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Copy Number Variation and Expression Dynamics of the Dominant Vernalization-A1a Allele in Wheat

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Abstract

Adaptability of wheat to various environmental conditions, and wheat’s seasonal growth habits and the development rate are mainly controlled by allelic diversity of VRN1 genes. Dominant allele Vrn-A1a is a major determinant of the spring growth habit of wheat. Recently, copy number variation of this allele was revealed. The present study is the first report on copy number variation of allele Vrn-A1a in European varieties of spring wheat. Unexpectedly, European varieties of wheat vary greatly in Vrn-A1a duplication. Although Vrn-A1a expression proved to be high enough to promote early flowering of wheat, despite its copy number in the genome, all the latest-flowering varieties carry a single haploid copy of this allele, implying an association of duplicated Vrn-A1a with early flowering of wheat. Vrn-A1a transcript abundance in dry embryos and expression dynamics of this allele during vegetative growth were analyzed in wheat varieties differing in this allele’s copy number. Duplicated Vrn-A1a showed at least twofold higher expression at all developmental stages. The expression increase rate of this allele during wheat growth positively correlated with its basal transcription level. Although in some varieties, the expression of Vrn-A1a could decrease during wheat growth, this pattern was not found to be typical for this allele. Analysis of diurnal expression of Vrn-A1a uncovered a specific pattern with a peak of transcriptional activity at the beginning of the photoperiod and a subsequent decline. This pattern was similar to that observed for the Vrn-A1e allele and opposite to that of Vrn-A1b and Vrn-A1c.

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Data Availability

All data necessary to replicate this study’s results are included in this published article (and its supplementary information files). Raw data are available upon request.

References

  • Alonso-Peral MM, Oliver SN, Casao MC, Greenup AA, Trevaskis B (2011) The promoter of the cereal VERNALIZATION1 gene is sufficient for transcriptional induction by prolonged cold. PLoS ONE 6(12):e29456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Carver BF, Wang S, Zhang F, Yan L (2009) Genetic loci associated with stem elongation and winter dormancy release in wheat. Theor Appl Genet 118(5):881–889

    Article  CAS  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):637–645

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

    Article  CAS  PubMed  PubMed Central  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(7):575–590

    Article  CAS  PubMed  Google Scholar 

  • Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS ONE 7(3):e33234

    Article  PubMed  PubMed Central  Google Scholar 

  • Dixon LE, Karsai I, Kiss T, Adamski NM, Liu Z, Ding Y, Allard V, Boden SA, Griffiths S (2019) VERNALIZATION1 controls developmental responses of winter wheat under high ambient temperatures. Development 146(3):dev172684

    Article  CAS  PubMed  PubMed Central  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(3):426–441

    Article  CAS  PubMed  Google Scholar 

  • Eagles HA, Cane K, Neil V (2009) The flow of alleles of important photoperiod and vernalisation genes through australian wheat. Crop and Pasture Science 60:646–657

    Article  CAS  Google Scholar 

  • Efremova TT, Arbuzova VS, Leonova IN, Makhmudova K (2011) Multiple allelism in the Vrn-B1 locus of common wheat. Cereal Res Commun 39:12–21

    Article  Google Scholar 

  • Fehrmann RS, Karjalainen JM, Krajewska M, Westra HJ, Maloney D, Simeonov A, Pers TH, Hirschhorn JN, Jansen RC, Schultes EA, van Haagen HH, de Vries EG, te Meerman GJ, Wijmenga C, van Vugt MA, Franke L (2015) Gene expression analysis identifies global gene dosage sensitivity in cancer. Nat Genet 47(2):115–125

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guedira M, Xiong M, Hao YF, Johnson J, Harrison S, Marshall D, Brown-Guedira G (2016) Heading date QTL in Winter Wheat (Triticum aestivum L.) coincide with major developmental genes VERNALIZATION1 and PHOTOPERIOD1. PLoS ONE 11(5):e0154242

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo M, Davis D, Birchler JA (1996) Dosage effects on gene expression in a maize ploidy series. Genetics 142(4):1349–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halloran GM (1967) Gene dosage and vernalization response in homoeologous group 5 of Triticum Aestivum. Genetics 57(2):401–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henrichsen CN, Chaignat E, Reymond A (2009a) Copy number variants, diseases and gene expression. Hum Mol Genet 18(R1):R1–8

    Article  CAS  PubMed  Google Scholar 

  • Henrichsen CN, Vinckenbosch N, Zöllner S, Chaignat E, Pradervand S, Schütz F, Ruedi M, Kaessmann H, Reymond A (2009b) Segmental copy number variation shapes tissue transcriptomes. Nat Genet 41(4):424–429

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Feulner PGD, Eizaguirre C, Lenz TL, Bornberg-Bauer E, Milinski M, Reusch TBH, Chain FJJ (2019) Genome-wide genotype-expression Relationships reveal both copy number and single nucleotide differentiation contribute to Differential Gene expression between Stickleback Ecotypes. Genome Biol Evol 11(8):2344–2359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaaska V (1978) NADP-dependent aromatic alcohol dehydrogenase in polyploid wheats and their diploid relatives. On the origin and phylogeny of polyploid wheats. Theor Appl Genet 53(5):209–217

    Article  CAS  PubMed  Google Scholar 

  • Kato H, Taketa S, Ban T, Iriki N, Murai K (2001) The influence of a spring habit gene, Vrn-D1, on heading time in wheat. Plant Breed 120:115–120

    Article  CAS  Google Scholar 

  • Khan AR, Enjalbert J, Marsollier AC, Rousselet A, Goldringer I, Vitte C (2013) Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biol 13:209

    Article  PubMed  PubMed Central  Google Scholar 

  • Kippes N, Debernardi JM, Vasquez-Gross HA, Akpinar BA, Budak H, Kato K, Chao S, Akhunov E, Dubcovsky J (2015) Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proc Natl Acad Sci U S A 112(39):E5401–E5410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kippes N, Guedira M, Lin L, Alvarez MA, Brown-Guedira GL, Dubcovsky J (2018) Single nucleotide polymorphisms in a regulatory site of VRN-A1 first intron are associated with differences in vernalization requirement in winter wheat. Mol Genet Genomics 293(5):1231–1243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiss T, Balla K, Veisz O, Láng L, Bedő Z, Griffiths S, Isaac P, Karsai I (2014) Allele frequencies in the VRN-A1, VRN-B1 and VRN-D1 vernalization response and PPD-B1 and PPD-D1 photoperiod sensitivity genes, and their effects on heading in a diverse set of wheat cultivars (Triticum aestivum L). Mol Breed 34:297–310

    Article  CAS  PubMed  Google Scholar 

  • Konopatskaia I, Vavilova V, Kondratenko EY, Blinov A, Goncharov NP (2016) VRN1 genes variability in tetraploid wheat species with a spring growth habit. BMC Plant Biol 16(Suppl 3):244

    Article  PubMed  Google Scholar 

  • Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138(4):2364–2373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makhoul M, Chawla HS, Wittkop B, Stahl A, Voss-Fels KP, Zetzsche H, Snowdon RJ, Obermeier C (2022) Long-Amplicon single-molecule sequencing reveals Novel, Trait-Associated Variants of VERNALIZATION1 homoeologs in Hexaploid Wheat. Front Plant Sci 13:942461

    Article  PubMed  PubMed Central  Google Scholar 

  • Más P, Yanovsky MJ (2009) Time for circadian rhythms: plants get synchronized. Curr Opin Plant Biol 12(5):574–579

    Article  PubMed  Google Scholar 

  • Milec Z, Tomkova L, Sumikova T, Pankova K (2012) A new multiplex PCR test for the determination of Vrn-B1 alleles in bread wheat (Triticum aestivum L). Mol Breed 30:317–323

    Article  CAS  Google Scholar 

  • Milec Z, Sumikova T, Tomkova L, Pankova K (2013) Distribution of different Vrn-B1 alleles in hexaploid spring wheat germplasm. Euphytica 192(3):371–378

    Article  CAS  Google Scholar 

  • Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44(12):1255–1265

    Article  CAS  PubMed  Google Scholar 

  • Muterko A, Kalendar R, Salina E (2016a) Novel alleles of the VERNALIZATION1 genes in wheat are associated with modulation of DNA curvature and flexibility in the promoter region. BMC Plant Biol 16(Suppl 1):9

    Article  PubMed  PubMed Central  Google Scholar 

  • Muterko A, Kalendar R, Salina E (2016b) Allelic variation at the VERNALIZATION-A1, VRN-B1, VRN-B3, and PHOTOPERIOD-A1 genes in cultivars of Triticum durum Desf. Planta 244(6):1253–1263

    Article  CAS  PubMed  Google Scholar 

  • Muterko AF, Salina EA (2017) Analysis of the VERNALIZATION-A1 exon-4 polymorphism in polyploid wheat. Vavilov J Genet Breed 21(3):323–333

    Article  Google Scholar 

  • Muterko A, Salina E (2018) Origin and distribution of the VRN-A1 exon 4 and exon 7 haplotypes in domesticated wheat species. Agronomy 8(8):156

    Article  CAS  Google Scholar 

  • Muterko A, Salina E (2019) VRN1-ratio test for polyploid wheat. Planta 250(6):1955–1965

    Article  CAS  PubMed  Google Scholar 

  • Muterko A, Salina E (2021) Features of transcriptional dynamics of the duplicated Vernalization-B1 gene in wheat (Triticum spp). Plant Breed 140(6):1023–1031

    Article  CAS  Google Scholar 

  • Muterko A (2022) Selective precipitation of RNA with linear polyacrylamide. Nucleosides Nucleotides Nucleic Acids 41(1):61–76

    Article  CAS  PubMed  Google Scholar 

  • Nishiura A, Kazama Y, Abe T, Mizuno N, Nasuda S, Murai K (2014) Level of VERNALIZATION 1 expression is correlated with earliness in extra early-flowering mutant wheat lines. Breed Sci 64(3):213–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowak M, Kowalczyk K (2010) Allelic variation at the VRN-1 locus of polish Cultivars of Common Wheat (Triticum aestivum L.). Acta biologica Cracoviensia. Ser Bot 522(2):86–91

    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 Nat Acad Sci USA 106:8386–8391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver SN, Deng W, Casao MC, Trevaskis B (2013) Low temperatures induce rapid changes in chromatin state and transcript levels of the cereal VERNALIZATION1 gene. J Exp Bot 64(8):2413–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orozco LD, Cokus SJ, Ghazalpour A, Ingram-Drake L, Wang S, van Nas A, Che N, Araujo JA, Pellegrini M, Lusis AJ (2009) Copy number variation influences gene expression and metabolic traits in mice. Hum Mol Genet 18(21):4118–4129

    Article  CAS  PubMed  PubMed Central  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 (1971) A genetic analysis of the spring-winter habit of growth in wheat. Aust J Agric Res 22:21–23

    Article  Google Scholar 

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

    Article  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 

  • Sasani S, Hemming MN, Oliver SN, Greenup A, Tavakkol-Afshari R, Mahfoozi S, Poustini K, Sharifi HR, Dennis ES, Peacock WJ, Trevaskis B (2009) The influence of vernalization and daylength on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). J Exp Bot 60(7):2169–2178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlattl A, Anders S, Waszak SM, Huber W, Korbel JO (2011) Relating CNVs to transcriptome data at fine resolution: assessment of the effect of variant size, type, and overlap with functional regions. Genome Res 21(12):2004–2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao X, Lv N, Liao J, Long J, Xue R, Ai N, Xu D, Fan X (2019) Copy number variation is highly correlated with differential gene expression: a pan-cancer study. BMC Med Genet 20(1):175

    Article  PubMed  PubMed Central  Google Scholar 

  • Shcherban A, Chebotar S, Chebotar G, Efremova T, Salina E (2012) A wide distribution of a new Vrn-B1c allele of wheat T.aestivum in Russia, Ukraine and adjacent regions. J Stress Physiol Biochem 8(3):S13

    Google Scholar 

  • Shcherban AB, Khlestkina EK, Efremova TT, Salina EA (2013) The effect of two differentially expressed wheat VRN-B1 alleles on the heading time is associated with structural variation in the first intron. Genetica 141(4–6):133–141. https://doi.org/10.1007/s10709-013-9712-y

    Article  CAS  PubMed  Google Scholar 

  • Shcherban AB, Boerner A, Salina EA (2015) Effect of VRN-1 and PPD-D1 genes on heading time in european bread wheat cultivars. Plant Breed 134(1):49–55

    Article  CAS  Google Scholar 

  • Shimada S, Ogawa T, Kitagawa S, Suzuki T, Ikari C, Shitsukawa N, Abe T, Kawahigashi H, Kikuchi R, Handa H, Murai K (2009) A genetic network of flowering-time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J 58(4):668–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stelmakh AF (1992) Genetic effects of vrn genes on heading date and agronomic traits in bread wheat. Euphytica 65(1):53–60

    Article  Google Scholar 

  • Stranger BE, Forrest MS, Dunning M, Ingle CE, Beazley C, Thorne N, Redon R, Bird CP, de Grassi A, Lee C, Tyler-Smith C, Carter N, Scherer SW, Tavaré S, Deloukas P, Hurles ME, Dermitzakis ET (2007) Relative impact of nucleotide and copy number variation on gene expression phenotypes. Science 315(5813):848–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strejčková B, Milec Z, Holušová K, Cápal P, Vojtková T, Čegan R, Šafář J (2021) In-Depth sequence analysis of Bread Wheat VRN1 genes. Int J Mol Sci 22(22):12284

    Article  PubMed  PubMed Central  Google Scholar 

  • Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Nat Acad Sci USA 100(22):13099–13104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trevaskis B, Hemming MN, Peacock WJ, Dennis ES (2006) HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol 140(4):1397–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Würschum T, Boeven PH, Langer SM, Longin CF, Leiser WL (2015) Multiply to conquer: copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet 16:96

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao J, Xu S, Li C, Xu Y, Xing L, Niu Y, Huan Q, Tang Y, Zhao C, Wagner D, Gao C, Chong K (2014) O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat. Nat Commun 5:4572

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Dong Q, Deng M, Lin D, Xiao J, Cheng P, Xing L, Niu Y, Gao C, Zhang W, Xu Y, Chong K (2021) The vernalization-induced long non-coding RNA VAS functions with the transcription factor TaRF2b to promote TaVRN1 expression for flowering in hexaploid wheat. Mol Plant 14(9):1525–1538

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN-1 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 JL, 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  PubMed Central  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L). Genome Biol 8(6):R96

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu M, Carver BF, Yan L (2014) TamiR1123 originated from a family of miniature inverted-repeat transposable elements (MITE) including one inserted in the Vrn-A1a promoter in wheat. Plant Sci 215–216:117–123

    Article  PubMed  Google Scholar 

  • Zhang X, Xiao Y, Zhang Y, Xia X, Dubcovsky J, He Z (2008) Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in chinese wheat cultivars and their association with growth habit. Crop Sci 48(2):458–470

    Article  CAS  Google Scholar 

  • Żmieńko A, Samelak A, Kozłowski P, Figlerowicz M (2014) Copy number polymorphism in plant genomes. Theor Appl Genet 127(1):1–18

    Article  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the Russian Science Foundation grant number 18-74-00080.

The manuscript prepared within the government-funded project FWNR-2022-0017.

The English language was corrected by shevchuk-editing.com.

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  1. Institute of Cytology and Genetics SB RAS, Lavrentyeva Avenue 10, Novosibirsk, 630090, Russian Federation

    Alexandr Muterko

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Muterko, A. Copy Number Variation and Expression Dynamics of the Dominant Vernalization-A1a Allele in Wheat. Plant Mol Biol Rep 42, 135–150 (2024). https://doi.org/10.1007/s11105-023-01406-5

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