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The New Wheat Vernalization Response Allele Vrn-D1s is Caused by DNA Transposon Insertion in the First Intron

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Abstract

Vernalization requirement in hexaploid wheat is largely controlled by a series of homoeologous VERNALIZATION (Vrn) genes, Vrn-A1, Vrn-B1, and Vrn-D1. The sequence of the promoter area and first intron of Vrn-D1 were analysed in 77 hexaploid accessions, representing five wheat species (Triticum compactum, Triticum sphaerococcum, Triticum spelta, Triticum vavilovii, and Triticum macha) sampled from different ecogeographic areas within 35 countries. Polymorphism was detected in the Vrn-D1 promoter, resulting in a new Vrn-D1 haplotype (named here, Hap-8T). Analysis of Vrn-D1 intron-1 sequences revealed a novel insertional mutation in a subset of T. spelta and T. compactum accessions. This mutant allele was designated Vrn-D1s. Analysis of the 844 bp insertion revealed it to be a novel transposable DNA element (named DTA_Chimera_KF800714) not previously described in Triticum, belonging to the hAT superfamily. Finally, we describe a PCR-based assay that discriminates the wild-type vrn-D1 allele from the Vrn-D1s allele. Collectively, the work described here highlights the potential of utilizing minor hexaploid wheat species for the identification of novel alleles of agronomic importance.

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References

  • Anderson O, Dubcovsky J, Matthews D, Sabot F, Wicker T (2005) Nomenclature, classification and annotation of repetitive elements. http://wheat.pw.usda.gov/ITMI/Repeats/Nomenclatures_for_TREP. Accessed 4 December 2002, revised April 2005

  • Bariana H, Brown G, Ahmed N, Khatkar S, Conner R, Wellings C, Haley S, Sharp P, Laroche A (2002) Characterisation of Triticum vavilovii-derived stripe rust resistance using genetic, cytogenetic and molecular analyses and its marker-assisted selection. Theor Appl Genet 104(2–3):315–320

    Article  CAS  PubMed  Google Scholar 

  • Bentley AR, Jensen EF, Mackay IJ, Hönicka H, Fladung M, Hori K, Yano M, Mullet JE, Armstead IP, Hayes C, Thorogood D, Lovatt A, Morris R, Pullen N, Mutasa-Göttgens E, Cockram J (2013) Flowering time. Genomics and breeding for climate-resilient crops 2 (Ed: C Cole):1-67

  • Brenchley R, Spannagl M, Pfeifer M, Barker GL, D'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491(7426):705–710

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Budowle B, Chakraborty R, Giusti AM, Eisenberg AJ, Allen RC (1991) Analysis of the VNTR locus D1S80 by the PCR followed by high-resolution PAGE. Am J Hum Genet 48(1):137–144

    PubMed Central  CAS  PubMed  Google Scholar 

  • Buerstmayr M, Lemmens M, Steiner B, Buerstmayr H (2011) Advanced backcross QTL mapping of resistance to Fusarium head blight and plant morphological traits in a Triticum macha × T. aestivum population. Theor Appl Genet 123(2):293–306

    Article  PubMed Central  PubMed  Google Scholar 

  • Chu CG, Tan CT, Yu GT, Zhong S, Xu SS, Yan L (2011) A novel retrotransposon inserted in the dominant Vrn-B1 allele confers spring growth habit in tetraploid wheat (Triticum turgidum L.). G3 (Bethesda) 1(7):637–645

    Article  CAS  Google Scholar 

  • Cockram J, Chiapparino E, Taylor SA, Stamati K, Donini P, Laurie DA, O'sullivan DM (2007a) Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype. Theor Appl Genet 115(7):993–1001

    Article  CAS  PubMed  Google Scholar 

  • Cockram J, Mackay IJ, O’Sullivan DM (2007b) The role of double-stranded break repair in the creation of phenotypic diversity at cereal VRN1 loci. Genetics 177(4):2535–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cockram J, Norris C, O’Sullivan DM (2009) PCR markers diagnostic for seasonal growth habit in barley. Crop Sci 49(2):403–410

    Article  CAS  Google Scholar 

  • Danyluk J, Kane N, Breton G, Limin A, Fowler D, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132(4):1849–1860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Diallo AO, Ali-Benali MA, Badawi M, Houde M, Sarhan F (2012) Expression of vernalization responsive genes in wheat is associated with histone H3 trimethylation. Mol Genet Genomics 287:575–590

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12(2):178–184

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19:11–15

    Google Scholar 

  • Dubcovsky J, Chen C, Yan L (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15:395–407

    Article  CAS  Google Scholar 

  • Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L (2006) Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol 60(64):469–480

    Article  CAS  PubMed  Google Scholar 

  • Dubcovsky J, Li C, Distelfeld A, Pidal B, Tranquilli G (2008) Genes and gene networks regulating wheat development. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (eds). Proceedings of 11th International Wheat Genetics Symposium: 24–29

  • Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734

    CAS  PubMed  Google Scholar 

  • Fu D, Szucs P, Yan L, Helguera M, Skinner J, Hayes P, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Gen Genomics 273(4):54–65

    Article  CAS  Google Scholar 

  • Golovnina K, Kondratenko E, Blinov A, Goncharov N (2010) Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats. BMC Plant Biology 10(168):168–183

    Article  PubMed Central  PubMed  Google Scholar 

  • Goncharov NP (2003) Genetics of growth habit (spring vs winter) in common wheat: confirmation of the existence of dominant Vrn4. Theor Appl Genet 107:768–772

    Article  CAS  PubMed  Google Scholar 

  • Gultyaeva EI, Mikhailova LA, Karetnikova ES, Anpilova NA (2002) Triticum spelta L. as a source of new genes of resistance to wheat leaf rust (Puccinia recondita Rob. ex Desm. f.sp. tritici). J Russ PhytopatholSoc 3:61–64

    Google Scholar 

  • Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Low temperature and day length cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147(1):355–366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hemming MN, Fieg S, Peacock WJ, Dennis ES, Trevaskis B (2009) Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Mol Genet Genomics 282(2):107–117

    Article  CAS  PubMed  Google Scholar 

  • Iwaki K, Nishida J, Yanagisawa T, Yoshida H, Kato K (2002) Genetic analysis of Vrn-B1 for vernalization requirement by using linked dCAPS markers in bread wheat (Triticum aestivum L.). Theor Appl Genet 104(4):571–576

    Article  CAS  PubMed  Google Scholar 

  • Kempken F, Windhofer F (2001) The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Kinjo H, Shitsukawa N, Takumi S, Murai K (2012) Diversification of three APETALA1/FRUITFULL-like genes in wheat. Mol Genet Genomics 287(4):283–294

    Article  CAS  PubMed  Google Scholar 

  • Kippes N, Zhu J, Chen A, Vanzetti L, Lukaszewski A, Nishida H, Kato K, Dvorak J, Dubcovsky J (2014) Fine mapping and epistatic interactions of the vernalization gene VRN-D4 in hexaploid wheat. Mol Genet Genomics 289(1):47–62

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7:474–481

    Article  PubMed Central  PubMed  Google Scholar 

  • Law C, Worland A, Giorgi B (1975) The genetic control of ear emergence time by chromosomes 5A and 5D of wheat. Heredity 36(1):49–58

    Article  Google Scholar 

  • Liu J, He YH, Amasino R, Chen XM (2004) siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 18:2873–2878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138(4):2364–2373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • MacRae AF, Clegg MT (1992) Evolution of Ac and Ds1 elements in select grasses (Poaceae). Genetica 86:55–66

    Article  CAS  PubMed  Google Scholar 

  • Nkongolo K, Quick J, Meyer W, Peairs F (1989) Russian wheat aphid resistance of wheat, rye and triticale in green-house tests. Cereal Res Commun 17:227–232

    Google Scholar 

  • Oliver S, Finnegan E, Dennis E, Peacock W, Trevaskis B (2009) Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Natl Acad Sci U S A 106(20):8386–8391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pidal B, Yan L, Fu D, Zhang F, Tranquilli G, Dubcovsky J (2009) The CArG-Box located upstream from the transcriptional start of wheat vernalization gene VRN1 is not necessary for the vernalization response. J Hered 100(3):355–364

    Article  CAS  PubMed  Google Scholar 

  • Pugsley AT (1972) Additional genes inhabiting winter habit in wheat. Euphytica 21:547–552

    Article  Google Scholar 

  • Rubin E, Lithwick G, Levy AA (2001) Structure and evolution of the hAT transposon superfamily. Genetics 158:949–957

    PubMed Central  CAS  PubMed  Google Scholar 

  • Santra DK, Santra M, Allan RE, Campbell KG, Kidwell KK (2009) Genetic and molecular characterization of vernalization genes Vrn-A1, Vrn-B1, and Vrn-D1 in spring wheat germplasm from the pacific northwest region of the USA. Plant Breed 128:576–584

    Article  CAS  Google Scholar 

  • Shcherban AB, Efremova TT, Salina EA (2012) Identification of a new Vrn-B1 allele using two near-isogenic wheat lines with difference in heading time. Mol Breed 29(3):675–685

    Article  CAS  Google Scholar 

  • Shitsukawa N, Ikari C, Shimada S, Kitagawa S, Sakamoto K, Saito H, Ryuto H, Fukunishi N, Abe T, Takumi S, Nasuda S, Murai K (2007) The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene. Genes Genet Syst 82(2):167–170

    Article  CAS  PubMed  Google Scholar 

  • Simon MR, Worland AJ, Cordo CA, Struik PC (2001) Chromosomal location of resistance to Septoria tritici in seedlings of a synthetic hexaploid wheat, Triticum spelta and two cultivars of Triticum aestivum. Euphytica 119(1):151–155

    Article  Google Scholar 

  • Steed A, Chandler E, Thomsett M, Gosman N, Faure S, Nicolson P (2005) Identification of type I resistance to Fusarium head blight controlled by a major gene located on chromosome 4A of Triticum macha. Theor Appl Genet 111:521–529

    Article  CAS  PubMed  Google Scholar 

  • Stelmakh AF (1993) Genetic effects of Vrn genes on heading date and agronomic traits in bread wheat. Euphytica 65:53–60

    Article  Google Scholar 

  • Stelmakh AF (1998) Genetic systems regulating flowering response in wheat. Euphytica 100:359–369

    Article  Google Scholar 

  • Takumi S, Koyama K, Fujiwara K, Kobayashi F (2011) Identification of a large deletion in the first intron of the Vrn-D1 locus, associated with loss of vernalization requirement in wild wheat progenitor Aegilops tauschii Coss. Genes Genet Syst 86(3):183–195

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trevaskis B, Bagnall D, Ellis M, Peacock W, Dennis E (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci U S A 100(22):13099–13104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trevaskis B, Hemming M, Dennis E, Peacock W (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12(8):352–357

    Article  CAS  PubMed  Google Scholar 

  • Tsubota SI, Huong DV (1991) Capture of flanking DNA by a P element in Drosophila melanogaster: creation of a transposable element. Proc Natl Acad Sci U S A 88:693–697

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • von Zitzewitz J, Szucs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen TH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59(3):449–467

    Article  CAS  Google Scholar 

  • Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci U S A 100(10):6263–6268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN1 promoter region in polyploid wheat. Theor Appl Genet 109(8):1677–1686

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen J, Echenique V, Dubcovsky J (2004b) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303(5664):1640–1644

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A 103(51):19581–19586

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Wang Y, Wu S, Yang J, Liu H, Zhou Y (2012) A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor Appl Genet 125(8):1697–1704

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Genomics and Biotechnology, Plant Breeding and Genetics Institute – National Center of Seed and Cultivar Investigation, Ovidiopolskaya Road 3, Odessa, 65036, Ukraine

    Alexandr Muterko, Irina Balashova & Yuri Sivolap

  2. National Institute of Agricultural Botany (NIAB), Huntington Road, Cambridge, CB3 0LE, UK

    James Cockram

  3. University of Helsinki, Institute of Biotechnology, MTT Plant Genomics Laboratory, Biocentre 3, P.O. Box 65, Viikinkaari 1, Helsinki, 00014, Finland

    Ruslan Kalendar

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  1. Alexandr Muterko
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  2. Irina Balashova
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  4. Ruslan Kalendar
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Correspondence to Alexandr Muterko.

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Muterko, A., Balashova, I., Cockram, J. et al. The New Wheat Vernalization Response Allele Vrn-D1s is Caused by DNA Transposon Insertion in the First Intron. Plant Mol Biol Rep 33, 294–303 (2015). https://doi.org/10.1007/s11105-014-0750-0

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