Abstract
Development of high-yielding cereal crops could meet increasing global demands for food, feed and bio-fuels. Wheat is one of the world’s most important cereal crops. The biosynthesis of starch is the major determinant of yield in wheat. Two starch biosynthesis genes, the waxy (Wx) genes and the starch synthase IIa (SSIIa) genes, were amplified and sequenced in 92 diverse wheat genotypes using genome-specific primers. Nucleotide diversity, haplotype analysis and association mapping were performed. The first exon (5′-UTR) and the first intron of the three homoeologous Wx genes were isolated using expressed sequence tag sequences. The Wx genes contained 12 exons separated by 11 introns. SNP (single nucleotide polymorphism) frequency ranged from 1 SNP/3,648 bp for Wx-D1 to 1 SNP/135 bp for SSIIa-A1, with an average of 1 SNP/230 bp. The average SNP frequencies in exon and intron regions were 1 SNP/322 bp and 1 SNP/228 bp, respectively. Thirty, 23 and 5 SNPs were identified and formed five, six and five haplotypes for SSIIa-A1, SSIIa-B1 and SSIIa-D1, respectively. However, no association was found between these SNPs and seven yield-related traits. Twenty-two, 15 and 1 SNPs were detected and formed nine, five and two haplotypes for Wx-A1, Wx-B1 and Wx-D1, respectively. Three unique nucleotides C+A+T at SNP5, SNP6 and SNP12 formed Wx-B1-H3, which was significantly associated with increased grain weight, thousand kernel weight, and total starch content in three spring wheat genotypes and five winter wheat genotypes. Cost-effective and co-dominant SNP markers were developed using temperature-switch (TS)-PCR and are being used for marker-assisted selection of doubled haploid lines with enhanced grain yield and starch content in winter wheat breeding programs.
Similar content being viewed by others
References
Bao JS, Corke H, Sun M (2006) Nucleotide diversity in starch synthase IIa and validation of single nucleotide polymorphisms in relation to starch gelatinization temperature and other physicochemical properties in rice (Oryza sativa L.). Theor Appl Genet 113:1171–1183
Blake NK, Sherman JD, Dvorak J, Talbert LE (2004) Genome specific primer sets for starch biosynthesis genes in wheat. Theor Appl Genet 109:1295–1302
Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder MS, Weber WE (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Cai XL, Wang ZY, Xing YY, Zhang JL, Hong MM (1998) Aberrant splicing of intron 1 leads to the heterogeneous 5’ UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. Plant J 14:459–465
Caldwell KS, Dvorak J, Lagudah ES, Akhunov E, Luo M, Wolters P, Powell W (2004) Sequence polymorphism in polyploidy wheat and their D-genome diploid ancestor. Genetics 167:941–947
Chen MH, Bergman C, Pinson S, Fjellstrom R (2008) Waxy gene haplotypes: associations with apparent amylose content and the effect by the environment in an international rice germplasm collection. J Cereal Sci 47:536–545
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
Emes MJ, Bowsher CG, Hedley C, Burrell MM, Scrase-Field ESF, Tetlow IJ (2003) Starch synthesis and carbon partitioning in developing endosperm. J Exp Bot 54:569–575
Hanashiro I, Itoh K, Kuratomi Y, Yamazaki M, Igarashi T, Matsugasako J, Takeda Y (2008) Granule-bound starch synthase I is responsible for biosynthesis of extra-long unit chains of amylopectin in rice. Plant Cell Physiol 49:925–933
Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, Yan J, Buckler ES (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319:330–333
Haseneyer G, Ravel C, Dardevet M, Balfourier F, Sourdille P, Charmet G, Brunel D, Sauer S, Geiger HH, Graner A, Stracke S (2008) High level of conservation between genes coding for the GAMYB transcription factor in barley (Hordeum vulgare L.) and bread wheat (Triticum aestivum L.) collections. Theor Appl Genet 117:321–331
Hayden MJ, Tabone T, Mather DE (2009) Development and assessment of simple PCR markers for SNP genotyping in barley. Theor Appl Genet 119:939–951
Huang XQ, Brûlé-Babel A (2010) Development of genome-specific primers for homoeologous genes in allopolyploid species: the waxy and starch synthase II genes in allohexaploid wheat (Triticum aestivum L.) as examples. BMC Res Notes 3:140
Huang XQ, Brûlé-Babel A (2011) Development of simple and co-dominant PCR markers to genotype the puroindoline a and b genes for grain hardness in bread wheat (Triticum aestivum L.). J Cereal Sci 53:277–284
Huang XQ, Cloutier S (2007) Hemi-nested touchdown PCR combined with primer-template mismatch PCR for rapid isolation and sequencing of low molecular weight glutenin subunit gene family from a hexaploid wheat BAC library. BMC Genet 8:18
Huang XQ, Zeller FJ, Hsam SLK, Wenzel G, Mohler V (2000) Chromosomal location of AFLP markers in common wheat (Triticum aestivum L.) utilizing nulli-tetrasomic stocks. Genome 43:298–305
Huang XQ, Cöster H, Ganal MW, Röder MS (2003) Advanced backcross QTL analysis for the identification of quantitative trait loci alleles from wild relatives of wheat (Triticum aestivum L.). Theor Appl Genet 106:1379–1389
Huang XQ, Kempf H, Ganal MW, Röder MS (2004) Advanced backcross QTL analysis in progenies derived from a cross between a German elite winter wheat variety and a synthetic wheat (Triticum aestivum L.). Theor Appl Genet 109:933–943
Huang XQ, Cloutier S, Lycar L, Radovanovic N, Humphreys DG, Noll JS, Somers DJ, Brown PD (2006) Molecular detection of QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theor Appl Genet 113:753–766
Isshiki M, Morino K, Nakajima M, Okagaki RJ, Wessler SR, Izawa T, Shimamoto K (1998) A naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 5′ splice site of the first intron. Plant J 15:133–138
James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222
Konik-Rose C, Thistleton J, Chanvrier H, Tan I, Halley P, Gidley M, Kosar-Hashemi B, Wang H, Larroque O, Ikea J, McMaugh S, Regina A, Rahman S, Morell M, Li Z (2007) Effects of starch synthase IIa gene dosage on grain, protein and starch in endosperm of wheat. Theor Appl Genet 115:1053–1065
Li Z, Chu X, Mouille G, Yan L, Kosar-Hashemi B, Hey S, Napier J, Shewry P, Clarke B, Appels R, Morell MK, Rahman S (1999) The localization and expression of the class II starch synthases of wheat. Plant Physiol 120:1147–1156
Li Z, Sun F, Xu S, Chu X, Mukai Y, Yamamoto M, Ali S, Rampling L, Kosar-Hashemi B, Rahman S, Morell MK (2003) The structural organisation of the gene encoding class II starch synthase of wheat and barley and the evolution of the genes encoding starch synthases in plants. Funct Integr Genomics 3:76–85
Matthies IE, Weise S, Röder MS (2009) Association of haplotype diversity in the a-amylase gene amy1 with malting quality parameters in barley. Mol Breed 23:139–152
Murai J, Taira T, Ohta D (1999) Isolation and characterization of the three Waxy genes encoding the granule-bound starch synthase in hexaploid wheat. Gene 234:71–79
Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Mol Gen Genet 248:253–259
Nakamura T, Shimbata T, Vrinten P, Saito M, Yonemar J, Seto Y, Yasuda H, Takahama M (2006) Sweet wheat. Genes Genet Syst 81:361–365
Neumann K, Kobiljski B, Denčić S, Varshney RK, Börner A (2011) Genome-wide association mapping: a case study in bread wheat (Triticum aestivum L.). Mol Breed 27:37–58
Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan MD (2006) Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173:975–983
Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Ral J-P, Colleoni C, Wattebled F, Dauvillée D, Nempont C, Deschamps P, Li Z, Morell MK, Chibbar R, Purton S, d′Hulst C, Ball SG (2006) Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiol 142:305–317
Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour F, Chalhoub B, Brunel D, Beckert M, Charmet G (2006) Single-nucleotide polymorphisms (SNPs) frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139
Rohde W, Becker D, Salamini F (1988) Structural analysis of the Waxy locus from Hordeum vulgare. Nucleic Acids Res 16:7185–7186
Shimbata T, Nakamura T, Vrinten P, Saito M, Yonemaru J, Seto Y, Yasuda H (2005) Mutations in wheat starch synthase II genes and PCR-based selection of a SGP-1 null line. Theor Appl Genet 111:1072–1079
Somers DJ, Kirkpatrick R, Moniwa M, Walsh A (2003) Mining single-nucleotide polymorphisms from hexaploid wheat ESTs. Genome 46:431–437
Tabone T, Mather DE, Hayden MJ (2009) Temperature switch PCR (TSP): robust assay design for reliable amplification and genotyping of SNPs. BMC Genomics 10:580
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Van K, Onoda S, Kim MY, Kim KD, Lee S-H (2008) Allelic variation of the Waxy gene in foxtail millet [Setaria italica (L.) P. Beauv.] by single nucleotide polymorphisms. Mol Genet Genomics 279:255–266
Vrinten PL, Nakamura T, Yamamori M (1999) Molecular characterization of waxy mutations in wheat. Mol Gen Genet 261:463–471
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Wilson LM, Whitt SR, Ibáñez AM, Rocheford TR, Goodman MM, Buckler ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733
Yamamori M, Fujita S, Hayakawa K, Matsuki J (2000) Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose. Theor Appl Genet 101:21–29
Yan H, Jiang H, Pan X, Li M, Chen Y, Wu G (2009) The gene encoding starch synthase IIc exists in maize and wheat. Plant Sci 176:51–57
Yao J, Wang L, Liu L, Zhao C, Zheng Y (2009) Association mapping of agronomic traits on chromosome 2A of wheat. Genetica 137:67–75
Yoo S-H, Jane J (2002) Structural and physical characteristics of waxy and other wheat starches. Carbohydr Polym 49:297–305
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. The Plant Genome 1:5–20
Acknowledgments
We thank Dr. J. Raupp, the Wheat Genetic and Genomic Resources Center (WGGRC), Department of Plant Pathology, Kansas State University, for providing the nulli-tetrasomic lines of Chinese Spring (CS). The seed of wheat genotypes was kindly supplied by Dr. H. Bockelman of the Germplasm Resources Information Network (GRIN), USDA-ARS, USA, D. Kessler of the Plant Gene Resources of Canada (PGRC), Agriculture and Agri-Food Canada, Canada, and Dr. Zdeněk Stehno of Gene Bank, Crop Research Institute, Czech Republic, respectively. This work was supported by NSERC (National Science and Engineering Research Council of Canada) and Husky Energy Inc.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Huang, XQ., Brûlé-Babel, A. Sequence diversity, haplotype analysis, association mapping and functional marker development in the waxy and starch synthase IIa genes for grain-yield-related traits in hexaploid wheat (Triticum aestivum L.). Mol Breeding 30, 627–645 (2012). https://doi.org/10.1007/s11032-011-9649-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-011-9649-8