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Molecular characterization and sequence diversity of genes encoding the large subunit of the ADP-glucose pyrophosphorylase in wheat (Triticum aestivum L.)

  • Plant Genetics • Original Paper
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Abstract

The large subunit of ADP glucose pyrophosphorylase (AGPase), the rate limiting enzyme in starch biosynthesis in Triticum aestivum L., is encoded by the ADP glucose pyrophosphorylase large subunit (AGP-L) gene. This was the first report on the development of three genome-specific primer sets for isolating the complete genomic sequence of all three homoeologous AGP-L genes on group 1 chromosomes. All three AGP-L genes consisted of 15 introns and 15 exons. The lengths of the structural genes from start to stop codon were 3334 bp for AGP-L-A1, 3351 bp for AGP-L-B1, and 3340 bp for AGP-L-D1. The coding region was 1569 bases long in all three genomes. All three AGP-L genes encoded 522 amino acid residues including the transit peptide sequences with 62 amino acid residues and the mature protein with 460 amino acid residues. The mature protein of three AGP-L genes was highly conserved. Three AGP-L genes were sequenced in 47 diverse spring and winter wheat genotypes. One and two haplotypes were found for AGP-L-D1 and AGP-L-A1, respectively. In total, 67 SNPs (single nucleotide polymorphisms) and 13 indels (insertions or deletions) forming five haplotypes were identified for AGP-L-B1. All 13 indels and 58 of the 67 SNPs among the 47 genotypes were located in the non-coding regions, while the remaining nine SNPs were synonymous substitutions in the coding region. Significant LD was found among the 45 SNPs and ten indels located from intron 2 to intron 3. Association analysis indicated that four SNPs were strongly associated with seed number per spike and thousand kernel weight.

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References

  • Ainsworth C, Hosein F, Tarvis M, Weir F, Burrell M, Devos KM, Gale MD (1995) Adenosine diphosphate glucose pyrophosphorylase genes in wheat: differential expression and gene mapping. Planta 197:1–10

    Article  PubMed  CAS  Google Scholar 

  • Beckles DM, Smith AM, Rees T (2001) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol 125:818–827

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Blake NK, Lehfeldt BR, Lavin M, Talbert LE (1999) Phylogenetic reconstruction based on low copy DNA sequence analysis in an allopolyploid: the B genome of wheat. Genome 42:351–360

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Article  PubMed  CAS  Google Scholar 

  • Bryan GJ, Stephenson P, Collins A, Kirby J, Smith JB, Gale MD (1999) Low levels of DNA sequence variation among adapted genotypes of hexaploid wheat. Theor Appl Genet 99:192–198

    Article  CAS  Google Scholar 

  • Burton RA, Johnson PE, Beckles DM, Fincher GB, Jenner JL, Naldrett MJ, Denyer K (2002) Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiol 130:1464–1475

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  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 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hammond-Kosack MCU, Holsworth MJ, Bevan MW (1993) In vivo footprinting of a low molecular weight glutenin gene (LMWG-1D1) in wheat endosperm. EMBO J 12:545–554

    PubMed  CAS  PubMed Central  Google Scholar 

  • Hannah LC (1997) Starch synthesis in the maize seed. In: Larkins BA, Vasil IK (eds) Cellular and molecular biology of plant seed development. Kluwer, Dordrecht, pp 375–405

  • Helguera M, Vanzetti L, Soria M, Khan IA, Kolmer J, Dubcovsky J (2005) PCR markers for Triticum speltoides leaf rust resistance gene Lr51 and their use to develop isogenic hard red spring wheat lines. Crop Sci 45:728–734

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang XQ, Brûlé-Babel A (2012) Sequence diversity, haplotype analysis, association mapping and functional marker development in the waxy and starch synthase II genes for grain yield-related traits in hexaploid wheat (Triticum aestivum L.). Mol Breed 30:627–645

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang XQ, Cloutier S (2008) Molecular characterization and genomic organization of low molecular weight glutenin subunit genes at the Glu-3 loci in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 116:953–966

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222

    Article  PubMed  CAS  Google Scholar 

  • Jauhar PP (2007) Genetic enhancement of polyploidy crops. In: Kang MS Priyadarshan PM (ed) Breeding major food staples. Blackwell, Iowa, pp 41–60

  • Jiang D, Cao W, Dai T, Jing Q (2003) Activities of key enzymes for starch synthesis in relation to growth of superior and inferior grains on winter wheat (Triticum aestivum L.) spike. Plant Growth Regul 41:247–257

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Manicacci D, Falque M, Le Guillou S, Piegu B, Henry AM, Le Guilloux M, Damerval C, De Vienne D (2007) Maize Sh2 gene is constrained by natural selection but escaped domestication. J Evol Biol 20:503–516

    Article  PubMed  CAS  Google Scholar 

  • Muller M, Knudsen S (1993) The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box. Plant J 4:345–355

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press

  • Rose AB (2008) Intron-mediated regulation of gene expression. Curr Top Microbiol Immunol 326:277–290

    PubMed  CAS  Google Scholar 

  • Sakulsingharoj C, Choi SB, Hwang SK, Edwards GE, Bork J, Meyer CR, Preiss J, Okita TW (2004) Engineering starch biosynthesis for increasing rive seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase. Plant Sci 167:1323–1333

    Article  CAS  Google Scholar 

  • Slafer GA, Araus JL, Richards RA (1999) Physiological traits that increase the yield potential of wheat. In: Satorre EH, Slafer GA (eds) Wheat ecology and physiology of yield determination. Food Products Press, New York, pp 379–401

  • Smidansky ED, Martin JM, Hannah LC, Fischer AM, Giroux MJ (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216:656–664

    PubMed  CAS  Google Scholar 

  • Smidansky E, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ (2002) Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Natl Acad Sci U S A 99:1724–1729

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Somers DJ, Kirkpatrick R, Moniwa M, Walsh A (2003) Mining single-nucleotide polymorphisms from hexaploid wheat ESTs. Genome 49:431–437

    Article  Google Scholar 

  • Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM (1992) Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science 258:287–292

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4 - molecular evolutionary genetics analysis software v4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thorneycroft D, Hosein F, Thangavelu M, Clark J, Vizir I, Burrell MM, Ainsworth C (2003) Characterization of a gene from chromosome 1B encoding the large subunit of ADPglucose pyrophosphorylase from wheat: evolutionary divergence and differential expression of Agp2genes between leaves and developing endosperm. Plant Biotechnol J 1:259–270

    Article  PubMed  CAS  Google Scholar 

  • Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci U S A 99:12959–12962

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wilkie GS, Kickson KS, Gray NK (2003) Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28:182–188

    Article  PubMed  CAS  Google Scholar 

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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.

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Author notes

  1. Meghan K. Rose

    Present address: Manitoba Agriculture, Food and Rural Development, Box 370 Swan River, Manitoba, R0L 1Z0, Canada

  2. Xiu-Qiang Huang

    Present address: Pioneer Hi-Bred Production LP, 12111 Mississauga Road, Caledon, Ontario, L7C 1X1, Canada

Authors and Affiliations

  1. Department of Plant Science, University of Manitoba, 66 Dafoe Road, Winnipeg, Manitoba, R3T 2N2, Canada

    Meghan K. Rose, Xiu-Qiang Huang & Anita Brûlé-Babel

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  1. Meghan K. Rose
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Correspondence to Xiu-Qiang Huang or Anita Brûlé-Babel.

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Communicated by: Andrzej Górny

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Rose, M.K., Huang, XQ. & Brûlé-Babel, A. Molecular characterization and sequence diversity of genes encoding the large subunit of the ADP-glucose pyrophosphorylase in wheat (Triticum aestivum L.). J Appl Genetics 57, 15–25 (2016). https://doi.org/10.1007/s13353-015-0298-1

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