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Association mapping of grain hardness, polyphenol oxidase, total phenolics, amylose content, and β-glucan in US barley breeding germplasm

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Abstract

A renewed interest in breeding barley specifically for food end-uses is being driven by increased consumer interest in healthier foods. We conducted association mapping on physicochemical properties of barley that play a role in food quality and processing including grain hardness, polyphenol oxidase activity, total phenolics, amylose content, and β-glucan. We used 3,069 elite two-row and six-row spring barley breeding lines from eight US breeding programs and 2,041 SNP markers for association mapping. Marker–trait associations were identified using a mixed model that incorporated population structure and kinship. We detected two previously identified QTL for grain hardness on chromosome 2H in the telomeric region of 5H along with two novel regions on 4H and 6H. For amylose content, we detected marker–trait associations on 7H from 0.63 to 30 cM. We detected four regions on chromosomes 1H, 2H, 3H, and 4H associated with polyphenol oxidase activity. The chromosome 2H region co-localized with the two previously mapped polyphenol oxidase genes PPO1 and PPO2, and the regions on chromosomes 1H, 3H, and 4H QTL were novel. For total phenolics, we identified three significant regions on 3H, 4H, and 5H. Two regions on 2H and 7H were associated with β-glucan. Both previously identified and novel QTL are segregating in elite US breeding germplasm. Only three of the 24 SNPs that were associated with traits using either the two-row or six-row mapping panel were identified in both panels. Nine SNPs were detected in the individual two-row or six-row panels that were not detected in the analysis using the complete panel and accounting for population structure. The distribution of favorable alleles at these loci that underpin food quality across the breeding programs suggests several strategies to use markers to improve barley for food uses.

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References

  • Baik BK, Ullrich SE (2008) Barley for food: characteristics, improvement, and renewed interest. J Cereal Sci 48:233–242

    Article  CAS  Google Scholar 

  • Beecher B, Bettge A, Smidansky E, Giroux MJ (2002a) Expression of wildtype pinB sequence in transgenic wheat complements a hard phenotype. Theor Appl Gen 105:870–877

    Article  CAS  Google Scholar 

  • Beecher B, Bowman J, Martin JM, Bettge AD, Morris CF, Blake TK, Giroux MJ (2002b) Hordoindolines are associated with a major endosperm-texture QTL in barley (Hordeum vulgare). Genome 45:584–591

    Article  PubMed  CAS  Google Scholar 

  • Behall KM, Scholfield DJ, Yuhauiak I, Canary J (1989) Diets containing high amylose vs amylopectin starch: effects on metabolic variables in human subjects. Am J Clin Nutr 49:337–344

    PubMed  CAS  Google Scholar 

  • Behall KM, Scholfield DJ, Hallfrisch J (2004) Diets containing barley significantly reduce lipids in mildly hypercholesterolemic men and women. Am J Clin Nutr 80:1185–1193

    PubMed  CAS  Google Scholar 

  • Bendelow VM (1977) Automated procedure for the estimation of total polyphenol content in beer, wort, malt, and barley. J Am Soc Brew Chem 35:150–152

    CAS  Google Scholar 

  • Berger GL, Liu S, Hall MD, Brooks WS, Chao S, Muehlbauer GJ, Baik BK, Steffenson B, Griffey CA (2013) Marker-trait associations in Virginia Tech winter barley identified using genome-wide mapping. Theor Appl Genet 126:693–710

    Article  PubMed  CAS  Google Scholar 

  • Bhave M, Morris CF (2008) Molecular genetics of puroindolines and related genes: allelic diversity in wheat and other grasses. Plant Mol Biol 66:205–219

    Article  PubMed  CAS  Google Scholar 

  • Bourdon I, Yokoyama W, Davis P, Hudson C, Backus R, Richter D, Knuckles B, Schneeman BO (1999) Postprandial lipid, glucose, insulin, and cholecystokinin responses in men fed barley pasta enriched with beta-glucan. Am J Clin Nutr 69:55–63

    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

    Article  PubMed  CAS  Google Scholar 

  • Caldwell KS, Langridge P, Powell W (2004) Comparative sequence analysis of the region harboring the hardness locus in barley and its colinear region in rice. Plant Physiol 136:1–14

    Article  Google Scholar 

  • Charles M, Tang H, Belcram H, Paterson A, Gornicki P, Chalhoub B (2009) Sixty million years in evolution of soft grain trait in grasses: emergence of the softness locus in the common ancestor of Pooideae and Ehrhartoideae, after their divergence from Panicoideae. Mol Biol Evol 26:1651–1661

    Article  PubMed  CAS  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, DeYoung 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 Genom 10:582

    Article  Google Scholar 

  • Dykes L, Rooney LW (2007) Phenolic compounds in cereal grains and their health benefits. Cereal Foods World 52:105–111

    CAS  Google Scholar 

  • Endelman JB (2011) Ridge regression and other kernels for genomic selection with R package rrBLUP. Plant Genome 4:250–255

    Article  Google Scholar 

  • Fox GP, Osborne B, Bowman J, Kelly A, Cakir M, Poulsen D, Inkerman A, Henry R (2007) Measurement of genetic and environmental variation in barley (Hordeumvulgare) grain hardness. J Cereal Sci 46:82–92

    Article  CAS  Google Scholar 

  • Gaines CS, Finney PF, Fleege LM, Andrews LC (1996) Predicting a hardness measurement using the single-kernel characterization system. Cereal Chem 73:278–283

    CAS  Google Scholar 

  • Giroux MJ, Morris CF (1997) A glycine to serine change in puroindoline b is associated with wheat grain hardness and low level of starch-surface friabilin. Theor Appl Genet 95:857–864

    Article  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 JL (2010) Population structure and linkage disequilibrium in U.S. barley germplasm: implications for association mapping. Crop Sci 50:556–566

  • Han F, Ullrich SE, Chirat S, Menteur S, Jestin L, Sarrafi A, Hayes PM, Jones BL, Blake TK, Wesenberg DM, Kleinhofs A, Kilian A (1995) Mapping of β-glucan content and β-glucanase activity loci in barley grain and malt. Theor Appl Genet 91:921–927

    PubMed  CAS  Google Scholar 

  • Hu G, Charlotte B, Chunyan Y (2010) Efficient measurement of amylose content in cereal grains. J Cereal Sci 51:35–40

    Article  CAS  Google Scholar 

  • Islamovic E, Obert DE, Oliver RE, Harrison SA, Ibrahim A, Marshall JM, Miclaus KJ, Hu G, Jackson EW (2013) Genetic dissection of grain beta-glucan and amylose content in barley (Hordeum vulgare L.). Mol Breed 31:15–25

    Article  CAS  Google Scholar 

  • Kang HM, Sul JH, Service SK, Zaitlen NA, Kong S, Freimer NB, Sabatti C, Eskin E (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42:348–354

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Knapp SJ, Bridges WC (1990) Using molecular markers to estimate quantitative trait locus parameters: power and genetic variances for unreplicated and replicated progeny. Genetics 126:769–777

    PubMed  CAS  PubMed Central  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  PubMed Central  Google Scholar 

  • Leonard W (1942) Inheritance of fertility in the lateral spikelets of barley. Genetics 27:299–316

    PubMed  CAS  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • McIntosh GH, Whyte J, McArthur R, Nestel PJ (1991) Barley and wheat foods: influence on plasma cholesterol concentrations in hypercholesterolemic men. Am J Clin Nutr 53:1205–1209

    PubMed  CAS  Google Scholar 

  • Muñoz-Amatriaín M, Moscou MJ, Bhat PR, Svensson JT, Bartoš J, Suchánková P, Šimková H, Endo TR, Fenton RD, Lonardi S, Castillo AM, Chao S, Cistué L, Cuesta-Marcos A, Forrest KL, Hayden MJ, Hayes PM, Horsley RD, Makoto K, Moody D, Sato K, Vallés MP, Wulff BBH, Muehlbauer GJ, Doležel J, Close TJ (2011) An improved consensus linkage map of barley based on flow-sorted chromosomes and single nucleotide polymorphism markers. Plant Genome 4:238–249

    Article  Google Scholar 

  • Nair S, Ullrich SE, Blake TK, Cooper B, Griffey CA, Hayes PM, Hole DJ, Horsley RD, Obert DE, Smith KP, Muehlbauer GJ, Baik BK (2010) Variation in kernel hardness and associated traits in USA barley breeding lines. Cereal Chem 87:461–466

    Article  CAS  Google Scholar 

  • Nair S, Ullrich SE, Baik BK (2011) Association of barley kernel hardness with physical grain traits and food processing parameters. Cereal Chem 88:147–152

    Article  CAS  Google Scholar 

  • Nelson JC, Andreescu C, Breseghello F, Finney PL, Gualberto DG, Bergman CJ, Pena RJ, Perretant MR, Leroy P, Qualset CO, Sorrells ME (2006) Quantitative trait locus analysis of wheat quality traits. Euphytica 149:145–159

    Article  CAS  Google Scholar 

  • Oziel A, Hayes PM, Chen FQ, Jones B (1996) Application of quantitative trait locus mapping to the development of winter habit malting barley. Plant Breed 115:43–51

    Article  CAS  Google Scholar 

  • QuindeAxtell Z, Ullrich SE, Baik BK (2004) Genotypic variation in color and discoloration potential of barley-based food products. Cereal Chem 81:752–758

    Article  Google Scholar 

  • QuindeAxtell Z, Powers J, Baik BK (2006) Retardation of discoloration in barley flour gel and dough. Cereal Chem 83:385–390

    Article  CAS  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www-R-project.org

  • Rohde W, Becker D, Salamini F (1988) Structural analysis of the waxy locus from Hordeumvulgare. Nucleic Acids Res 16:7185–7186

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rouvès S, Boeuf C, Zwickert-Menteur S, Gautier MF, Joudrier P, Nelson JC, Bernard M, Jestin L (1996) Locating supplementary RFLP markers on barley chromosome 7 and synteny with homoeologous wheat group 5. Plant Breed 115:511–513

    Article  Google Scholar 

  • Rutkoski JE, Poland J, Jannink JL, Sorrells ME (2013) Imputation of unordered markers and the impact on genomic selection accuracy. G3 3:427–439

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmitt MR, Wise ML (2009) Barley and oat β-glucan content measured by Calcofluor fluorescence in a microplate assay. Cereal Chem 86:187–190

    Article  CAS  Google Scholar 

  • Schondelmaier J, Jacobi A, Fischbeck G, Jahoor A (1992) Genetical studies on the mode of inheritance and localization of the amo1 (high amylose) gene in barley. Plant Breed 109:274–280

    Article  Google Scholar 

  • See D, Kanazin V, Kephart K, Blake T (2002) Mapping genes controlling variation in barley grain protein concentration. Crop Sci 42:680–685

    Article  CAS  Google Scholar 

  • Shimizu C, Kihara M, Aoe S, Araki S, Ito K, Hayashi K, Watari J, Sakata Y, Ikegami S (2008) Effect of high beta-glucan barley on serum cholesterol concentrations and visceral fat area in Japanese men—a randomized, double-blinded, placebo-controlled trial. Plant Foods Hum Nutr 63:21–25

    Article  PubMed  CAS  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Szűcs P, Blake VC, Bhat PR, Chao S, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay L, Waugh R, Hayes PM (2009) An integrated resource for barley linkage map and malting quality QTL alignment. Plant Genome 2:134–140

    Article  Google Scholar 

  • Taketa S, Matsuki K, Amano S, Saisho D, Himi E, Shitsukawa N, You T, Noda K, Takeda K (2010) Duplicate polyphenol oxidase genes on barley chromosome 2H and their functional differentiation in the phenol reaction of spikes and grains. J Exp Bot 61:3983–3993

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Turuspekov Y, Beecher B, Darlington Y, Bowman J, Blake TK, Giroux MJ (2008a) Hardness locus sequence variation and endosperm texture in spring barley. Crop Sci 48:1007–1019

    Article  CAS  Google Scholar 

  • Turuspekov Y, Martin JM, Bowman JGP, Beecher BS, Giroux MJ (2008b) Associations between Vrs1 alleles and grain quality traits in spring barley Hordeum vulgare L. Cereal Chem 85:817–823

    Article  CAS  Google Scholar 

  • Ullrich SE, Clancy JA, Eslick RF, Lance RCM (1986) β-Glucan content and viscosity of extracts from waxy barley. J Cereal Sci 4:279–285

    Article  CAS  Google Scholar 

  • Walker CK, Panozzo JF, Ford R, Eckermann P, Moody D, Lehmensiek A, Appels R (2011) Chromosomal loci associated with endosperm hardness in a malting barley cross. Theor Appl Genet 122:151–162

    Article  PubMed  Google Scholar 

  • Wang M, Jiang N, Jia T, Leach L, Cockram J, Comadran J, Shaw P, Waugh R, Luo Z (2012) Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor Appl Genet 124:233–246

    Article  PubMed  Google Scholar 

  • Williams PC, Kuzina FD, Hlynka I (1970) A rapid colorimetric procedure for estimating the amylose content of starches and flours. Cereal Chem 47:411–421

    CAS  Google Scholar 

  • Wood PJ, Weisz J (1984) Use of calcofluor in analysis of oat beta-D-glucan. Cereal Chem 61:73–75

    CAS  Google Scholar 

  • Yadav SK, Luthra YP, Sood DR, Aggarwal NK (2000) Gibberellic acid (GA3) induced changes in proanthocyanidins and malt quality of two- and six-row husked barleys. Plant Foods Hum Nutr 55:87–96

    Article  PubMed  CAS  Google Scholar 

  • Yanaka M, Takata K, Terasawa Y, Ikeda TM (2011) Chromosome 5H of Hordeum species involved in reduction in grain hardness in wheat genetic background. Theor Appl Genet 123:1013–1018

    Article  PubMed  Google Scholar 

  • Zheng GH, Sosulski FW (1998) Determination of water separation from cooked starch and flour pastes after refrigeration and freeze-thaw. J Food Sci 63:134–139

    Article  CAS  Google Scholar 

  • Zhou H, Muehlbauer G, Steffenson B (2012) Population structure and linkage disequilibrium in elite barley breeding germplasm from the United States. J Zhejiang Univ Sci B 13:438–451

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We gratefully acknowledge the technical support of Tracy Harris for phenotyping the barley lines. We also thank the breeders who contributed two-row spring lines for this research: D. Obert, formerly USDA-ARS, Aberdeen, ID; T. Blake, Montana State University; and R. Horsley, North Dakota State University. T. Blake and K. Smith grew the grain samples for phenotyping. This research was supported by USDA-CSREES-NRI Grant No. 2006-55606-16722 and USDA-NIFA Grant No. 2009-85606-05701 and 2011-68002-30029, the Washington State University Agricultural Research Center, and the Washington State University Center for Sustaining Agriculture and Natural Resources.

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Authors and Affiliations

  1. Department of Agronomy and Plant Genetics, University of Minnesota, 411 Borlaug Hall, 1991 Upper Buford Circle, St. Paul, MN, 55108-6026, USA

    Mohsen Mohammadi, Gary J. Muehlbauer & Kevin P. Smith

  2. Department of Horticulture, University of Wisconsin, Madison, WI, 53706, USA

    Jeffrey B. Endelman

  3. Department of Crop and Soil Sciences, Washington State University, Pullman, WA, 99164, USA

    Sindhu Nair, Stephen S. Jones & Steven E. Ullrich

  4. Biosciences Research Lab, USDA-ARS, Fargo, ND, 58105, USA

    Shiaoman Chao

  5. Cereal Crops Research, USDA-ARS, Madison, WI, 53726, USA

    Mitchell L. Wise

  6. Soft Wheat Quality Lab, USDA-ARS, Wooster, OH, 44691, USA

    Byung-Kee Baik

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  1. Mohsen Mohammadi
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  2. Jeffrey B. Endelman
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  3. Sindhu Nair
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  4. Shiaoman Chao
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  6. Gary J. Muehlbauer
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  9. Mitchell L. Wise
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  10. Kevin P. Smith
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Correspondence to Kevin P. Smith.

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Supplemental Fig. S1. Histograms displaying phenotypic variations of traits. (PPTX 76 kb)

Supplemental Fig. S2. Linkage disequilibrium for the entire sample for a window of 0-50 cM in terms of R2. (PPTX 80 kb)

11032_2014_112_MOESM3_ESM.pptx

Supplemental Fig. S3. Manhattan plots of genome-wide association mapping for five traits with P + K model for entire, six-row and two-row association panels, and individual year panels. A horizontal line is drawn at the 5 % false discovery rate when significant associations are detected. (PPTX 4703 kb)

11032_2014_112_MOESM4_ESM.xlsx

Supplemental Table S1. SNP names and map coordinates along with minor allele frequencies and marker–trait association signals obtained from the entire sample, six-row, two-row, and individual years association panels. The map distances are shown in cM. A total of 2041 polymorphic and map markers which did not have more than 10 % missing data were used for kinship and population structure. On the basis of a minimum number of 30 individuals for accurate phenotype estimation of the rare variants and the total size of each panel, we determined appropriate minor allele frequency filter for each association panel. Data points for each trait are –log P values obtained from P + K model for each association panel. The multi-year analyses for grain hardness (GH), β-glucan (BG), and polyphenol oxidase (PPO) are based on data obtained from 2006 to 2009 and for amylose content (AC) and total phenolics (TP) on data from 2006 to 2008. Cells highlighted in grey (0 s) represent markers that were filtered due to less than 30 variants in the minor allele class. Cells highlighted in salmon represent markers that showed significant marker–trait association at FDR 5 % for each association panel. (XLSX 1476 kb)

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Mohammadi, M., Endelman, J.B., Nair, S. et al. Association mapping of grain hardness, polyphenol oxidase, total phenolics, amylose content, and β-glucan in US barley breeding germplasm. Mol Breeding 34, 1229–1243 (2014). https://doi.org/10.1007/s11032-014-0112-5

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