Abstract
To characterize the structure and expression of a large multigene family of α/β-gliadin genes, 90 individual α/β-gliadin genes harboring a promoter region were identified in the wheat cultivar Chinese Spring. These genes were classified into eleven groups by phylogenetic analysis, and the chromosomes they were derived from were determined. Of these genes, 50 had the basic α/β-gliadin domains and six conserved cysteine residues and 16, 16 and 18 of them were, respectively, located on chromosome 6A, 6B and 6D. Six genes had an additional cysteine residue, suggesting that these α/β-gliadins acquired the property of binding other proteins through intermolecular disulphide bands. Expression of α/β-gliadin genes in developing seeds was measured by quantitative RT-PCR using group-specific primers over 3 years. Expression patterns of these genes on the basis of accumulated temperature were similar among gene groups, whereas expression levels differed for the 3 years. The expression of most α/β-gliadin and other prolamin genes was correlated with the sunshine duration. On the other hand, although all α/β-gliadin genes had a common E-box within the −300 promoter region, some genes showed a particular expression pattern with respect to the sunshine duration, similarly to gene encoding high-molecular weight glutenin subunits and endosperm enzymes. These observations suggested that expression of each α/β-gliadin gene is differentially regulated by multiple regulatory factors.
Similar content being viewed by others
References
Altenbach SB, Kothari KM (2007) Omega gliadin genes expressed in Triticum aestivum cv. Butte 86: effects of post-anthesis fertilizer on transcript accumulation during grain development. J Cereal Sci 46:169–177
Anderson OD, Greene FC (1997) The α-gliadin gene family. ΙΙ. DNA and protein sequence variation, subfamily structure, and origins of pseudogenes. Theor Appl Genet 95:59–65
Anderson OD, Dong L, Huo N, Gu YQ (2012) A new class of wheat gliadin genes and proteins. PLoS One 7:e52139
Dickinson CD, Evans PR, Nielsen NC (1988) RY repeats are conserved in the 5′-flanking regions of legume seed-protein genes. Nucl Acid Res 16:371
Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J Cereal Sci 38:133–146
Dupont FM, Hurkman WJ, Vensel WH, Tanaka C, Kothari KM, Chung OK, Altenbach SB (2006) Protein accumulation and composition in wheat grain: effects of mineral nutrients and high temperature. Eur J Agron 25:96–107
Grierson C, Du JS, Zabala MT, Beggs K, Smith C, Holdsworth M, Bevan M (1994) Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant J 5:815–826
Gu YQ, Crossman C, Kong X, Luo M, You FM, Coleman-Derr D, Dubcovsky J, Anderson OD (2004) Genomic organization of the complex α-gliadin gene loci in wheat. Theor Appl Genet 109:648–657
Hammond-Kosack M, Holdsworth M, Bevan M (1993) In vivo foot-printing of a low molecular weight glutenin gene (LMWG-1D1) in wheat endosperm. EMBO J 12:545–554
International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788
Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and β-amylase from sweet potato. Mol Genet Genom 244:563–571
Jackson EA, Holt LM, Payne PI (1983) Characterization of high molecular weight gliadin and low-molecular-weight glutenin subunits of wheat endosperm by two-dimensional electrophoresis and the chromosomal localization of their controlling genes. Theor Appl Genet 66:29–37
Kasarda DD (1989) Glutenin structure in relation to wheat quality. In: Pomeranz Y (ed) Wheat is Unique. American Association of Cereal Chemists, Minnesota, pp 277–302
Kawaura K, Mochida K, Ogihara Y (2005) Expression profile of two storage-protein gene families in hexaploid wheat revealed by large-scale analysis of expressed sequence tags. Plant Physiol 139:1870–1880
Kawaura K, Wu J, Matsumoto T, Kanamori H, Katagiri S, Ogihara Y (2012) Genome change in wheat observed through the structure and expression of α/β-gliadin genes. Funct Integ Genom 12:341–355
Maeo K, Tomiya T, Hayashi K, Akaike M, Morikami A, Ishiguro S, Nakamura K (2001) Sugar-responsible elements in the promoter of a gene for β-amylase of sweet potato. Plant Mol Biol 46:627–637
Muccilli V, Cunsolo V, Saletti R, Foti S, Masci S, Lafiandra D (2005) Characterization of B- and C-type low molecular weight glutenin subunits by electrospray ionization mass spectrometry and matrix-assisted laser desorption/ionization mass spectrometry. Proteomics 5:719–728
Müller S, Wieser H (1995) The location of disulphide bonds in α-type gliadins. J Cereal Sci 22:21–27
Okita TW, Cheesbrough V, Reeves CD (1985) Evolution and heterogeneity of the α-/β-type and γ-type gliadin DNA sequences. J Biol Chem 260:8203–8213
Pan J, Zhu W, Dai T, Jiang D (2006) Predicting the protein content of grain in winter wheat with meteorological and genotypic factors. Plant Prod Sci 9:323–333
Payne PI (1987) Genetics of wheat storage proteins and the effect of allelic variation on bread-making quality. Ann Rev Plant Physiol 38:141–153
Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR, Mayer KF, Olsen OA (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:125009
Salentijn EM, Goryunova SV, Bas N, van der Meer IM, van den Broeck HC, Bastien T, Gilissen LJ, Smulders MJ (2009) Tetraploid and hexaploid wheat varieties reveal large differences in expression of alpha-gliadins from homoeologous Gli-2 loci. BMC Genom 10:48
Stephenson TJ, McIntyre CL, Collet C, Xue GP (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65:77–92
Tamura K, Nei M, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729
Tanaka T, Kobayashi F, Joshi GP, Onuki R, Sakai H, Kanamori H, Wu J, Simkova H, Nasuda S, Endo TR, Hayakawa K, Doležel J, Ogihara Y, Itoh T, Matsumoto T, Handa H (2014) Next-generation survey sequencing and the molecular organization of wheat chromosome 6B. DNA Res 21:103–114
Tao HP, Kasarda DD (1989) Two-dimensional gel mapping and N-terminal sequencing of LMW-glutenin subunits. J Exp Bot 40:1015–1020
van Herpen TW, Goryunova SV, van der Schoot J, Mitreva M, Salentijn E, Vorst O, Schenk MF, van Veelen PA, Koning F, van Soest LJ, Vosman B, Bosch D, Hamer RJ, Gilissen LJ, Smulders MJ (2006) Alpha-gliadin genes from the A, B, and D genomes of wheat contain different sets of celiac disease epitopes. BMC Genom 10(7):1
van Herpen TW, Riley M, Sparks C, Jones HD, Gritsch C, Dekking EH, Hamer RJ, Bosch D, Salentijn EM, Smulders MJ, Shewry PR, Gilissen LJ (2008) Detailed Analysis of the Expression of an Alpha-gliadin Promoter and the Deposition of Alpha-gliadin Protein During Wheat Grain Development. Ann Bot 102:331–342
Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci USA 94:7685–7690
Wu CY, Washida H, Onodera Y, Harada K, Takaiwa F (2000) Quantitative nature of the Prolamin-box, AGCT and AACA motifs in rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant J. 23:415–421
Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119:1397–1412
Acknowledgments
This is contribution no. 1024 from the Kihara Institute for Biological Research, Yokohama City University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animal performed by any of the authors.
Additional information
Communicated by S. Hohmann.
S. Noma and K. Kawaura contributed equally to the work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Noma, S., Kawaura, K., Hayakawa, K. et al. Comprehensive molecular characterization of the α/β-gliadin multigene family in hexaploid wheat. Mol Genet Genomics 291, 65–77 (2016). https://doi.org/10.1007/s00438-015-1086-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-015-1086-7