Skip to main content
Log in

Changes in FLC and VIN3 Expression during Vernalization of Arabidopsisthaliana Plants from Northern Natural Populations

  • PLANT GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Specific expression patterns of the FLC and VIN3 genes, which play a key role in the vernalization-mediated transition to flowering of A. thaliana plants from northern natural populations (Karelia), have been revealed. The differences in the FLC and VIN3 expression patterns during vernalization for populations represented by late-flowering forms, on one hand, and a population which was mixed with respect to the onset of flowering, on the other hand, were observed. A low level of FLC and VIN3 expression in plants from the studied populations prior to cold exposure was established. During vernalization, the FLC mRNA levels increased on the 10th and 20th day, followed by its decrease by the 30th day. Prolonged exposure to cold caused an increase in VIN3 expression with a peak in the populations represented by late-flowering plant forms on the 30th day of vernalization and in the mixed population for the flowering onset of plants on the 40th day. Specific patterns of FLC and VIN3 expression during vernalization was observed in S1 offspring of one early-flowering plant, while FLC expression in it changed according to classical scheme; i.e., the initially high level of FLC expression decreased in the process of vernalization. It is suggested that genetic and epigenetic mechanisms involved in controlling the flowering rate and the genes involved in this process may differ in plants from populations of different geographic regions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Koornneef, M., Alonso-Blanco, C., Peeters, A.J.M., and Soppe, W., Genetic control of flowering time in Arabidopsis, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1998, vol. 49, pp. 345—370.

    Article  CAS  PubMed  Google Scholar 

  2. Boss, P.K., Bastow, R.M., Mylne, J.S., and Dean, C., Multiple pathways in the decision to flower: enabling, promoting and resetting, Plant Cell, 2004, vol. 16, pp. 18—31. https://doi.org/10.1105/tpc.015958

    Article  Google Scholar 

  3. Michaels, S.D. and Amasino, R.M., FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering, Plant Cell, 1999, vol. 11, pp. 949—956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Schmitz, R.J. and Amasino, R.M., Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants, Biochim. Biophys. Acta, 2007, no. 1769, pp. 269—275. https://doi.org/10.1016/j.bbaexp.2007.02.003

  5. He, Y., Michaels, S.D., and Amasino, R.M., Regulation of flowering time by histone acetylation in Arabidopsis, Science, 2003, vol. 302, pp. 1751—1754. https://doi.org/10.1126/science.1091109

    Article  CAS  PubMed  Google Scholar 

  6. Ausin, L., Alonso-Blanco, C., and Martinez-Zapater, J.M., Regulation of flowering time by FVE, a retinoblastoma-associated protein, Nat. Genet., 2004, vol. 36, pp. 162—166.

    Article  CAS  PubMed  Google Scholar 

  7. Johanson, U., West, J., Lister, C., et al., Molecular analysis of FRIGIDA, major determinant of natural variation in Arabidopsis flowering time, Science, 2000, vol. 290, pp. 344—347. https://doi.org/10.1126/science.290.5490.344

    Article  CAS  PubMed  Google Scholar 

  8. Le Corre, V., Roux, F., and Reboud, X., DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time, Mol. Biol. Evol., 2002, vol. 19, no. 8, pp. 1261—1271. https://doi.org/10.1093/oxfordjournals.molbev.a004187

    Article  CAS  PubMed  Google Scholar 

  9. Gazzani, S., Gendall, A.R., Lister, C., and Dean, C., Analysis of the molecular basis of flowering time variation in Arabidopsis accessions, Plant Physiol., 2003, vol. 132, pp. 1107—1114. https://doi.org/10.1104/pp.103.021212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Shindo, Ch., Aranzana, M.J., Lister, C., et al., Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis, Plant Physiol., 2005, vol. 138, pp. 1163—1173. https://doi.org/10.1104/pp.105.061309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sheldon, C.C., Rouse, D.T., Finnegan, E.J., et al., The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC), Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 3753—3758. https://doi.org/10.1073/pnas.060023597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Saleh, A., Alvarez-Venegas, R., and Avramova, Z., Dynamic and stable histone H3 methylation patterns at the Arabidopsis FLC and AP1 loci, Gene, 2008, vol. 423, pp. 43—47. https://doi.org/10.1016/j.gene.2008.06.022

    Article  CAS  PubMed  Google Scholar 

  13. Sung, S. and Amasino, R.M., Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3, Nature, 2004, vol. 427, pp. 159—164. https://doi.org/10.1038/nature02195

    Article  CAS  PubMed  Google Scholar 

  14. Li, H., Ilin, S., Wang, W., et al., Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF, Nature, 2006, vol. 442, pp. 91—95. https://doi.org/10.1038/nature04802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Jung, C. and Muller, A.F., Flowering time control and applications in plant breeding, Trends Plant Sci., 2009, vol. 14, pp. 563—573. https://doi.org/10.1016/j.tplants.2009.07.005

    Article  CAS  PubMed  Google Scholar 

  16. Adrian, J., Torti, S., and Turck, F., From decision to commitment: the molecular memory of flowering, Mol. Plant, 2009, vol. 2, pp. 628—642.

    Article  CAS  PubMed  Google Scholar 

  17. Andrés, F. and Coupland, G., The genetic basis of flowering responses to seasonal cues, Nat. Rev. Genet., 2012, vol. 13, pp. 627—639. https://doi.org/10.1038/nrg3291

    Article  CAS  PubMed  Google Scholar 

  18. De Lucia, F., Crevillen, P., Jones, A.M., et al., A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization, Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, no. 44, pp. 16831—16836. https://doi.org/10.1073/pnas.0808687105

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kim, D.H., Doyle, M.R., Sung, S., and Amasino, R.M., Vernalization: winter and the timing of flowering in plants, Annu. Rev. Cell Dev. Biol., 2009, vol. 25, pp. 277—299. https://doi.org/10.1146/annurev.cellbio.042308.113411

    Article  CAS  PubMed  Google Scholar 

  20. Jiang, D., Wang, Y., Wang, Y., and He, Y., Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb Repressive Complex 2 components, PLoS One, 2008, vol. 3, no. 10. e3404. https://doi.org/10.1371/journal.pone.0003404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Heo, J.B. and Sung, S., Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA, Science, 2011, vol. 331, no. 6013, pp. 76—79.https://doi.org/10.1126/science.1197349

  22. Lee, J., Yun, J.Y., Zhao, W., et al., A methyltransferase required for proper timing of the vernalization response in Arabidopsis, Proc. Natl. Acad. Sci. U.S.A., 2015, vol. 112, pp. 2269—2274. https://doi.org/10.1073/pnas.1423585112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kim, D.H. and Sung, S., Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis, Plant Cell, 2013, vol. 25, pp. 454—469. https://doi.org/10.1105/tpc.112.104760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Fedorenko, O.M., Gritskikh, M.V., and Nikolaevskaya, T.S., Polymorphism based on the onset of flowering in Arabidopsis thaliana (L.) Heynh. at the northern limit of the distribution range, in Trudy Karelskogo nauchnogo tsentra Rossiiskoi Akademii Nauk (Transactions of Karelian Research Centre of Russian Academy of Science), no. 2: Eksperimentalnaya biologiya (Experimental Biology), Petrozavodsk: Karel. Nauch. Tsentr Ross. Akad. Nauk, 2012, pp. 139—146.

  25. Kranz, A.R. and Kircheim, B., Genetic resources in Arabidopsis, AIS, 1987, vol. 24, p. 249.

    Google Scholar 

  26. Kurbidaeva, A.S., Zaretskaya, M.V., Soltabaeva, A.D., et al., Genetic base of Arabidopsis thaliana (L.) Heynh.: fitness of plants for extreme conditions in northern margins of species range, Russ. J. Genet., 2013, vol. 49, no. 8, pp. 819—826. https://doi.org/10.1134/S1022795413080097

    Article  CAS  Google Scholar 

  27. Ivanov, V.I., Kas’yanenko, A.G., Sanina, A.V., and Timofeeva-Resovskaya, E.A., Experiments on radiation genetics of Arabidopsis thaliana (L.) Heynh., Genetika (Moscow), 1966, no. 8, pp. 55—70.

  28. Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆Ct method, Methods, 2001, vol. 25, pp. 402—408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  Google Scholar 

  29. Eickelberg, G.J. and Fisher, A.J., Environmental regulation of plant gene expression: an RT-PCR laboratory project for an upper-level undergraduate biochemistry or molecular biology course, Biochem. Mol. Biol. Education., 2013, vol. 41, no. 5, pp. 325—333. https://doi.org/10.1002/bmb.20722

    Article  CAS  Google Scholar 

  30. Oliver, S.N., Finnegan, E.J., Dennis, E.S., et al., Vernalization induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION 1 gene, Proc. Natl. Acad. Sci. U.S.A., 2009, vol. 106, pp. 8386—8391. https://doi.org/10.1073/pnas.0903566106

  31. Banerjee, A. and Roychoudhury, A., The gymnastics of epigenomics in rice, Plant Cell Rep., 2017, vol. 37, no. 1, pp. 25—49. https://doi.org/10.1007/s00299-017-2192-2

  32. Choi, J., Hyun, Y., Kang, M.J., et al., Resetting and regulation of flowering locus C expression during Arabidopsis reproductive development, Plant J., 2009, vol. 57, pp. 918—931. https://doi.org/10.1111/j.1365-313X.2008.03776.x

    Article  CAS  PubMed  Google Scholar 

  33. Xing, D., Zhao, H., Xu, R., and Li, Q.Q., Arabidopsis PCFS4, a homologue of yeast polyadenylation factor Pcfl1p, regulates FCA alternative processing and promotes flowering time, Plant J., 2008, vol. 54, pp. 899—910. https://doi.org/10.1111/j.1365-313X.2008.03455.x

    Article  CAS  PubMed  Google Scholar 

  34. Klose, R.J., Yamane, K., Bae, Y., et al., The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36, Nature, 2006, vol. 442, pp. 312—316. https://doi.org/10.1038/nature04853

    Article  CAS  PubMed  Google Scholar 

  35. Turck, F. and Coupland, G., When vernalization makes sense, Science, 2011, vol. 331, pp. 36—37. https://doi.org/10.1126/science.1200786

    Article  CAS  PubMed  Google Scholar 

  36. Coustham, V., Li, P., Strange, A., et al., Quantitative modulation of Polycomb silencing underlies natural variation in vernalization, Science, 2012, vol. 337, pp. 584—587. https://doi.org/10.1126/science.1221881

    Article  CAS  PubMed  Google Scholar 

  37. Duncan, S., Holm, S., Questa, J., et al., Seasonal shift in timing of vernalization as an adaptation to extreme winter, ELIFE, 2015, vol. 23, no. 4. e06620. https://doi.org/10.7554/eLife.06620

    Article  Google Scholar 

Download references

Funding

The study was carried out under state order (project no. 0218-2019-0077).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. M. Fedorenko.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by N. Maleeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fedorenko, O.M., Topchieva, L.V., Zaretskaya, M.V. et al. Changes in FLC and VIN3 Expression during Vernalization of Arabidopsisthaliana Plants from Northern Natural Populations. Russ J Genet 55, 865–871 (2019). https://doi.org/10.1134/S1022795419060036

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795419060036

Keywords:

Navigation