A genome wide association scan for (1,3;1,4)-β- glucan content in the grain of contemporary 2-row Spring and Winter barleys

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Houston, Kelly ^a   Russell, Joanne ^a   Schreiber, Miriam ^a   Halpin, Claire ^a   Oakey, Helena ^a   Washington, Jennifer M ^b   Booth, Allan ^a   Shirley, Neil ^b   Burton, Rachel A ^b   Fincher, Geoffrey B ^b   Waugh, Robbie ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

(1,3; 1,4) glucan; Barley; Cell walls; GWAS; Soluble fibre

Indexed keywords

BETA GLUCAN; GLUCOSYLTRANSFERASE; GLYCOSIDASE;

ARTICLE; BARLEY; CARBOHYDRATE SYNTHESIS; CHROMOSOME 2; CONTROLLED STUDY; CSLF10 GENE; CSLF12 GENE; CSLF3 GENE; CSLF4 GENE; CSLF8 GENE; CSLH GENE; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PLANT GENE; PLANT GENOME; SINGLE NUCLEOTIDE POLYMORPHISM; ENZYMOLOGY; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; SEASON;

BETA-GLUCANS; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GENOMICS; GLUCOSYLTRANSFERASES; GLYCOSIDE HYDROLASES; HORDEUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SEASONS;

EID: 84964315172     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-907     Document Type: Article

References (74)

1. Bazzano LA, He J, Ogden LG, Loria CM, Whelton PK: Dietary fiber intake and reduced risk of coronary heart disease in US men and women: the National Health and Nutrition Examination Survey I Epidemiologic Follow-up Study. Arch Intern Med 2003, 163:1897-1904.
2. Erkkilä AT, Herrington DM, Mozaffarian D, Lichtenstein AH: Cereal fiber and whole-grain intake are associated with reduced progression of coronary-artery atherosclerosis in postmenopausal women with coronary artery disease. Am Heart J 2005, 150(1):94-101.
3. FDA Allows Barley Products to Claim Reduction in Risk of Coronary Heart Disease. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2005/ucm108543.htm.
4. Food and Drug Administration S. HH: Food labeling: health claims; soluble dietary fiber from certain foods and coronary heart disease. Final rule. Fed Regist 2006, 71(98):29248-29250.
5. Food and Drug Administration S. HH: Food labeling: health claims; soluble fiber from certain foods and risk of coronary heart disease. Final rule. Fed Regist 2008, 73(159):47828-47829.
6. Newton AC, Flavell AJ, George TS, Leat P, Mullholland B, Ramsay L, Giha CR, Russell J, Steffenson BJ, Swanston JS, Thomas WTB, Waugh R, White PJ, Bingham IJ: Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Security 2011, 3:141-178.
7. Andersen MA, Cook JA, Stone BA: Enzymatic determination of (1,3;1,4)-β-glucans in barley grain and other cereals. Inst Brew 1978, 84:233-239.
8. Havrlentova M, Kraic J: Content of β-D-glucan in cereal grains. J Food Nutr Res 2006, 45:97-103.
9. Sustagrain ®Barley. http://www.conagramills.com/media/Sustagrain%20Sell %20Sheet.pdf.
10. BARLEYmax™: high fibre wholegrain with resistant starch. http://www. csiro.au/resources/BARLEYmax.html.
11. Han F, Ullrich SE, Chirat S, Menteur S, Jestin L, Sarrafi A, Hayes PM, Jones BL, Blake TK, Wesenberg DM, Kleinhofs A, Kilian A: Mapping of (1,3;1,4)-β-glucan content and β-glucanase activity loci in barley grain and malt. Theor Appl Genet 1995, 91(6-7):921-927.
12. Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB: Cellulose Synthase-Like CslF Genes Mediate the Synthesis of Cell Wall (1-3;1-4)-β-D-Glucans. Science 2006, 311(5769):1940-1942.
13. Doblin MS, Pettolino FA, Wilson SM, Campbell R, Burton RA, Fincher GB, Newbigin E, Bacic A: A barley cellulose synthase-like CSLH gene mediates (13;14)-beta-D-glucan synthesis in transgenic Arabidopsis. Proc Natl Acad Sci U S A 2009, 106(14):5996-6001.
14. Schreiber M, Wright F, MacKenzie K, Hedley PE, Schwerdt JG, Little A, Burton RA, Fincher GB, Marshall D, Waugh R, Halpin C: The barley genome sequence assembly reveals three additional members of the CslF (1,3;1,4)-β-glucan synthase gene family. PloS One 2014. doi:10.1371/journal.pone.0090888.
15. Richmond T, Somerville C: The cellulose synthase superfamily. Plant Physiol 2000, 124:495-498.
16. Burton RA, Collins HM, Kibble NAJ, Smith JA, Shirley NJ, Jobling SA, Henderson M, Singh RR, Pettolino F, Wilson SM, Bird AR, Topping DL, Bacic A, Fincher GB: Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (13;14)-β-D-glucans and alters their fine structure. Plant Biotechnol J 2011, 9(2):117-135.
17. Clarke B, Liang R, Morell MK, Bird AR, Jenkins CL, Li Z: Gene expression in a starch synthase IIa mutant of barley: changes in the level of gene transcription and grain composition. Funct Integr Genomics 2008, 8(3):211-221.
18. Munck L, Møller B, Jacobsen S, Søndergaard I: Near infrared spectra indicate specific mutant endosperm genes and reveal a new mechanism for substituting starch with (1→3,1→4)-β-glucan in barley. J Cereal Sci 2004, 40:213-222.
19. Trafford K, Haleux P, Henderson M, Parker M, Shirley NJ, Tucker MR, Fincher GB, Burton RA: Grain development in Brachypodium and other grasses: Interactions between cell expansion, starch deposition and cell wall synthesis. J. Exp Bot 2013, 64:5033-5047.
20. Guillon F, Bouchet B, Jamme F, Robert P, Quemener B, Barron C, Larre C, Dumas P, Saulnier L: Brachypodium distachyon grain: characterization of endosperm cell walls. J Exp Bot 2011, 62:1001-1015.
21. Hoffman D, Dahleen L: Markers polymorphic among malting barley (Hordeum vulgareL.) cultivars of a narrow gene pool associated with key QTLs. Theor Appl Genet 2002, 105:544-554.
22. Molina-Cano J-L, Moralejo M, Elía M, Muñoz P, Russell JR, Pérez-Vendrell AM, Ciudad F, Swanston JS: QTL analysis of a cross between European and North American malting barleys reveals a putative candidate gene for (1,3;1,4)-β-glucan content on chromosome 1H. Mol Breed 2007, 19(3):275-284.
23. Powell W, Caligari PDS, Swanston JS, Jinks JL: Genetical investigations into (1,3;1,4)-β-glucan content in barley. Theor Appl Genet 1985, 71(3):461-466.
24. Henry RJ: Genetic and environmental variation in the pentosan and (1,3;1,4)-β-glucan contents of barley and their relation to malting quality. J Cereal Sci 1986, 4:269-277.
25. Kellogg EA: The grasses: A Case Study in Macroevolution. Annu Rev Ecol Syst 2000, 2000(31):217-238.
26. Houston K, McKim SM, Comadran J, Bonar N, Druka I, Uzrek N, Cirillo E, Guzy-Wrobelska J, Collins N, Halpin C, Hansson M, Dockter C, Druka A, Waugh R: Variation in the interaction between alleles of HvAPETALA2 and microRNA172 determines the density of grains on the barley inflorescence. Proc Natl Acad Sci U S A 2013, 110(41):16675-16680.
27. Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal MW, Shaw P, Bayer M, Thomas WT, Marshall D, Hedley P, Tondelli A, Pecchioni N, Francia E, Korzun V, Walther A, Waugh R: Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 2012, 44:1388-1392.
28. Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WT, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, Hayes PM, Lundqvist U, Franckowiak JD, Close TJ, Muehlbauer GJ, Waugh R: INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 2011, 43:169-172.
29. Cory AT, Baga M, Anyia A, Rossnagel BG, Chibbar RN: Genetic markers for ClsF6 gene associated with (1,3;1,4)-β-glucan concentration in barley grain. J Cereal Sci 2012, 56(2):332-339.
30. Taketa S, Yuo T, Tonooka T, Tsumuraya Y, Inagaki Y, Haruyama N, Larroque O, Jobling SA: Functional characterization of barley betaglucanless mutants demonstrates a unique role for CslF6 in (1,3;1,4)-(beta)-D-glucan biosynthesis. J Exp Bot 2012, 63:381-392.
31. IBSC: A physical genetic and functional sequence assembly of the barley genome. Nature 2012, 491(7426):711-716.
32. Schober MS, Burton RA, Shirley NJ, Jacobs AK, Fincher GB: Analysis of the (1,3)-b-D-glucan synthase gene family of barley. Phytochemistry 2009, 70:713-720.
33. Mohammadi M, Endelman JB, Nair S, Chao S, Jones SS, Muehlbauer GJ, Ullrich SE, Baik BK, Wise ML, Smith KP: Association mapping of grain hardness, polyphenol oxidase, total phenolics, amylose content, and β-glucan in US barley breeding germplasm. Mol Breeding. doi:10.1007/s11032-014-0112-5.
34. Burton RA, Jobling SA, Harvey AJ, Shirley NJ, Mather DE, Bacic A, Fincher GB: The Genetics and Transcriptional Profiles of the Cellulose Synthase-Like HvCslF Gene Family in Barley. Plant Physiol 2008, 146:1821-1833.
35. Li J, Baga M, Rossnagel BG, Legge WG, Chibbar RN: Identification of quantitative trait loci for (1,3;1,4)-β-glucan concentration in barley grain. J Cereal Sci 2008, 48(3):647-655.
36. Szucs P, Blake VC, Bhat PR, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay LV, Waugh R, Hayes PM: An Integrated Resource for Barley Linkage Map and Malting Quality QTL Alignment. Plant Gen 2009, 2:134-140.
37. Hirschhorn JN, Daly MJD: Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 2005, 6:95-108.
38. Mackay I, Powell W: Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 2007, 12(2):57-63.
39. Waugh R, Jannink JL, Muehlbauer GJ, Ramsay L: The emergence of whole genome association scans in barley. Curr Opin Plant Biol 2009, 12(2):218-222.
40. Islamovic E, Obert DE, Oliver RE, Harrison SA, Ibrahim A, Marshall JM, Miclaus KJ Hu G, Jackson EW: Genetic dissection of grain beta-glucan and amylose content in barley (Hordeum vulgare L.). Mol Breeding 2013, 31:15-25.
41. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP: A membrane associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 1995, 92:9353-9357.
42. Buckeridge MS, Vergara CE, Carpita NC: Mechanism of synthesis of a cereal mixed-linkage (1-3;1-4)-β-d-glucan: evidence for multiple sites of glucosyl transfer in the synthase complex. Plant Physiol 1999, 120:1105-1116.
43. Urbanowicz BR, Rayon C, Carpita NC: Topology of the Maize Mixed Linkage (1-3;1-4)-β-D Glucan Synthase at the Golgi Membrane. Plant Physiol 2004, 134(2):758-768.
44. Oziel A, Hayes PM, Chen FQ, Jones B: Application of quantitative trait locus mapping to the development of winter-habit malting barley. Plant Breeding 1996, 115:43-51.
45. Panozzo JH, Eckermann PJ, Mather DE, Moody DB, Black CK, Collins HM, Barr AR, Lim P, Cullis BR: QTL analysis of malting quality traits in two barley populations. Aust J Agric Res 2007, 58:858-866.
46. Hu G, Burton C, Hong Z, Jackson E: A mutation of the cellulose-synthaselike (CslF6) gene in barley (Hordeum vulgare L.) partially affects the β-glucan content in grains. J Cereal Sci 2014. doi:10.1016/j.jcs.2013.12.009.
47. Mezaka I, Bleidere M, Legzdina L, Rostoks N: Whole genome association mapping identifies naked grain locus NUD as determinant of (1,3;1,4)-β-glucan content in barley. Žemdirbyste-Agriculture 2011, 98(3):283-292.
48. 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, Szucs 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: Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 2009, 10:582.
49. Chutimanitsakun Y, Cuesta-Marcos A, Chao S, Corey A, Filichkin T, Fisk S, Kolding M, Meints B, Ong Y-L, Rey JI, Ross AS, Hayes PM: Application of marker-assisted selection and genome-wide association scanning to the development of winter food barley germplasm resources. Plant Breeding 2013, 132(6):563-570.
50. Oscarsson M, Andersson R, Salomonsson AC, Aman P: Chemical composition of barley samples focusing on dietary fiber components. J Cereal Sci 1996, 24:161-169.
51. Luchsinger WW, Chen SC: The mechanism of action of malt β-glucanases: VI. Hydrolysis of barley β-d-glucan by endo-β-glucanases from germinated barley. Arch Biochem Biophys 1964, 106:71-77.
52. Hrmova M, Banik M, Harvey AJ, Garrett T, Varghese J, Høj P, Fincher GB: Polysaccharide hydrolases in germinated barley and their role in the depolymerization of plant and fungal cell walls. Int J Biol Macromol 1997, 21(1-2):67-72.
53. Hrmova M, Farkas V, Lahnstein J, Fincher GB: A barley xyloglucan xyloglucosyl transferase covalently links xyloglucan, cellulosic substrates, and (1,3;1,4)-β-D-glucans. J Biol Chem 2007, 282(17):12951-12962.
54. Fincher GB: Exploring the evolution of (1,3;1,4)-b-D-glucans in plant cell walls: comparative genomics can help! Curr Opin Plant Biol 2009, 12:140-147.
55. Woodward JR, Fincher GB: Purification and chemical properties of two 1,3;1,4-beta-glucan endohydrolases from germinating barley. Eur J Biochem 1982, 121:663.
56. Henrissat B: A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 1991, 280:309-316.
57. Szyjanowicz PM, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR: The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 2004, 37:730-740.
58. Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB: Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 2006, 4:145-167.
59. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B: The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
60. Wang J, Xu P, Fincher GB: Purification, characterization and gene structure of (1→3)-β-glucanase isoenzyme GIII from barley (Hordeum vulgare). Eur J Biochem 1992, 209:103-109.
61. Baumann MJ, Eklöf JM, Michel G, Kallas AM, Teeri TT, Czjzek M, Brumer H 3rd: Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. Plant Cell 2007, 19:1947-1963.
62. Burton RA, Gidley MJ, Fincher GB: Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 2010, 6:724-732.
63. Hrmova M, Fincher GB: Dissecting the catalytic mechanism of a plant β-d-glucan glucohydrolase through structural biology using inhibitors and substrate analogues. Carbohydr Res 2007, 342(12-13):1613-1623.
64. Stone BA, Jacobs AK, Hrmova M, Burton RA, Fincher GB: The Biosynthesis of Plant Cell Wall and Related Polysaccharides by Enzymes of the GT2 and GT48 Families. Annual Plant Reviews 2011, 41:109-166.
65. Bertholdsson NO: Characterization of malting barley cultivars with more or less stable grain protein content under varying environmental conditions. Eur J Agron 1999, 10:1-8.
66. Coventry SJ, Barr AR, Eglinton JK, McDonald GK: The determinants and genome locations influencing grain weight and size in barley (Hordeum vulgare L.). Aust J Agr Res 2003, 54(12):1103-1115.
67. Hayes PM, Castro A, Marquez-Cedillo L, Corey A, Henson C, Jones BL, Kling D, Mather D, Matus I, Rossi C, Sato K: Genetic diversity for quantitatively inherited agronomic and malting quality traits. In Diversity in barley. Edited by Von Bothmer R, et al. Amsterdam: Elsevier Science Publishers; 2003.
68. Pauly M, Keegstra K: Plant cell walls as precursors for biofuels. Curr Opin Plant Biol 2010, 13(3):305-312.
69. Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
70. Dabney A, Storey JD, Warnes GR: qvalue: Q-value estimation for false discovery rate control. 2010. R package version 1.38.0.
71. Mayer KF, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Dolezel J, Waugh R, Stein N: Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 2011, 23:1249-1263.
72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood Evolutionary Distance and Maximum Parsimony Methods. Mol Biol Evol 2011, 28(10):2731-2739.
73. Criscuolo A, Gribaldo S: BMGE (Block Mapping and Gathering with Entropy): selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010, 10:210.
74. Milne I, Lindner D, Bayer M, Husmeier D, McGuire G, Marshall DF, Wright F: TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 2008, 25:126-127.