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FLC: A key regulator of flowering time in Arabidopsis

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Abstract

The timing of floral transition has significant consequences for reproductive success in plants. The molecular genetic dissection of flowering time control in Arabidopsis identified an integrated network of pathways that quantitatively control this developmental switch. A central player in this process is the FLOWERING LOCUS C gene (FLC), which blocks flowering by inhibiting the genes required to switch the meristem from vegetative to floral development. Three systems (the FRIGIDA gene, vernalization, and the autonomous pathway) all influence the state of FLC. Last years many new genes have been identified that regulate FLC expression, and most of them are involved in the modification of FLC chromatin. This review focuses on recent insights in FLC regulation.

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Abbreviations

ChIP:

chromatin immunoprecipitation

FLC :

FLOWERING LOCUS C

FRI :

FRIGIDA

LD:

long day

NLS:

nuclear localization signal

PHD:

plant homeodomain

RRM:

RNA recognition motifs

siRNA:

short interfering RNA

WT:

wild type

References

  1. Koornneef, M., Alonso-Blanco, C., Peeters, A.J., 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. Simpson, G.G. and Dean, C., Arabidopsis, the Rosetta Stone of Flowering Time? Science, 2002, vol. 296, pp. 285–289.

    Article  CAS  PubMed  Google Scholar 

  3. Bäurle, I. and Dean, C., The Timing of Developmental Transitions in Plants, Cell, 2006, vol. 125, pp. 655–664.

    Article  PubMed  Google Scholar 

  4. Suárez-López, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and Coupland, G., CONSTANS Mediates between the Circadian Clock and the Control of Flowering in Arabidopsis, Nature, 2001, vol. 410, pp. 1116–1120.

    Article  PubMed  Google Scholar 

  5. Wilson, R.N., Heckman, J.W., and Somerville, C.R., Gibberellin Is Required for Flowering in Arabidopsis thaliana under Short Days, Plant Physiol., 1992, vol. 100, pp. 403–408.

    Article  CAS  PubMed  Google Scholar 

  6. Gómez-Mena, C., Pineiro, M., Franco-Zorrilla, J.M., Salinas, J., Coupland, G., and Martínez-Zapater, J.M., EARLY BOLTING IN SHORT DAYS: An Arabidopsis Mutation That Causes Early Flowering and Partially Suppresses the Floral Phenotype of Leafy, Plant Cell, 2001, vol. 13, pp. 1011–1024.

    Article  PubMed  Google Scholar 

  7. Sheldon, C.C., Finnegan, E.J., Rouse, D.T., Tadege, M., Bagnall, D.J., Helliwell, C.A., Peacock, W.J., and Dennis, E.S., The Control of Flowering by Vernalization, Curr. Opin. Plant Biol., 2000, vol. 3, pp. 418–422.

    Article  CAS  PubMed  Google Scholar 

  8. 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  Google Scholar 

  9. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and Dennis, E.S., The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation, Plant Cell, 1999, vol. 11, pp. 445–458.

    Article  CAS  PubMed  Google Scholar 

  10. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C., Molecular Analysis of FRIGIDA, a Major Determinant of Natural Variation in Arabidopsis Flowering Time, Science, 2000, vol. 290, pp. 344–347.

    Article  CAS  PubMed  Google Scholar 

  11. Helliwell, C.A., Wood, C.C., Robertson, M., Peacock, W.J., and Dennis, E.S., The Arabidopsis FLC Protein Interacts Directly In Vivo with SOC1 and FT Chromatin and Is Part of a High-Molecular-Weight Protein Complex, Plant J., 2006, vol. 46, pp. 183–192.

    Article  CAS  PubMed  Google Scholar 

  12. Ratcliffe, O.J., Kumimoto, R.W., Wong, B.J., and Riechmann, J.L., Analysis of the Arabidopsis MADS AFFECTING FLOWERING Gene Family: MAF2 Prevents Vernalization by Short Periods of Cold, Plant Cell, 2003, vol. 15, pp. 1159–1169.

    Article  CAS  PubMed  Google Scholar 

  13. Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L., and Riechmann, J.L., Regulation of Flowering in Arabidopsis by an FLC Homologue, Plant Physiol., 2001, vol. 126, pp. 122–132.

    Article  CAS  PubMed  Google Scholar 

  14. Michaels, S.D., Bezerra, I.C., and Amasino, R.M., FRIGIDA-Related Genes Are Required for the Winter-Annual Habit in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 3281–3285.

    Article  CAS  PubMed  Google Scholar 

  15. Schmitz, R.J., Hong, L., Michaels, S.D., and Amasino, R.M., FRIGIDA-ESSENTIAL 1 Interacts Genetically with FRIGIDA and FRIGIDA-LIKE 1 to Promote the Winter-Annual Habit of Arabidopsis thaliana, Development, 2005, vol. 132, pp. 5471–5478.

    Article  CAS  PubMed  Google Scholar 

  16. Kim, S.Y. and Michaels, S.D., SUPPRESSOR OF FRI 4 Encodes a Nuclear-Localized Protein That Is Required for Delayed Flowering in Winter-Annual Arabidopsis, Development, 2006, vol. 133, pp. 4699–4707.

    Article  CAS  PubMed  Google Scholar 

  17. He, Y., Doyle, M.R., and Amasino, R.M., PAF1-Complex-Mediated Histone Methylation of FLOWERING LOCUS C Chromatin Is Required for the Vernalization-Responsive, Winter-Annual Habit in Arabidopsis, Genes Dev., 2004, vol. 18, pp. 2774–2784.

    Article  CAS  PubMed  Google Scholar 

  18. Kim, S.Y., He, Y., Jacob, Y., Noh, Y.S., Michaels, S., and Amasino, R.M., Establishment of the Vernalization-Responsive, Winter-Annual Habit in Arabidopsis Requires a Putative Histone H3 Methyl Transferase, Plant Cell, 2005, vol. 17, pp. 3301–3310.

    Article  CAS  PubMed  Google Scholar 

  19. Zhao, Z., Yu, Y., Meyer, D., Wu, C., and Shen, W.H., Prevention of Early Flowering by Expression of FLOWERING LOCUS C Requires Methylation of Histone H3 K36, Nat. Cell Biol., 2005, vol. 7, pp. 1256–1260.

    Article  PubMed  Google Scholar 

  20. Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.P., Steinmetz, A., and Shen, W.H., Di- and Tribut Not Monomethylation on Histone H3 Lysine 36 Marks Active Transcription of Genes Involved in Flowering Time Regulation and Other Processes in Arabidopsis thaliana, Mol. Cell Biol., 2008, vol. 28, pp. 1348–1360.

    Article  CAS  PubMed  Google Scholar 

  21. Deal, R.B., Kandasamy, M.K., McKinney, E.C., and Meagher, R.B., The Nuclear Actin-Related Protein ARP6 Is a Pleiotropic Developmental Regulator Required for the Maintenance of FLOWERING LOCUS C Expression and Repression of Flowering in Arabidopsis, Plant Cell, 2005, vol. 17, pp. 2633–2646.

    Article  CAS  PubMed  Google Scholar 

  22. Choi, K., Kim, S., Kim, S.Y., Kim, M., Hyun, Y., Lee, H., Choe, S., Kim, S.G., Michaels, S., and Lee, I., SUPPRESSOR OF FRIGIDA 3 Encodes a Nuclear ACTIN-RELATED PROTEIN 6 Required for Floral Repression in Arabidopsis, Plant Cell, 2005, vol. 17, pp. 2647–2660.

    Article  CAS  PubMed  Google Scholar 

  23. Martin-Trillo, M., Lazaro, A., Poethig, R.S., Gómez-Mena, C., Pineiro, M.A., MartÍnez-Zapater, J.M., and Jarillo, J.A., EARLY IN SHORT DAYS 1 (ESD1) Encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a Putative Component of Chromatin Remodelling Complexes That Positively Regulates FLC Accumulation in Arabidopsis, Development, 2006, vol. 133, pp. 1241–1252.

    Article  CAS  PubMed  Google Scholar 

  24. Noh, Y.S. and Amasino, R.M., PIE1, an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis, Plant Cell, 2003, vol. 15, pp. 1671–1682.

    Article  CAS  PubMed  Google Scholar 

  25. Choi, K., Park, C., Lee, J., Oh, M., Noh, B., and Lee, I., Arabidopsis Homologs of Components of the SWR1 Complex Regulate Flowering and Plant Development, Development, 2007, vol. 134, pp. 1931–1941.

    Article  CAS  PubMed  Google Scholar 

  26. March-Diaz, R., Garcia-Dominguez, M., Florencio, F.J., and Reyes, J.C., SEF, a New Protein Required for Flowering Repression in Arabidopsis, Interacts with PIE1 and ARP6, Plant Physiol., 2007, vol. 143, pp. 893–901.

    Article  CAS  PubMed  Google Scholar 

  27. Deal, R.B., Topp, C.N., McKinney, E.C., and Meagher, R.B., Repression of Flowering in Arabidopsis Requires Activation of FLOWERING LOCUS C Expression by the Histone Variant H2A.Z, Plant Cell, 2007, vol. 19, pp. 74–83.

    Article  CAS  PubMed  Google Scholar 

  28. Pien, S., Fleury, D., Mylne, J.S., Crevillen, P., Inze, D., Avramova, Z., Dean, C., and Grossniklaus, U., ARABI-DOPSIS TRITHORAX1 Dynamically Regulates FLOWERING LOCUS C Activation via Histone 3 Lysine 4 Trimethylation, Plant Cell, 2008, vol. 20, pp. 580–588.

    Article  CAS  PubMed  Google Scholar 

  29. Rivera, B.B., Ruzicka, D.R., Deal, R.B., McKinney, E.C., Reid, L.K., and Meagher, R.B., ACTIN DEPOLYMERIZING FACTOR9 Controls Development and Gene Expression in Arabidopsis, Plant Mol. Biol., 2008, vol. 68, pp. 619–632.

    Article  Google Scholar 

  30. Gu, X., Jiang, D., Wang, Y., Bachmair, A., and He, Y., Repression of the Floral Transition via Histone H2B Monoubiquitination, Plant J., 2008, vol. 57, pp. 522–533.

    Article  PubMed  Google Scholar 

  31. Cao, Y., Da, Y., Cui, S., and Ma, L., Histone H2B Monoubiquitination in the Chromatin of FLOWERING LOCUS C Regulates Flowering Time in Arabidopsis, Plant Cell, 2008, vol. 20, pp. 2586–2602.

    Article  CAS  PubMed  Google Scholar 

  32. Xu, L., Menard, R., Berr, A., Fuchs, J., Cognat, V., Meyer, D., and Shen, W.H., The E2 Ubiquitin-Conju gating Enzymes, AtUBC1 and AtUBC2, Play Redundant Roles and Are Involved in Activation of FLC Expression and Repression of Flowering in Arabidopsis thaliana, Plant J., 2008, vol. 57, pp. 279–288.

    Article  PubMed  Google Scholar 

  33. Gendall, A.R., Levy, Y.Y., Wilson, A., and Dean, C., The VERNALIZATION 2 Gene Mediates the Epigenetic Regulation of Vernalization in Arabidopsis, Cell, 2001, vol. 107, pp. 525–535.

    Article  CAS  PubMed  Google Scholar 

  34. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R., and Dean, C., Multiple Roles of Arabidopsis VRN1 in Vernalization and Flowering Time Control, Science, 2002, vol. 297, pp. 243–246.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Sung, S., Schmitz, R.J., and Amasino, R.M., A PHD Finger Protein Involved in Both the Vernalization and Photoperiod Pathways in Arabidopsis, Genes Dev., 2006, vol. 20, pp. 3244–3248.

    Article  CAS  PubMed  Google Scholar 

  37. Wood, C.C., Robertson, M., Tanner, G., Peacock, W.J., Dennis, E.S., and Helliwell, C.A., The Arabidopsis thaliana Vernalization Response Requires a Polycomb-Like Protein Complex That Also Includes VERNALIZATION INSENSITIVE 3, Proc. Natl. Acad. Sci. USA, 2006, vol. 103, pp. 14 631–14 636.

    Google Scholar 

  38. De Lucia, F., Crevillen, P., Jones, A.M., Greb, T., and Dean, C., A PHD-Polycomb Repressive Complex 2 Triggers the Epigenetic Silencing of FLC during Vernalization, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 16 831–16 836.

    Google Scholar 

  39. Sung, S.B., He, Y.H., Eshoo, T.W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S.E., and Amasino, R.M., Epigenetic Maintenance of the Vernalized State in Arabidopsis thaliana Requires LIKE HETEROCHROMATIN PROTEIN 1, Nat. Genet., 2006, vol. 38, pp. 706–710.

    Article  CAS  PubMed  Google Scholar 

  40. Schmitz, R.J., Sung, S., and Amasino, R.M., Histone Arginine Methylation Is Required for Vernalization-Induced Epigenetic Silencing of FLC in Winter-Annual Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 411–416.

    Article  CAS  PubMed  Google Scholar 

  41. Lee, I., Aukerman, M.J., Gore, S.L., Lohman, K.N., Michaels, S.D., Weaver, L.M., John, M.C., Feldmann, K.A., and Amasino, R.M., Isolation of LUMINIDEPENDENS: A Gene Involved in the Control of Flowering Time in Arabidopsis, Plant Cell, 1994, vol. 6, pp. 75–83.

    Article  CAS  PubMed  Google Scholar 

  42. Aukerman, M., Lee, I., Weigel, D., and Amasino, R.M., The Arabidopsis Flowering-Time Gene LUMINIDE-PENDENS Is Expressed Primarily in Regions of Cell Proliferation and Encodes a Nuclear Protein That Regulates LEAFY Expression, Plant J., 1999, vol. 18, pp. 195–203.

    Article  CAS  PubMed  Google Scholar 

  43. Schomburg, F.M., Patton, D.A., Meinke, D.W., and Amasino, R.M., FPA, a Gene Involved in Floral Induction in Arabidopsis, Encodes a Protein Containing RNA-Recognition Motifs, Plant Cell, 2001, vol. 13, pp. 1427–1436.

    Article  CAS  PubMed  Google Scholar 

  44. Lim, M.H., Kim, J., Kim, Y.S., Chung, K.S., Seo, Y.H., Lee, I., Kim, I., Kim, J., Hong, C.B., Kim, H.J., and Park, C.M., A New Arabidopsis Gene, FLK, Encodes an RNA Binding Protein with K Homology Motifs and Regulates Flowering via FLOWERING LOCUS C, Plant Cell, 2004, vol. 16, pp. 731–740.

    Article  CAS  PubMed  Google Scholar 

  45. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., and Dean, C., FCA, a Gene Controlling Flowering Time in Arabidopsis, Encodes a Protein Containing RNA-Binding Domains, Cell, 1997, vol. 89, pp. 737–745.

    Article  CAS  PubMed  Google Scholar 

  46. Simpson, G.G., Dijkwel, P.P., Quesada, V., Henderson, I., and Dean, C., FY Is an RNA 3′-End Processing Factor That Interacts with FCA to Control the Arabidopsis Floral Transition, Cell, 2003, vol. 13, pp. 777–787.

    Article  Google Scholar 

  47. Xing, D., Zhao, H., Xu, R., and Li, Q.Q., Arabidopsis PCFS4, a Homologue of Yeast Polyadenylation Factor Pcf11p, Regulates FCA Alternative Processing and Promotes Flowering Time, Plant J., 2008, vol. 54, pp. 899–910.

    Article  CAS  PubMed  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. Ausin, L., Alonso-Blanco, C., and Martínez-Zapater, J.M., Regulation of Flowering Time by FVE, a Retinobastoma-Associated Protein, Nat. Genet., 2004, vol. 36, pp. 162–166.

    Article  CAS  PubMed  Google Scholar 

  50. Jin, J.B., Jin, Y.H., Lee, J., Miura, K., Yoo, C.Y., Kim, W.Y., Oosten, M.V., Hyun, Y., Somers, D.E., Lee, I., Yun, D.J., Bressanand, R.A., and Hasegawa, P.M., The SUMO E3 Ligase, AtSIZ1, Regulates Flowering by Controlling a Salicylic Acid-Mediated Floral Promotion Pathway and through Affects on FLC Chromatin Structure, Plant J., 2008, vol. 53, pp. 530–540.

    Article  CAS  PubMed  Google Scholar 

  51. Noh, B., Lee, S.H., Kim, H.J., Yi, G., Shin, E.A., Lee, M., Jung, K.J., Doyle, M.R., Amasino, R.M., and Noh, Y.S., Divergent Roles of a Pair of Homologous Jumonji/Zinc-Finger-Class Transcription Factor Proteins in the Regulation of Arabidopsis Flowering Time, Plant Cell, 2004, vol. 16, pp. 2601–2613.

    Article  CAS  PubMed  Google Scholar 

  52. Klose, R.J., Yamane, K., Bae, Y., Zhang, D., Erdjument-Bromage, H., Tempst, P., Wong, J., and Zhang, Y., The Transcriptional Repressor JHDM3A Demethylates Trimethyl Histone H3 Lysine 9 and Lysine 36, Nature, 2006, vol. 442, pp. 312–316.

    Article  CAS  PubMed  Google Scholar 

  53. Swiezewski, S., Crevillen, P., Liu, F., Ecker, J.R., Jerzmanowski, A., and Dean, C., Small RNA-Mediated Chromatin Silencing Directed to the 3′ Region of the Arabidopsis Gene Encoding the Developmental Regulator, FLC, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 3633–3638.

    Article  CAS  PubMed  Google Scholar 

  54. Schmitz, R.J., Hong, L., Fitzpatrickand, K.E., and Amasino, R.M., DICER-LIKE1 and DICER-LIKE3 Redundantly Act to Promote Flowering via Repression of FLOWERING LOCUS C in Arabidopsis thaliana, Genetics, 2007, vol. 176, pp. 1359–1362.

    Article  CAS  PubMed  Google Scholar 

  55. Deng, W.W., Liu, C.Y., Pei, Y.X., Deng, X., Niu, L.F., and Cao, X.F., Involvement of the Histone Acetyltransferase AtHAC1 in the Regulation of Flowering Time via Repression of FLOWERING LOCUS C in Arabidopsis, Plant Physiol., 2007, vol. 143, pp. 1660–1668.

    Article  CAS  PubMed  Google Scholar 

  56. Wu, K., Zhang, L., Zhou, C., Yu, C., and Chaikam, V., HDA6 Is Required for Jasmonate Response, Senes cence and Flowering in Arabidopsis, J. Exp. Bot., 2008, vol. 59, pp. 225–234.

    Article  CAS  PubMed  Google Scholar 

  57. Jiang, D., Yang, W., He, Y., and Amasino, R.M., Arabidopsis Relatives of the Human Lysine-Specific Demethylase 1 Repress the Expression of FWA and FLOWERING LOCUS C and Thus Promote the Floral Transition, Plant Cell, 2008, vol. 19, pp. 2975–2987.

    Article  Google Scholar 

  58. Niu, L., Zhang, Y., Pei, Y., Liu, C., and Cao, X., Redundant Requirement for a Pair of PROTEIN ARGININE METHYLTRANSFERASE4 Homologs for the Proper Regulation of Arabidopsis Flowering Time, Plant Physiol., 2008, vol. 148, pp. 490–503.

    Article  CAS  PubMed  Google Scholar 

  59. He, Y.H. and Amasino, R.M., Role of Chromatin Modification in Flowering-Time Control, Trends Plant Sci., 2005, vol. 10, pp. 30–35.

    Article  CAS  PubMed  Google Scholar 

  60. Farrona, S., Coupland, G., and Turck, F., The Impact of Chromatin Regulation on the Floral Transition, Semin. Cell Dev. Biol., 2008, vol. 19, pp. 560–573.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. MOE Key Laboratory of Arid and Grassland Ecology, Institute of Cell Biology, Life Science School, Lanzhou University, Gansu, 730000, China

    Zhiqiang Yan, Dawei Liang, Heng Liu & Guochang Zheng

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  1. Zhiqiang Yan
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  2. Dawei Liang
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  3. Heng Liu
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  4. Guochang Zheng
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Correspondence to Heng Liu.

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Published in Russian in Fiziologiya Rastenii, 2010, Vol. 57, No.2, pp. 177–185.

This text was submitted by the authors in English.

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Yan, Z., Liang, D., Liu, H. et al. FLC: A key regulator of flowering time in Arabidopsis. Russ J Plant Physiol 57, 166–174 (2010). https://doi.org/10.1134/S1021443710020020

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