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Wheat VIN3-like PHD finger genes are up-regulated by vernalization

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Abstract

The term ‘vernalization’ describes the acceleration of the transition between the vegetative and reproductive stages after exposing plants to an extended period of low temperature. In Arabidopsis, vernalization promotes flowering by silencing the flowering repressor gene FLOWERING LOCUS C (FLC). Mitotically stable repression of FLC is the result of chromatin modifications mediated by the Vernalization-INsensitive 3 (VIN3) and VIN3-Like (VIL) proteins. In this study, we identified and characterized three VIL genes in diploid wheat (Triticum monococcum L.), named TmVIL1, TmVIL2, and TmVIL3. Similar to Arabidopsis VIN3, all three wheat VIL proteins carry three conserved domains including a plant homeodomain finger motif (PHD), a fibronectin type III domain (FNIII), and a VIN3 interacting domain (VID). Genetic mapping placed TmVIL1, TmVIL2, and TmVIL3 loci in the centromeric regions of chromosome 5, 6, and 1, respectively. The chromosome location of TmVIL1 is close to that of the vernalization gene VRN-D5, but more precise mapping information is required to validate this relationship. Transcription of the wheat VIL genes was up-regulated by vernalization, with a peak after 4–6 weeks of cold treatment. When transferred back to warm conditions, transcript levels of the wheat VIL genes returned to pre-vernalization levels. In addition, the transcript levels of wheat VIL genes are affected by photoperiod. This study indicates that wheat VIL genes have retained a similar structure and transcriptional regulation as their Arabidopsis VIN3/VIL homologues, suggesting that they might have retained some of their functions.

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Abbreviations

dCAPS:

Degenerate cleaved amplified polymorphic sequences

FLC:

Flowering locus C

FNIII:

Fibronectin type III

LD:

Long day

PcG:

Polycomb-group

PHD:

Plant homeodomain

SD:

Short day

VID:

VIN3 interacting domain

VIL:

VIN3-like

VIN3:

Vernalization-INsensitive 3

References

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD-finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem Sci 20:56–59

    Article  CAS  PubMed  Google Scholar 

  • Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559

    Article  CAS  PubMed  Google Scholar 

  • Aspberg A, Miura R, Bourdoulous S, Shimonaka M, Heinegård D, Schachner M, Ruoslahti E, Yamaguchi Y (1997) The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc Natl Acad Sci USA 94:10116–10121

    Article  CAS  PubMed  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141

    Article  CAS  PubMed  Google Scholar 

  • Chandler J, Wilson A, Dean C (1996) Arabidopsis mutants showing an altered response to vernalization. Plant J 10:637–644

    Article  CAS  PubMed  Google Scholar 

  • Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:191–238

    Article  CAS  Google Scholar 

  • Cokol M, Nair R, Rost B (2000) Finding nuclear localization signals. EMBO Rep 1:411–415

    Article  CAS  PubMed  Google Scholar 

  • Dubcovsky J, Luo MC, Zhong GY, Bransteitter R, Desai A, Kilian A, Kleinhofs A, Dvořák J (1996) Genetic map of diploid wheat, Triticum monococcum L, and its comparison with maps of Hordeum vulgare L. Genetics 143:983–999

    CAS  PubMed  Google Scholar 

  • Dubcovsky J, Galvez AF, Dvořák J (1994) Comparison of the genetic organization of the early salt-stress-response gene system in salt-tolerant Lophopyrum-elongatum and salt-sensitive wheat. Theor Appl Genet 87:957–964

    Article  CAS  Google Scholar 

  • Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G (1998) Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor Appl Genet 97:968–975

    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 60:469–480

    Article  CAS  PubMed  Google Scholar 

  • Dvořák J, McGuire PE, Cassidy B (1988) Apparent sources of the A genomes of wheats inferred from the polymorphism in abundance and restriction fragment length of repeated nucleotide sequences. Genome 30:680–689

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fu D, Amand PCS, Xiao Y, Muthukrishnan S, Liang GH (2006) Characterization of T-DNA integration in creeping bentgrass. Plant Sci 170:225–237

    Article  CAS  Google Scholar 

  • Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535

    Article  CAS  PubMed  Google Scholar 

  • Gilbert BE (1926) Interrelation of relative day length and temperature. Bot Gaz 81:1–24

    Google Scholar 

  • Islam-Faridi MN, Worland AJ, Law CN (1996) Inhibition of ear-emergence time and sensitivity to day-length determined by the group 6 chromosomes of wheat. Heredity 77:572–580

    Google Scholar 

  • Kato K, Yamashita M, Ishimoto K, Yoshino H, Fujita M (2003) Genetic analysis of two genes for vernalization response, the former Vrn2 and Vrn4, using PCR based molecular markers. In: Pogna NE, Romano N, Pogna EA, Galterio G (eds) Proceedings of the 10th international wheat genet symposium, vol 3, Instituto Sperimentale per la Cerealcoltura, Rome, Italy, pp971–973

  • Koornneef M, Alonso-Blanco C, Peeters AJM, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 49:345–370

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment brief. Bioinformatics 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Law CN, Wolfe MS (1966) Location of genetic factors for mildiew resistance and ear emergence time on chromosome 7B of wheat. Can J Genet Cytol 8:462–470

    Google Scholar 

  • Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246

    Article  CAS  PubMed  Google Scholar 

  • Lijavetzky D, Muzzi G, Wicker T, Keller B, Wing R, Dubcovsky J (1999) Construction and characterization of a bacterial artificial chromosome (BAC) library for the A genome of wheat. Genome 42:1176–1182

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 to the (-Delta Delta Ct) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lupas A, van Dyke M, Stock J (1991) Predicting coled coils from protein sequences. Science 252:1162–1164

    Article  CAS  Google Scholar 

  • McIntosh RA, Yamazaki Y, Devos KM, Dubcovsky J, Rogers WJ, Appels R (2003) Catalogue of gene symbols for wheat. In: Pogna NE, Romano M, Pogna E, Galterio G (eds) Proceedings of the 10th international wheat genetics symposium, vol 4, Instituto Sperimentale per la Cerealicoltura, Rome pp1–34

  • Michaels SD, Amasino RM (1998) A robust method for detecting single-nucleotide changes as polymorphic markers by PCR. Plant J 14:381–385

    Article  CAS  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  CAS  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13:935–942

    Article  CAS  PubMed  Google Scholar 

  • Nair R, Rost B (2005) Mimicking cellular sorting improves prediction of subcellular localization. J Mol Biol 348:85–100

    Article  CAS  PubMed  Google Scholar 

  • Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615

    Article  CAS  PubMed  Google Scholar 

  • Pankov R, Yamada KM (2002) Fibronectin at a glance. J Cell Sci 115:3861–3863

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, USA, pp 365–386

    Google Scholar 

  • Schonrock N, Bouveret R, Leroy O, Borghi L, Kohler C, Gruissem W, Hennig L (2006) Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev 20:1667–1678

    Article  CAS  PubMed  Google Scholar 

  • Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537

    Article  CAS  PubMed  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758

    Article  CAS  PubMed  Google Scholar 

  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    Article  CAS  PubMed  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the rosetta stone of flowering time. Science 296:285–289

    Article  CAS  PubMed  Google Scholar 

  • Sung S, Amasino RM (2004a) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164

    Article  CAS  Google Scholar 

  • Sung S, Amasino RM (2004b) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10

    Article  CAS  Google Scholar 

  • Sung S, Schmitz RJ, Amasino RM (2006) A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20:3244–3248

    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  CAS  PubMed  Google Scholar 

  • Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286:481–486

    Article  CAS  PubMed  Google Scholar 

  • Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103:14631–14636

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004b) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor Appl Genet 109:1677–1686

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA (in press). DOI:10.1073/PNAS.0607142103

  • Yasuda S (1969) Linkage and pleiotropic effects on agronomic characters of the genes for spring growth habit. Barley Newsl 12:57–58

    Google Scholar 

Download references

Acknowledgments

This research was supported by the United States Department of Agriculture CSREES NRI competitive grant 2006-01160, and NSF-Plant Genome grant DBI-0321462. The work has been carried out in compliance with the current laws governing genetic experimentation in the USA.

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Correspondence to Jorge Dubcovsky.

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Communicated by S. Hohmann.

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Fu, D., Dunbar, M. & Dubcovsky, J. Wheat VIN3-like PHD finger genes are up-regulated by vernalization. Mol Genet Genomics 277, 301–313 (2007). https://doi.org/10.1007/s00438-006-0189-6

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