivated (Hordeum vulgare ssp. vulgare) accessions. Seventy-eight accessions were classified as resistant or moderately resistant. The collection of FHB resistant accessions consists of 5, 27, 46 of winter, wild and spring barley, respectively. The population structure and genetic relationships of the germplasm were investigated with 1,727 Diversity Array Technology (DArT) markers. Multiple clustering analyses suggest the presence of four subpopulations. Within cultivated barley, substructure is largely centered on spike morphology and growth habit. Analysis of molecular variance indicated highly significant genetic variance among clusters and within clusters, suggesting that the FHB resistant sources have broad genetic diversity. The haplotype diversity was characterized with DArT markers associated with the four FHB QTLs on chromosome 2H bin8, 10 and 13 and 6H bin7. In general, the wild barley accessions had distinct haplotypes from those of cultivated barley. The haplotype of the resistant source Chevron was the most prevalent in all four QTL regions, followed by those of the resistant sources Fredrickson and CIho4196. These resistant QTL haplotypes were rare in the susceptible cultivars and accessions grown in the upper Midwest USA. Some two- and six-rowed accessions were identified with high FHB resistance, but contained distinct haplotypes at FHB QTLs from known resistance sources. These germplasm warrant further genetic studies and possible incorporation into barley breeding programs.

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References

  • Anderson MJ (2003) PCO: a FORTRAN computer program for principal coordinate analysis. Department of Statistics, University of Auckland, New Zealand

  • Bai G, Shaner G (2004) Management and resistance in wheat and barley to fusarium head blight. Annu Rev Phytopathol 42:135–161

    PubMed  Article  CAS  Google Scholar 

  • Bai G, Guo P, Kolb FL (2003) Genetic relationships among head blight resistant cultivars of wheat assessed on the basis of molecular markers. Crop Sci 43:498–507

    Article  CAS  Google Scholar 

  • Beaubien KA, Nduulu LM, Smith KA (2004) Mapping FHB resistance QTL in a barley population derived from an Atahualpa x M81 cross. Proceedings of the 2nd international symposium on Fusarium head blight, Orlando, FL USA 11-15 December 2004

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

  • Buerstmayr H, Legzdina L, Steiner B, Lemmens M (2004) Variation for resistance to Fusarium head blight in spring barley. Euphytica 137:279–290

    Article  CAS  Google Scholar 

  • Canci PC, Nduulu LM, Muehlbauer GJ, Dill-Macky R, Rasmusson DC, Smith KP (2004) Validation of quantitative trait loci for Fusarium head blight and kernel discoloration in barley. Mol Breeding 14:91–104

    Article  CAS  Google Scholar 

  • Chen X-M, Yang Y-H, Gao D-S (1991) Primary identification of resistance to scab of Chinese barley germplasm sources. Zhejing Agric Sci 2:91–97

    Google Scholar 

  • Choo TM (2005) Breeding Barley for Resistance to Fusarium Head Blight and Mycotoxin Accumulation. Plant Breeding Reviews. John Wiley & Sons, Inc., pp 125-169

  • Choo TM, Martin RA, Ho KM, Shen Q, Fedak G, Savard M, Voldeng H, Falk DE, Etienne M, Sparry E (2004) Fusarium head blight and deoxynivalenol accumulation of barley in eastern Canada: cultivar response and correlation analysis. Plant Dis 88:837–844

    Article  CAS  Google Scholar 

  • Comadran J, Thomas WT, van Eeuwijk FA, 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

    PubMed  Article  CAS  Google Scholar 

  • Dahl SK, Bockelman HE, Kovaleva O, Loskotov I, Kleijer G, Ottosson F, Valkoun J, Kessler D, St. Pierre R, Anikster Y, Steffenson BJ (2009) Evaluation of Hordeum accessions for resistance to Fusarium head blight. Proceedings of the 2009 national Fusarium head blight forum, Orlando, FL 7–9 December 2009

  • Dahleen LS, Agrama HA, Horsley RD, Steffenson BJ, Schwarz PB, Mesfin A, Franckowiak JD (2003) Identification of QTLs associated with Fusarium head blight resistance in Zhedar 2 barley. Theor Appl Genet 108:95–104

    PubMed  Article  CAS  Google Scholar 

  • de la Peña RC, Smith KP, Capettini F, Muehlbauer GJ, Gallo-Meagher M, Dill-Macky R, Somers DA, Rasmusson DC (1999) Quantitative trait loci associated with resistance to Fusarium head blight and kernel discoloration in barley. Theor Appl Genet 99:561–569

    PubMed  Article  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4, available from http://www.geneious.com/

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP—Phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Hori K, Kobayashi T, Sato K, Takeda K (2005) QTL analysis of Fusarium head blight resistance using a high-density linkage map in barley. Theor Appl Genet 111:1661–1672

    PubMed  Article  CAS  Google Scholar 

  • Hori K, Sato K, Kobayashi T, Takeda K (2006) QTL analysis of Fusarium head blight severity in recombinant inbred population derived from a cross between two-rowed barley varieties. Breed Sci 56:25–30

    Article  CAS  Google Scholar 

  • Horsley RD, Schmierer D, Maier C, Kudrna D, Urrea CA, Steffenson BJ, Schwarz PB, Franckowiak JD, Green MJ, Zhang B, Kleinhofs A (2006) Identification of QTLs associated with Fusarium head blight resistance in barley accession CIho 4196. Crop Sci 46:145–156

    Article  CAS  Google Scholar 

  • Ma Z, Steffenson BJ, Prom LK, Lapitan NLV (2000) Mapping of quantitative trait loci for Fusarium head blight resistance in barley. Phytopathology 90:1079–1088

    PubMed  Article  CAS  Google Scholar 

  • Ma H, Ge H, Zhang X, Lu W, Yu D, Chen H, Chen J (2009) Resistance to Fusarium head blight and deoxynivalenol accumulation in Chinese barley. J Phytopathol 157:166–171

    Article  CAS  Google Scholar 

  • Massman J, Cooper B, Horsley R, Neate S, Dill-Macky R, Chao S, Dong Y, Schwarz P, Muehlbauer G, Smith K (2011) Genome-wide association mapping of Fusarium head blight resistance in contemporary barley breeding germplasm. Mol Breeding 27:439–454

    Article  Google Scholar 

  • McCallum BD, Tekauz A, Gilbert J (2004) Reaction of a diverse collection of barley lines to Fusarium head blight. Plant Dis 88:167–174

    Article  Google Scholar 

  • McCartney CA, Somers DJ, Fedak G, Cao W (2004) Haplotype diversity at Fusarium head blight resistance QTLs in wheat. Theor Appl Genet 109:261–271

    PubMed  Article  CAS  Google Scholar 

  • McMullen M, Jones R, Gallenberg D (1997) Scab of wheat and barley: a re-emerging disease of devasting impact. Plant Dis 81:1340–1348

    Article  Google Scholar 

  • Mesfin A, Smith KP, Dill-Macky R, Evans CK, Waugh R, Gustus CD, Muehlbauer GJ (2003) Quantitative trait loci for Fusarium head blight resistance in barley detected in a two-rowed by six-rowed population. Crop Sci 43:307–318

    Article  CAS  Google Scholar 

  • Nduulu L, Mesfin A, Muehlbauer G, Smith K (2007) Analysis of the chromosome 2(2H) region of barley associated with the correlated traits Fusarium head blight resistance and heading date. Theor Appl Genet 115:561–570

    PubMed  Article  CAS  Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    PubMed  Article  CAS  Google Scholar 

  • Nganje WE, Kaitibie S, Wilson WW, Leistritz FL, Bangsund DA (2004) Economic impacts of Fusarium head blight in wheat and barley: 1993–2001. Agribusiness and Applied Economics Report No. 538. North Dakota State University

  • Nielsen R (2000) Estimation of population parameters and recombination rates from single nucleotide polymorphisms. Genetics 154:931–942

    PubMed  CAS  Google Scholar 

  • Niks RE, Parleliet JE, Lindhout P, Bai YL (2011) Breeding crops with resistance to diseases and pests. Wageningen Academic Publishers, Wageningen, the Netherlands

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

    PubMed  CAS  Google Scholar 

  • Prom LK, Steffenson BJ, Salas B, Fetch TG, Casper HH (1996) Evaluation of selected barley accessions for resistance to Fusarium head blight and deoxynivalenol concentration. In: Slinkard A, Scoles G, Rossnagel B (eds) Proceedings of the Seventh International Barley Genetics Symposium, University Extension Press, Saskatoon, Saskatchewan, p 764–766

  • Ramage RT, Thompson RK, Eslick RF, Wesenberg DM, Wiebe GA, Craddock JC (1976) Registration of barley composite crosses XXX-A to G. Crop Sci 16:314

    Article  Google Scholar 

  • Rasmusson DC, Wilcoxson RD, Dill-Macky R, Schiefelbein EL, Wiersma JV (1999) Registration of MNBrite barley. Crop Sci 39:290

    Article  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 inbred crop varieties. Proc Natl Acad Sci USA 103:18656–18661

    PubMed  Article  CAS  Google Scholar 

  • Russell J, Dawson IK, Flavell AJ, Steffenson B, Weltzien E, Booth A, Ceccarelli S, Grando S, Waugh R (2011) Analysis of >1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol 191:564–578

    PubMed  Article  Google Scholar 

  • Steffenson BJ (1992) Analysis of durable resistance to stem rust in barley. Euphytica 63:153–167

    Article  Google Scholar 

  • Steffenson BJ (2003a) Fusarium head blight of barley: impact, epidemics, management, and strategies for identifying and utilizing genetic resistance. In: Leonard KJ, Bushnell WR (eds) Fusarium head blight of wheat and barley. The American Phytopathological Society, St. Paul, pp 241–295

    Google Scholar 

  • Steffenson BJ (2003b) A population approach for identifing Fusarium head blight resistance in barley. 2003 National Fusarium head blight forum proceedings, Bloomington, MN 13–15 December 2003

  • Steffenson BJ, Dahl SK (2003) Evaluation of Swiss barley landraces for resistance to Fusarium head blight. 2003 National Fusarium head blight forum proceedings, Bloomington, MN 13–15 December 2003

  • Steffenson BJ, Dahl SK (2008) Into the wild: FHB resistance identified in Hordeum vulgare subsp. spontaneum. Proceedings of the 2008 national Fusarium head blight forum, Indianapolis, IN 2–4 December 2008

  • Steffenson BJ, Scholz U (2001) Evaluation of Hordeum accessions for resistance to Fusarium head blight. 2001 National Fusarium head blight forum proceedings, Erlanger, KY 8–10 December 2001

  • Steffenson BJ, Dahl SK, Loskotov I (2005) Fusarium head blight resistance in barley accessions from the N. I. Vavilov institute. Proceedings of the 2005 national Fusarium head blight forum, Milwaukee, WI 11–13 December 2005

  • Takeda K, Heta H (1989) Establishing the testing method and a search for the resistant varieties to Fusarium head blight in barley. Jpn J Breed 39:203–216

    Google Scholar 

  • Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity Arrays Technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920

    PubMed  Article  CAS  Google Scholar 

  • Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesna J, Cakir M, Poulsen D, Wang J, Raman R, Smith KP, Muehlbauer GJ, Chalmers KJ, Kleinhofs A, Huttner E, Kilian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206

    PubMed  Article  Google Scholar 

  • Wingbermuehle WJ, Gustus C, Smith KP (2004) Exploiting selective genotyping to study genetic diversity of resistance to Fusarium head blight in barley. Theor Appl Genet 109:1160–1168

    PubMed  Article  CAS  Google Scholar 

  • Yoshida M, Kawada N, Tohnooka T (2005) Effect of row type, flowering type and several other spike characters on resistance to Fusarium head blight in barley. Euphytica 141:217–227

    Article  Google Scholar 

  • Yu JB, Bai GH, Cai SB, Ban T (2006) Marker-assisted characterization of Asian wheat lines for resistance to Fusarium head blight. Theor Appl Genet 113:308–320

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Zhou X, Chao M, Liang X (1991) Screening and testing of barley varieties for scab resistance. Acta Phytophylacica Sin 18:261–265

    Google Scholar 

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Acknowledgments

This work was supported by grants from the U.S. Wheat and Barley Scab Initiative (United States Department of Agriculture-Agricultural Research Service) to G. J. Muehlbauer, K. P. Smith and B. J. Steffenson, grant from Minnesota Small Grains Initiative to G. J. Muehlbauer, and Lieberman-Okinow Endowment at the University of Minnesota to B. J. Steffenson. We thank Harold Bockelman (USDA-ARS National Small Grains Collection); O. Kovaleva and I. Loskotov (N. I. Vavilov All-Russian Scientific Research Institute of Plant Industry); G. Kleijer (Station federale de recherché en production vegetale de Changins); F. Ottosson (Nordic Gene Bank, now NordGen); Y. Anikster (Institute for Cereal Crops Improvement); J. Valkoun (International Center for Agricultural Research in the Dry Areas); and D. Kessler and R. St. Pierre (Plant Genetic Resources of Canada) for providing the germplasm used in this study.

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Correspondence to Gary J. Muehlbauer.

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Communicated by A. Graner.

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Huang, Y., Millett, B.P., Beaubien, K.A. et al. Haplotype diversity and population structure in cultivated and wild barley evaluated for Fusarium head blight responses. Theor Appl Genet 126, 619–636 (2013). https://doi.org/10.1007/s00122-012-2006-4

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  • DOI: https://doi.org/10.1007/s00122-012-2006-4

Keywords

  • Quantitative Trait Locus
  • Fusarium Head Blight
  • Chevron
  • Quantitative Trait Locus Region
  • DArT Marker