Arabidopsis MSI1 functions in photoperiodic flowering time control

Frontiers in Plant Science

Volumn 5, Issue MAR, 2014, Pages

  Steinbach, Yvonne ^a   Hennig, Lars ^b  

^a ETH ZURICH   (Switzerland)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Arabidopsis; Chromatin; CONSTANS (CO); FLOWERING LOCUS T (FT); Flowering time; MSI1; Photoperiod

Indexed keywords

EID: 84901068710     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00077     Document Type: Article

References (74)

1. Alexandre, C., Möller-Steinbach, Y., Schönrock, N., Gruissem, W., and Hennig, L. (2009). Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol. Plant 2, 675-687. doi: 10.1093/mp/ssp012
2. Andres, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. doi: 10.1038/nrg3291
3. Ausin, I., Alonso-Blanco, C., Jarillo, J. A., Ruiz-Garcia, L., and Martinez-Zapater, J. M. (2004). Regulation of flowering time by FVE, a Retinoblastoma-associated protein. Nat. Genet. 36, 162-166. doi: 10.1038/ng1295
4. Bäckström, S., Elfving, N., Nilsson, R., Wingsle, G., and Björklund, S. (2007). Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol. Cell 26, 717-729. doi: 10.1016/j.molcel.2007.05.007
5. Baurle, I., Smith, L., Baulcombe, D. C., and Dean, C. (2007). Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318, 109-112. doi: 10.1126/science.1146565
6. Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K., et al. (2000). A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591-599. doi: 10.1046/j.1365-313x.2000.00906.x
7. Bouveret, R., Schönrock, N., Gruissem, W., and Hennig, L. (2006). Regulation of flowering time by Arabidopsis MSI1. Development 133, 1693-1702. doi: 10.1242/dev.02340
8. Cerdan, P. D., and Chory, J. (2003). Regulation of flowering time by light quality. Nature 423, 881-885. doi: 10.1038/nature01636
9. Choi, K., Park, C., Lee, J., Oh, M., Noh, B., and Lee, I. (2007). Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134, 1931-1941. doi: 10.1242/dev.001891
10. Clarke, J. H., and Dean, C. (1994). Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol. Gen. Genet. 242, 81-89.
11. Corbesier, L., Gadisseur, I., Silvestre, G., Jacqmard, A., and Bernier, G. (1996). Design in Arabidopsis thaliana of a synchronous system of floral induction by one long day. Plant J. 9, 947-952. doi: 10.1046/j.1365-313X.1996.9060947.x
12. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., et al. (2007). FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033. doi: 10.1126/science.1141752
13. De Lucia, F., Crevillen, P., Jones, A. M., Greb, T., and Dean, C. (2008). A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc. Natl. Acad. Sci. U.S.A. 105, 16831-16836. doi: 10.1073/pnas.0808687105
14. Derkacheva, M., Steinbach, Y., Wildhaber, T., Mozgova, I., Mahrez, W., Nanni, P., et al. (2013). Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 32, 2073-2085. doi: 10.1038/emboj.2013.145
15. Dumbliauskas, E., Lechner, E., Jaciubek, M., Berr, A., Pazhouhandeh, M., Alioua, M., et al. (2011). The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J. 30, 731-743. doi: 10.1038/emboj.2010.359
16. Elfving, N., Davoine, C., Benlloch, R., Blomberg, J., Brännström, K., Müller, D., et al. (2011). The Arabidopsis thaliana Med25 mediator subunit integrates environmental cues to control plant development. Proc. Natl. Acad. Sci. U.S.A. 108, 8245-8250. doi: 10.1073/pnas.1002981108
17. Exner, V., Aichinger, E., Shu, H., Wildhaber, T., Alfarano, P., Caflisch, A., et al. (2009). The Chromodomain of LIKE HETERO-CHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS ONE 4:e5335. doi: 10.1371/journal.pone.0005335
18. Exner, V., Alexandre, C., Rosenfeldt, G., Alfarano, P., Nater, M., Caflisch, A., et al. (2010). A gain-of-function mutation of Arabidopsis cryptochrome1 promotes flowering. Plant Physiol. 154, 1633-1645. doi: 10.1104/pp.110.160895
19. Exner, V., Taranto, P., Schonrock, N., Gruissem, W., and Hennig, L. (2006). Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 133, 4163-4172. doi: 10.1242/dev.02599
20. Guitton, A. E., and Berger, F. (2005). Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in Arabidopsis. Curr. Biol. 15, 750-754. doi: 10.1016/j.cub.2005.02.066
21. Guitton, A. E., Page, D. R., Chambrier, P., Lionnet, C., Faure, J. E., Grossniklaus, U., et al. (2004). Identification of new members of fertilisation independent seed polycomb group pathway involved in the control of seed development in Arabidopsis thaliana. Development 131, 2971-2981. doi: 10.1242/dev.01168
22. Halliday, K. J., and Whitelam, G. C. (2003). Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiol. 131, 1913-1920. doi: 10.1104/pp.102.018135
23. Hennig, L., Bouveret, R., and Gruissem, W. (2005). MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol. 15, 295-302. doi: 10.1016/j.tcb.2005.04.004
24. Hennig, L., Taranto, P., Walser, M., Schönrock, N., and Gruissem, W. (2003). Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130, 2555-2565. doi: 10.1242/dev.00470
25. Hepworth, S. R., Valverde, F., Ravenscroft, D., Mouradov, A., and Coupland, G. (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327-4337. doi: 10.1093/emboj/cdf432
26. Imaizumi, T., Schultz, T. F., Harmon, F. G., Ho, L. A., and Kay, S. A. (2005). FKF1 F-Box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309, 293-297. doi: 10.1126/science.1110586
27. Iñigo, S., Alvarez, M. J., Strasser, B., Califano, A., and Cerdán, P. D. (2012a). PFT1, the MED25 subunit of the plant Mediator complex, promotes flowering through CONSTANS dependent and independent mechanisms in Arabidopsis. Plant J. 69, 601-612. doi: 10.1111/j.1365-313X.2011.04815.x
28. Iñigo, S., Giraldez, A. N., Chory, J., and Cerdán, P. D. (2012b). Proteasome-mediated turnover of Arabidopsis MED25 is coupled to the activation of FLOWERING LOCUS T transcription. Plant Physiol. 160, 1662-1673. doi: 10.1104/pp.112.205500
29. Jarillo, J. A., and Piñeiro, M. (2011). Timing is everything in plant development. The central role of floral repressors. Plant Sci. 181, 364-378. doi: 10.1016/j.plantsci.2011.06.011
30. Jeon, J., and Kim, J. (2011). FVE, an Arabidopsis homologue of the retinoblastoma-associated protein that regulates flowering time and cold response, binds to chromatin as a large multiprotein complex. Mol. Cells. 32, 227-234. doi: 10.1007/s10059-011-1022-6
31. Jiang, D., Wang, Y., Wang, Y., and He, Y. (2008). Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis polycomb repressive complex 2 components. PLoS ONE 3:e3404. doi: 10.1371/journal.pone.0003404
32. Jullien, P. E., Mosquna, A., Ingouff, M., Sakata, T., Ohad, N., and Berger, F. (2008). Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 6:e194. doi: 10.1371/journal.pbio.0060194
33. Kardailsky, I., Shukla, V. K., Ahn, J. H., Dagenais, N., Christensen, S. K., Nguyen, J. T., et al. (1999). Activation tagging of the floral inducer FT. Science 286, 1962-1965. doi: 10.1126/science.286.5446.1962
34. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. doi: 10.1016/S1360-1385(02)02251-3
35. Kaya, H., Shibahara, K. I., Taoka, K. I., Iwabuchi, M., Stillman, B., and Araki, T. (2001). FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142. doi: 10.1016/S0092-8674(01)00197-0
36. Kidd, B. N., Edgar, C. I., Kumar, K. K., Aitken, E. A., Schenk, P. M., Manners, J. M., et al. (2009). The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21, 2237-2252. doi: 10.1105/tpc.109.066910
37. Kim, H. J., Hyun, Y., Park, J. Y., Park, M. J., Park, M. K., Kim, M. D., et al. (2004). A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 36, 167-171. doi: 10.1038/ng1298
38. Kim, S. Y., Yu, X., and Michaels, S. D. (2008). Regulation of CONSTANS and FLOWERING LOCUS T expression in response to changing light quality. Plant Physiol. 148, 269-279 doi: 10.1104/pp.108.122606
39. King, R. W., Hisamatsu, T., Goldschmidt, E. E., and Blundell, C. (2008). The nature of floral signals in Arabidopsis. I. Photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T (FT). J. Exp. Bot. 59, 3811-3820. doi: 10.1093/jxb/ern231
40. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M., and Araki, T. (1999). A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960-1962. doi: 10.1126/science.286.5446.1960
41. Köhler, C., Hennig, L., Bouveret, R., Gheyselinck, J., Grossniklaus, U., and Gruissem, W. (2003). Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 22, 4804-4814. doi: 10.1093/emboj/cdg444
42. Koornneef, M., Hanhart, C. J., and Van Der Veen, J. H. (1991). A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol. Gen. Genet. 229, 57-66. doi: 10.1007/BF00264213
43. Lazaro, A., Gomez-Zambrano, A., Lopez-Gonzalez, L., Pineiro, M., and Jarillo, J. A. (2008). Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development. J. Exp. Bot. 59, 653-666. doi: 10.1093/jxb/erm332
44. Lee, H., Suh, S. S., Park, E., Cho, E., Ahn, J. H., Kim, S. G., et al. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376. doi: 10.1101/gad.813600
45. Lee, I., and Amasino, R. M. (1995). Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108, 157-162.
46. Lee, I., Bleecker, A., and Amasino, R. (1993). Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237, 171-176.
47. Leroy, O., Hennig, L., Breuninger, H., Laux, T., and Köhler, C. (2007). Polycomb group proteins function in the female gametophyte to determine seed development in plants. Development 134, 3639-3648. doi: 10.1242/dev.009027
48. Martin-Trillo, M., Larazo, A., Poethig, R. S., Gomez-Mena, C., Piñeiro, M. A., Martinez-Zapater, J. M., et al. (2006). 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 133, 1241-1252. doi: 10.1242/dev.02301
49. Mayfield, J. D., Folta, K. M., Paul, A. L., and Ferl, R. J. (2007). The 14-3-3 Proteins μ and υ influence transition to flowering and early phytochrome response. Plant Physiol. 145, 1692-1702. doi: 10.1104/pp.107.108654
50. Michaels, S. D., and Amasino, R. M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956.
51. Michaels, S. D., and Amasino, R. M. (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, 935-941. doi: 10.1105/tpc.13.4.935
52. Möller-Steinbach, Y., Alexandre, C., and Hennig, L. (2010). Flowering time control. Methods Mol. Biol. 655, 229-237. doi: 10.1007/978-1-60761-765-5_15
53. Putterill, J., Robson, F., Lee, K., Simon, R., and Coupland, G. (1995). The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847-857. doi: 10.1016/0092-8674(95)90288-0
54. Redei, G. P. (1962). Supervital mutants of Arabidopsis. Genetics 47, 443-460.
55. Robson, F., Costa, M. M., Hepworth, S. R., Vizir, I., Pineiro, M., Reeves, P. H., et al. (2001). Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J. 28, 619-631. doi: 10.1046/j.1365-313x.2001.01163.x
56. Ruckle, M. E., Demarco, S. M., and Larkin, R. M. (2007). Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19, 3944-3960. doi: 10.1105/tpc.107.054312
57. Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, M. F., et al. (2000). Distinct roles of CONSTANS target genes in reproductive develop-ment of Arabidopsis. Science 288, 1613-1616. doi: 10.1126/science.288.5471.1613
58. Sawa, M., and Kay, S. A. (2011). GIGANTEA directly activates FLOWERING LOCUS T in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 108, 11698-11703. doi: 10.1073/pnas.1106771108
59. Sawa, M., Nusinow, D. A., Kay, S. A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for Day-Length measurement in Arabidopsis. Science 318, 261-265. doi: 10.1126/science.1146994
60. Schönrock, N., Bouveret, R., Leroy, O., Borghi, L., Köhler, C., Gruissem, W., et al. (2006a). Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev. 20, 1667-1678. doi: 10.1101/gad.377206
61. Schönrock, N., Exner, V. Probst, A., Gruissem, W., and Hennig, L. (2006b). Functional genomic analysis of CAF-1 mutants in Arabidopsis thaliana. J. Biol. Chem. 281, 9560-9568 doi: 10.1074/jbc.M513426200
62. Searle, I., and Coupland, G. (2004). Induction of flowering by seasonal changes in photoperiod. EMBO J. 23, 1217-1222. doi: 10.1038/sj.emboj.7600117
63. Simpson, G. G. (2004). The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol. 7, 570-574. doi: 10.1016/j.pbi.2004.07.002
64. Srikanth, A., and Schmid, M. (2011). Regulation of flowering time: all roads lead to Rome. Cell. Mol. Life Sci. 68, 2013-2037. doi: 10.1007/s00018-011-0673-y
65. Suarez-Lopez, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and Coupland, G. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116-1120. doi: 10.1038/35074138
66. Thomas, B. (2006). Light signals and flowering. J. Exp. Bot. 57, 3387-3393. doi: 10.1093/jxb/erl071
67. Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coupland, G. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006. doi: 10.1126/science.1091761
68. Wollenberg, A. C., Strasser, B., Cerdan, P. D., and Amasino, R. M. (2008). Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol. 148, 1681-1694 doi: 10.1104/pp.108.125468
69. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M., and Araki, T. (2005). TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol. 46, 1175-1189. doi: 10.1093/pcp/pci151
70. Yanovsky, M. J., and Kay, S. A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308-312. doi: 10.1038/nature00996
71. Yoo, S. K., Chung, K. S., Kim, J., Lee, J. H., Hong, S. M., Yoo, S. J., et al. (2005). CONSTANS Activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol. 139, 770-778. doi: 10.1104/pp.105.066928
72. Yoshida, N., Yanai, Y., Chen, L., Kato, Y., Hiratsuka, J., Miwa, T., et al. (2001). EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13, 2471-2481.
73. Zeevaart, J. A. (2008). Leaf-produced floral signals. Curr. Opin. Plant Biol. 11, 541-547. doi: 10.1016/j.pbi.2008.06.009
74. Zografos, B. R., and Sung, S. (2012). Vernalization-mediated chromatin changes. J. Exp. Bot. 63, 4343-4348. doi: 10.1093/jxb/ers157