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Low molecular weight glutenin subunit gene composition at Glu-D3 loci of Aegilops tauschii and common wheat and a further view of wheat evolution

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A comprehensive comparison of LMW-GS genes between Ae. tauschii and its progeny common wheat.

Abstract

Low molecular weight glutenin subunits (LMW-GSs) are determinant of wheat flour processing quality. However, the LMW-GS gene composition in Aegilops tauschii, the wheat D genome progenitor, has not been comprehensively elucidated and the impact of allohexaploidization on the Glu-D3 locus remains elusive. In this work, using the LMW-GS gene molecular marker system and the full-length gene-cloning method, LMW-GS genes at the Glu-D3 loci of 218 Ae. tauschii and 173 common wheat (Triticum aestivum L.) were characterized. Each Ae. tauschii contained 11 LMW-GS genes, and the whole collection was divided into 25 haplotypes (AeH01–AeH25). The Glu-D3 locus in common wheat lacked the LMW-GS genes D3-417, D3-507 and D3-552, but shared eight genes of identical open reading frame (ORF) sequences when compared to that of Ae. tauschii. Therefore, the allohexaploidization induces deletions, but exerts no influence on LMW-GS gene coding sequences at the Glu-D3 locus. 92.17% Ae. tauschii had 7-9 LMW-GSs, more than the six subunits in common wheat. The haplotypes AeH16, AeH20 and AeH23 of Ae. tauschii ssp. strangulate distributed in southeastern Caspian Iran were the main putative D genome donor of common wheat. These results facilitate the utilization of the Ae. tauschii glutenin gene resources and the understanding of wheat evolution.

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References

  • Aghaei MJ, Mozafari J, Taleei AR, Naghavi MR, Omidi M (2008) Distribution and diversity of Aegilops tauschii in Iran. Genet Resour Crop Evol 55:341–349

    Article  Google Scholar 

  • Arora S, Singh N, Kaur S, Bains NS, Uauy C, Poland J, Chhuneja P (2017) Genome-wide association study of grain architecture in wild wheat Aegilops tauschii. Front Plant Sci 8:886

    Article  Google Scholar 

  • Caldwell KS, Dvorak J, Lagudah ES, Akhunov E, Luo MC, Wolters P, Powell W (2004) Sequence polymorphism in polyploid wheat and their D-genome diploid ancestor. Genetics 167:941–947

    Article  CAS  Google Scholar 

  • Dong LL, Zhang XF, Liu DC, Fan HJ, Sun JZ, Zhang ZJ, Qin HJ, Li B, Hao ST, Li ZS, Wang DW, Zhang AM, Ling HQ (2010) New insights into the organization, recombination, expression and functional mechanism of low molecular weight glutenin subunit genes in bread wheat. PLoS ONE 5:e13548

    Article  Google Scholar 

  • Dong ZY, Yang YS, Li YW, Zhang KP, Lou HJ, An XL, Dong LL, Gu YQ, Anderson OD, Liu X, Qin HJ, Wang DW (2013) Haplotype variation of Glu-D1 locus and the origin of Glu-D1d allele conferring superior end-use qualities in common wheat. PLoS ONE 8:e74859

    Article  CAS  Google Scholar 

  • D’Ovidio R, Masci S (2004) The low-molecular-weight glutenin subunits of wheat gluten. J Cereal Sci 39:321–339

    Article  Google Scholar 

  • Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866

    Article  CAS  Google Scholar 

  • Dudnikov AJ (1998) Allozyme variation in Transcaucasian populations of Aegilops squarrosa. Heredity 80:248–258

    Article  Google Scholar 

  • Dudnikov AJ (2000) Multivariate analysis of genetic variation in Aegilops tauschii from the world germplasm collection. Genet Resour Crop Evol 47:185–190

    Article  Google Scholar 

  • Dudnikov AJ (2012) Spatial patterns of adenylate kinase, catalase, endopeptidase and fructose-1,6-diphosphatase encoding genes allelic variation in Aegilops tauschii Coss. Genet Resour Crop Evol 59:1–8

    Article  CAS  Google Scholar 

  • Dvorak J, Luo MC, Yang ZL, Zhang HB (1998) The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor Appl Genet 97:657–670

    Article  CAS  Google Scholar 

  • Dvorak J, Deal KR, Luo MC, You FM, von Borstel K, Dehghani H (2012) The origin of spelt and free-threshing hexaploid wheat. J Hered 103:426–441

    Article  CAS  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279

    Article  CAS  Google Scholar 

  • Giles RJ, Brown TA (2006) GluDy allele variations in Aegilops tauschii and Triticum aestivum: implications for the origins of hexaploid wheats. Theor Appl Genet 112:1563–1572

    Article  CAS  Google Scholar 

  • Hammer K (1980) Vorarbeiten zur monographischen Darstellung von Wildpflanzensortimenten: Aegilops L. Kulturpflanze 28:33–180

    Article  Google Scholar 

  • Hudson RR (2002) Generating samples under a Wright–Fisher neutral model of genetic variation. Bioinformatics 18:337–338

    Article  CAS  Google Scholar 

  • Jaaska V (1980) Electrophoretic survey of seedling esterases in wheats in relation to their phylogeny. Theor Appl Genet 56:273–284

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  Google Scholar 

  • Lagudah ES, Appels R, Brown AHD, Mcneil D (1991) The molecular-genetic analysis of Triticum tauschii, the D-Genome donor to hexaploid wheat. Genome 34:375–386

    Article  CAS  Google Scholar 

  • Lew EJ-L, Kuzmicky D, Kasarda DD (1992) Characterization of low molecular weight glutenin subunits by reversed-phase high-performance liquid chromatography, sodium dodecyl sulfate-polyacrylamide gel electrophoresis, and N-terminal amino acid sequencing. Cereal Chem 69:508–515

    CAS  Google Scholar 

  • Li AL, Liu DC, Wu J, Zhao XB, Hao M, Geng SF, Yan J, Jiang XX, Zhang LQ, Wu JY, Yin LJ, Zhang RZ, Wu L, Zheng YL, Mao L (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26:1878–1900

    Article  CAS  Google Scholar 

  • Lubbers EL, Gill KS, Cox TS, Gill BS (1991) Variation of molecular markers among geographically diverse accessions of Triticum tauschii. Genome 34:354–361

    Article  Google Scholar 

  • Luo GB, Zhang XF, Zhang YL, Yang WL, Li YW, Sun JZ, Zhan KH, Zhang AM, Liu DC (2015) Composition, variation, expression and evolution of low-molecular-weight glutenin subunit genes in Triticum urartu. BMC Plant Biol 15:68

    Article  Google Scholar 

  • Matsuoka Y, Takumi S, Kawahara T (2008) Flowering time diversification and dispersal in central Eurasian wild wheat Aegilops tauschii Coss.: genealogical and ecological framework. PLoS ONE 3:e3138

    Article  Google Scholar 

  • Matsuoka Y, Nishioka E, Kawahara T, Takumi S (2009) Genealogical analysis of subspecies divergence and spikelet-shape diversification in central Eurasian wild wheat Aegilops tauschii Coss. Plant Syst Evol 279:233–244

    Article  Google Scholar 

  • Miranda LM, Murphy JP, Marshall D, Leath S (2006) Pm34: a new powdery mildew resistance gene transferred from Aegilops tauschii Coss. to common wheat (Triticum aestivum L.). Theor Appl Genet 113:1497–1504

    Article  CAS  Google Scholar 

  • Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol 19:999–1013

    Article  Google Scholar 

  • Nakai Y (1979) Isozyme variations in Aegilops and Triticum, IV. The origin of the common wheats revealed from the study on esterase isozymes in synthesized hexaploid wheats. Jpn J Genet 54:175–189

    Article  Google Scholar 

  • Olson EL, Rouse MN, Pumphrey MO, Bowden RL, Gill BS, Poland JA (2013) Introgression of stem rust resistance genes SrTA10187 and SrTA10171 from Aegilops tauschii to wheat. Theor Appl Genet 126:2477–2484

    Article  CAS  Google Scholar 

  • Peng JH, Sun DF, Nevo E (2011) Domestication evolution, genetics and genomics in wheat. Mol Breed 28:281–301

    Article  CAS  Google Scholar 

  • Pestsova E, Ganal MW, Roder MS (2000) Isolation and mapping of microsatellite markers specific for the D genome of bread wheat. Genome 43:689–697

    Article  CAS  Google Scholar 

  • Saeidi H, Rahiminejad MR, Vallian S, Heslop-Harrison JS (2006) Biodiversity of diploid D-genome Aegilops tauschii Coss. in Iran measured using microsatellites. Genet Resour Crop Evol 53:1477–1484

    Article  Google Scholar 

  • Saeidi H, Rahiminejad MR, Heslop-Harrison JS (2008) Retroelement insertional polymorphisms, diversity and phylogeography within diploid, D-genome Aegilops tauschii (Triticeae, poaceae) sub-taxa in Iran. Ann Bot 101:855–861

    Article  CAS  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the Near East. Nat Rev Genet 3:429–441

    Article  CAS  Google Scholar 

  • Shewry PR (2009) Wheat. J Exp Bot 60:1537–1553

    Article  CAS  Google Scholar 

  • Shewry PR, Tatham AS, Barro F, Barcelo P, Lazzeri P (1995) Biotechnology of breadmaking: unraveling and manipulating the multi-protein gluten complex. Biotechnology 13:1185–1190

    CAS  Google Scholar 

  • Shewry PR, Halford NG, Belton PS, Tatham AS (2002) The structure and properties of gluten: an elastic protein from wheat grain. Philos Trans R Soc Lond Ser B Biol Sci 357:133–142

    Article  CAS  Google Scholar 

  • Singh M, Chabane K, Valkoun J, Blake T (2006) Optimum sample size for estimating gene diversity in wild wheat using AFLP markers. Genet Resour Crop Evol 53:23–33

    Article  CAS  Google Scholar 

  • Sohail Q, Shehzad T, Kilian A, Eltayeb AE, Tanaka H, Tsujimoto H (2012) Development of diversity array technology (DArT) markers for assessment of population structure and diversity in Aegilops tauschii. Breed Sci 62:38–45

    Article  CAS  Google Scholar 

  • Takumi S, Nishioka E, Morihiro H, Kawahara T, Matsuoka Y (2009) Natural variation of morphological traits in wild wheat progenitor Aegilops tauschii Coss. Breed Sci 59:579–588

    Article  Google Scholar 

  • Talbert LE, Smith LY, Blake MK (1998) More than one origin of hexaploid wheat is indicated by sequence comparison of low-copy DNA. Genome 41:402–407

    Article  CAS  Google Scholar 

  • Trethowan RM, Mujeeb-Kazi A (2008) Novel germplasm resources for improving environmental stress tolerance of hexaploid wheat. Crop Sci 48:1255–1265

    Article  Google Scholar 

  • Van Slageren MW (1994) Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach): Eig (Poaceae). Wageningen Agricultural University Papers 94-7. Wageningen and Aleppo

  • Watanabe N, Fujii Y, Takesada N, Martinek P (2006) Cytological and microsatellite mapping of the gene for brittle rachis in a Triticum aestivum-aegilops tauschii introgression line. Euphytica 151:63–69

    Article  Google Scholar 

  • Zhang XF, Liu DC, Yang WL, Liu KF, Sun JZ, Guo XL, Li YW, Wang DW, Ling HQ, Zhang AM (2011a) Development of a new marker system for identifying the complex members of the low-molecular-weight glutenin subunit gene family in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:1503–1516

    Article  CAS  Google Scholar 

  • Zhang XF, Liu DC, Jiang W, Guo XL, Yang WL, Sun JZ, Ling HQ, Zhang AM (2011b) PCR-based isolation and identification of full-length low-molecular-weight glutenin subunit genes in bread wheat (Triticum aestivum L.). Theor Appl Genet 123:1293–1305

    Article  CAS  Google Scholar 

  • Zhang XF, Jin H, Zhang Y, Liu DC, Li GY, Xia XC, He ZH, Zhang AM (2012) Composition and functional analysis of low-molecular-weight glutenin alleles with Aroona near-isogenic lines of bread wheat. BMC Plant Biol 12:243

    Article  CAS  Google Scholar 

  • Zhang HK, Bian Y, Gou XW, Zhu B, Xu CM, Qi B, Li N, Rustgi S, Zhou H, Han FP, Jiang JM, von Wettstein D, Liu B (2013a) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proc Natl Acad Sci USA 110:3447–3452

    Article  CAS  Google Scholar 

  • Zhang XF, Liu DC, Zhang JH, Jiang W, Luo GB, Yang WL, Sun JZ, Tong YP, Cui DQ, Zhang AM (2013b) Novel insights into the composition, variation, organization, and expression of the low-molecular-weight glutenin subunit gene family in common wheat. J Exp Bot 64:2027–2040

    Article  CAS  Google Scholar 

  • Zhao N, Zhu B, Li MJ, Wang L, Xu LY, Zhang HK, Zheng SS, Qi B, Han FP, Liu B (2011) Extensive and heritable epigenetic remodeling and genetic stability accompany allohexaploidization of wheat. Genetics 188:499-U450

    Article  Google Scholar 

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Acknowledgements

The authors declare no competing financial interests. We thank Dr. Xiaofei Zhang (North Carolina State University) for critical review. And we thank May, David B Iii and Schneider, Matthew G from University of Florida for their scientific English editing. This work was supported by the Ministry of Science and Technology of China (2014CB138101), the National Natural Science Foundation of China (31371610) and the National Transgenic Research Projects (2016ZX08009-003-004).

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Author notes

  1. Lisha Shen, Guangbin Luo and Yanhong Song have contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Plant Cell and Chromosome Engineering, National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 1 West Beichen Road, Chaoyang District, Beijing, 100101, China

    Lisha Shen, Guangbin Luo, Yanhong Song, Shuyi Song, Yiwen Li, Wenlong Yang, Xin Li, Jiazhu Sun, Dongcheng Liu & Aimin Zhang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Lisha Shen

  3. College of Agronomy, The Collaborative Innovation Center of Grain Crops in Henan, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, China

    Yanhong Song & Shuyi Song

  4. Agronomy Department, University of Florida, Gainesville, FL, 32611, USA

    Guangbin Luo

  5. Biology and Agriculture Research Center, School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing, 100024, China

    Dongcheng Liu

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  1. Lisha Shen
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Correspondence to Dongcheng Liu or Aimin Zhang.

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Communicated by Andreas Graner.

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Shen, L., Luo, G., Song, Y. et al. Low molecular weight glutenin subunit gene composition at Glu-D3 loci of Aegilops tauschii and common wheat and a further view of wheat evolution. Theor Appl Genet 131, 2745–2763 (2018). https://doi.org/10.1007/s00122-018-3188-1

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