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The detection of a de novo allele of the Glu-1Dx gene in wheat–rye hybrid offspring

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Abstract

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This study provides a link between a de novo gene and novel phenotype in wheat–rye hybrids that can be used as a model for induced de novo genetic variation.

Abstract

Wide hybridization can produce de novo DNA variation that may cause novel phenotypes. However, there is still a lack of specific links between changed genes and novel phenotypes in wide hybrids. The well-studied high-molecular-weight glutenin subunit (HMW-GS) genes in tribe Triticeae provide a useful model for addressing this issue. In this study, we investigated the feasibility of a wheat–rye hybridization method for inducing de novo phenotypes using the Glu-1Dx2.2 subunit as an example. We developed three hexaploid wheat lines with normal fertility and a Glu-1Dx2.2 variant, named Glu-1Dx2.2 v, derived from three F1 hybrids. The wild-type Glu-1Dx2.2 has two direct repeats of 295 bp length separated by an intervening 101 bp in its central repetitive region. In the mutant Glu-1Dx2.2 v, one copy of the repeats and the intervening sequence were deleted, probably through homology-dependent illegitimate recombination (IR). This study provides a direct link between a de novo allele and novel phenotype. Our results indicate that the wheat–rye method may be a useful tool to induce de novo genetic variations that broaden the genetic diversity for wheat improvement.

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References

  • Arnold MA (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2007) Patterns in grass genome evolution. Curr Opin Plant Biol 10:176–181

    Article  PubMed  CAS  Google Scholar 

  • Chantret N, Salse J, Sabot F, Rahman S, Bellec A, Laubin B, Dubois I, Dossat C, Sourdille P, Joudrier P (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Ann Rev Plant Biol 58:377–406

    Article  CAS  Google Scholar 

  • Contento A, Heslop-Harrison J, Schwarzacher T (2005) Diversity of a major repetitive DNA sequence in diploid and polyploid Triticeae. Cytogenet Genome Res 109:34–42

    Article  PubMed  CAS  Google Scholar 

  • Crouch J, Payne T, Dreisigacker S, Wu H, Braun H (2009) Improved discovery and utilization of new traits for breeding. In: Dixon J, Braum HJ, Kosina P, Crouch J (eds) Wheat facts and futures 2009. CIMMYT, Mexico, pp 42–51

    Google Scholar 

  • Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dvorak J, Akhunov ED, Akhunov AR, Deal KR, Luo MC (2006) Molecular characterization of a diagnostic DNA marker for domesticated tetraploid wheat provides evidence for gene flow from wild tetraploid wheat to hexaploid wheat. Mol Biol Evol 23:1386–1396

    Article  PubMed  CAS  Google Scholar 

  • Feldman M (2001) Origin of cultivated wheat. In: Bonjean AP, Angus WJ (eds) The world wheat book, a history of wheat breeding. Lavoisier Publishing, Paris, pp 3–56

    Google Scholar 

  • Feldman M, Levy AA (2009) Genome evolution in allopolyploid wheat—a revolutionary reprogramming followed by gradual changes. J Genet Genomics 36:511–518

    Article  PubMed  CAS  Google Scholar 

  • Finigan P, Tanurdzic M, Martienssen RA (2012) Origins of novel phenotypic variation in polyploids. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Berlin, pp 57–76

    Chapter  Google Scholar 

  • Fujisawa M, Yamagata H, Kamiya K, Nakamura M, Saji S, Kanamori H, Wu J, Matsumoto T, Sasaki T (2006) Sequence comparison of distal and proximal ribosomal DNA arrays in rice (Oryza sativa L.) chromosome 9S and analysis of their flanking regions. Theor Appl Genet 113:419–428

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Liu SW, Sun Q, Xia GM (2010) High frequency of HMW-GS sequence variation through somatic hybridization between Agropyron elongatum and common wheat. Planta 231:245–250

    Article  PubMed  CAS  Google Scholar 

  • Gupta PK, Priyadarshan PM (1982) Triticale, present status and future prospects. Adv Genet 21:255–345

    Article  Google Scholar 

  • Han F, Liu B, Fedak G, Liu Z (2004) Genomic constitution and variation in five partial amphiploids of wheat—Thinopyrum intermedium as revealed by GISH, multicolor GISH and seed storage protein analysis. Theor Appl Genet 109:1070–1076

    Article  PubMed  CAS  Google Scholar 

  • Hao M, Luo J, Yang M, Zhang L, Yan Z, Yuan Z, Zheng Y, Zhang H, Liu D, Gustafson P (2011) Comparison of homoeologous chromosome pairing between hybrids of wheat genotypes Chinese Spring ph1b and Kaixian-luohanmai with rye. Genome 54:959–964

    Article  PubMed  Google Scholar 

  • Hao M, Luo J, Zhang L, Yuan Z, Yang Y, Wu M, Chen W, Zheng Y, Zhang H, Liu D (2013) Production of hexaploid triticale by a synthetic hexaploid wheat–rye hybrid method. Euphytica 193:347–357

    Article  CAS  Google Scholar 

  • Hawkesford MJ, Araus JL, Park R, Calderini D, Miralles D, Shen T, Zhang J, Parry MA (2013) Prospects of doubling global wheat yields. Food Energy Secur 2:34–48

    Article  Google Scholar 

  • Hu X, Dai S, Pu Z, Liu D, Pu Z, Jiang J, Wei Y, Wu B, Lan X, Zheng Y, Yan Z (2013) Quality of synthetic hexaploid wheat containing null alleles at Glu-A1 and Glu-B1 loci. J Genet 92:241–245

    Article  PubMed  CAS  Google Scholar 

  • Jiang QT, Zhao QZ, Yang Q, Ma J, Zhang XW, Wang CS, Wang XY, Cao X, Lu ZX, Wei YM (2014) Amphidiploids between tetraploid wheat and Aegilops sharonensis Eig exhibit variations in high-molecular-weight glutenin subunits. Genet Resour Crop Evol 61:299–305

    Article  CAS  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hortic 19:13–14

    Google Scholar 

  • Ko JM, Park HM, Cho JH, Suh DY (2004) Alteration of HMW glutenin subunits in wheat lines possessing new 1BL. 1RS translocation. Gene Genomics 26:261–267

    CAS  Google Scholar 

  • Kong XY, Gu YQ, You FM, Dubcovsky J, Anderson OD (2004) Dynamics of the evolution of orthologous and paralogous portions of a complex locus region in two genomes of allopolyploid wheat. Plant Mol Biol 54:55–69

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Wendel JF (2002) Non-mendelian phenomena in allopolyploid genome evolution. Curr Genomics 3:489–505

    Article  CAS  Google Scholar 

  • Liu B, Vega J, Feldman M (1998) Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. II. Changes in low-copy coding DNA sequences. Genome 41:535–542

    Article  PubMed  CAS  Google Scholar 

  • Liu D, Zhang H, Zhang L, Yuan Z, Hao M, Zheng Y (2014) Distant hybridization: a tool for interspecific manipulation of chromosomes. In: Kumar J, Pratap A (eds) Alien gene transfer in crop plants. Springer, New York, pp 25–42

    Chapter  Google Scholar 

  • Luo J, Hao M, Zhang L, Chen J, Zhang L, Yuan Z, Yan Z, Zheng Y, Zhang H, Yen Y (2012) Microsatellite mutation rate during allohexaploidization of newly resynthesized wheat. Int J Mol Sci 13:12533–12543

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ma XF, Gustafson JP (2008) Allopolyploidization-accommodated genomic sequence changes in triticale. Ann Bot 101:825–832

    Article  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  PubMed  CAS  Google Scholar 

  • McFadden E, Sears E (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37:107–116

    Google Scholar 

  • Mestiri I, Chagué V, Tanguy AM, Huneau C, Huteau V, Belcram H, Coriton O, Chalhoub B, Jahier J (2010) Newly synthesized wheat allohexaploids display progenitor—dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol 186:86–101

    Article  PubMed  CAS  Google Scholar 

  • Nakamura H (2001) Genetic diversity of high-molecular-weight glutenin subunit compositions in landraces of hexaploid wheat from Japan. Euphytica 120:227–234

    Article  CAS  Google Scholar 

  • Nakamura H, Fujimaki H (2002) Specific Glu-D1 f allele frequency of Japanese common wheat compared with distribution of Glu-1 alleles in chinese wheat. Cereal Chem 79:486–490

    Article  CAS  Google Scholar 

  • Ozkan H, Levy AA, Feldman M (2001) Allopolyploidy-induced rapid genome evolution in the wheat (AegilopsTriticum) group. Plant Cell 13:1735–1747

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Qi L, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res 15:3–19

    Article  PubMed  CAS  Google Scholar 

  • Ramanna MS, Jacobsen E (2003) Relevance of sexual polyploidization for crop improvement—A review. Euphytica 133:3–8

    Article  Google Scholar 

  • Renny-Byfield S, Kovařík A, Chester M, Nichols RA, Macas J, Novák P, Leitch AR (2012) Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7:e36963

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MA, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60:1899–1918

    Article  PubMed  CAS  Google Scholar 

  • Schwarzacher T, Bento M, Gustafson JP, Viegas W, Silva M (2011) Size matters in Triticeae polyploids: larger genomes have higher remodeling. Genome 54:175–183

    Article  Google Scholar 

  • Sears ER, Miller TE (1985) The history of Chinese spring wheat. Cereal Res Commun 13:261–263

    Google Scholar 

  • Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shewry P, Halford N, Tatham A (1992) High molecular weight subunits of wheat glutenin. J Cereal Sci 15:105–120

    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. Nat Biotechnol 13:1185–1190

    Article  CAS  Google Scholar 

  • Silkova OG, Shchapova AI, Shumny VK (2011) Patterns of meiosis in ABDR amphihaploids depend on the specific type of univalent chromosome division. Euphytica 178:415–426

    Article  Google Scholar 

  • Stebbins GL (1971) Chromosomal evolution in higher plants. Addison-Wesley, Reading

    Google Scholar 

  • Tang Z, Fu S, Ren Z, Zou Y (2009) Rapid evolution of simple sequence repeat induced by allopolyploidization. J Mol Evol 69:217–228

    Article  PubMed  CAS  Google Scholar 

  • Verbruggen I, Veraverbeke W, Vandamme A, Delcour J (1998) Simultaneous isolation of wheat high molecular weight and low molecular weight glutenin subunits. J Cereal Sci 28:25–32

    Article  CAS  Google Scholar 

  • Wan Y, Liu K, Wang D, Shewry P (2000) High-molecular-weight glutenin subunits in the Cylindropyrum and Vertebrata section of the Aegilops genus and identification of subunits related to those encoded by the Dx alleles of common wheat. Theor Appl Genet 101:879–884

    Article  CAS  Google Scholar 

  • Wan Y, Yan Z, Liu K, Zheng Y, D’Ovidio R, Shewry PR, Halford NG, Wang D (2005) Comparative analysis of the D genome-encoded high-molecular weight subunits of glutenin. Theor Appl Genet 111:1183–1190

    Article  PubMed  CAS  Google Scholar 

  • Wang D (2009) Wide hybridization: engineering the next leap in wheat yield. J Genet Genomics 36:509–510

    Article  PubMed  Google Scholar 

  • Wegel E, Vallejos RH, Christou P, Stöger E, Shaw P (2005) Large-scale chromatin decondensation induced in a developmentally activated transgene locus. J Cell Sci 118:1021–1031

    Article  PubMed  CAS  Google Scholar 

  • Wei YM, Zheng YL, Liu DC, Zhou YH, Lan XJ (2000) Gliadin and HMW-glutenin variations in Triticum turgidum L. ssp.turgidum and T. aestivum L. landraces native to Sichuan, China. Wheat Inform Serv 90:13–20

    Google Scholar 

  • Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu ZD, Dubcovsky J, Keller B (2003) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell 15:1186–1197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wicker T, Yahiaoui N, Keller B (2007) Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J 51:631–641

    Article  PubMed  CAS  Google Scholar 

  • Xie R, Wan Y, Zhang Y, Wang D (2001) HMW glutenin subunits in multiploid Aegilops species: composition analysis and molecular cloning of coding sequences. Chin Sci Bull 46:309–313

    Article  CAS  Google Scholar 

  • Yan Z, Wan Y, Liu K, Zheng Y, Wang D (2002) Identification of a novel HMW glutenin subunit and comparison of its amino acid sequence with those of homologous subunits. Chin Sci Bull 47:222–226

    Google Scholar 

  • Yuan Z, Liu D, Zhang L, Zhang L, Chen W, Yan Z, Zheng Y, Zhang H, Yen Y (2011) Mitotic illegitimate recombination is a mechanism for novel changes in high-molecular-weight glutenin subunits in wheat–rye hybrids. PLoS One 6:e23511

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhang LQ, Yen Y, Zheng YL, Liu DC (2007) Meiotic restriction in emmer wheat is controlled by one or more nuclear genes that continue to function in derived lines. Sex Plant Reprod 20:159–166

    Article  Google Scholar 

  • Zhang L, Luo JT, Hao M, Zhang LQ, Yuan ZW, Yan ZH, Liu YX, Zhang B, Liu BL, Liu DC (2012) Genetic map of Triticum turgidum based on a hexaploid wheat population without genetic recombination for D genome. BMC Genet 13:69

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank the two anonymous reviewers for helpful suggestions. This work was supported by projects of the National Natural Science Foundation of China (31201210, 31271723) and the Scientific Research Foundation of the Education Department of Sichuan Province (11ZB056).

Conflict of interest

All authors read the manuscript and do not have any conflict of interest.

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The experiments reported here comply with the current laws of the countries in which they were performed.

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Correspondence to Dengcai Liu.

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Communicated by Bernd Friebe.

Z. Yuan, M. Liu and Y. Ouyang have contributed equally to this work.

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Yuan, Z., Liu, M., Ouyang, Y. et al. The detection of a de novo allele of the Glu-1Dx gene in wheat–rye hybrid offspring. Theor Appl Genet 127, 2173–2182 (2014). https://doi.org/10.1007/s00122-014-2370-3

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  • DOI: https://doi.org/10.1007/s00122-014-2370-3

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