journal article May 01, 2003

Analysis of the ArabidopsisMADS AFFECTING FLOWERINGGene Family:MAF2Prevents Vernalization by Short Periods of Cold [W]

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Abstract
AbstractThe Arabidopsis FLOWERING LOCUS C (FLC) gene is a key floral repressor in the maintenance of a vernalization response. In vernalization-sensitive genetic backgrounds, FLC levels are high, and they decline after exposure to long cold periods. Four FLC paralogs (MAF2 [MADS AFFECTING FLOWERING2] to MAF5) are arranged in a tandem array on the bottom of Arabidopsis chromosome V. We used a reverse genetics approach to analyze their functions. Loss-of-function and gain-of-function studies indicate that MAF2 acts as a floral repressor. In particular, maf2 mutant plants display a pronounced vernalization response when subjected to relatively short cold periods, which are insufficient to elicit a strong flowering response in the wild type, despite producing a large reduction in FLC levels. MAF2 expression is less sensitive to vernalization than that of FLC, and its repressor activity is exerted independently or downstream of FLC transcription. Thus, MAF2 can prevent premature vernalization in response to brief cold spells. Overexpression of MAF3 or MAF4 produces alterations in flowering time that suggest that these genes also act as floral repressors and might contribute to the maintenance of a vernalization requirement. However, the final gene in the cluster, MAF5, is upregulated by vernalization. Therefore, MAF5 could play an opposite role to FLC in the vernalization response.
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References
49
[1]
Alvarez-Buylla, E.R., Liljegren, S.J., Pelaz, S., Gold, S.E., Burgeff, C., Ditta, G.S., Vergara-Silva, F., and Yanofsky, M.F. (2000a). MADS-box gene evolution beyond flowers: Expression in pollen, endosperm, guard cells, roots and trichomes. Plant J.  24  ,  457–466. 10.1046/j.1365-313x.2000.00891.x
[2]
Alvarez-Buylla, E.R., Pelaz, S., Liljegren, S.J., Gold, S.E., Burgeff, C., Ditta, G.S., Ribas de Pouplana, L., Martinez-Castilla, L., and Yanofsky, M.F. (2000b). An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci. USA  97  ,  5328–5333. 10.1073/pnas.97.10.5328
[3]
Bagnall, D.J. (1992). Control of flowering in Arabidopsis thaliana by light, vernalization and gibberellins. Aust. J. Plant Physiol.  19  ,  401–409.
[4]
Bechtold, N., and Pelletier, G. (1998). In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol. Biol.  82  ,  259–266.
[5]
Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K., and Melzer, S. (2000). A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J.  24  ,  591–599. 10.1046/j.1365-313x.2000.00906.x
[6]
Burn, J.E., Bagnall, D.J., Metzger, J.D., Dennis, E.S., and Peacock, W.J. (1993). DNA methylation, vernalization, and the initiation of flowering. Proc. Natl. Acad. Sci. USA  90  ,  287–291. 10.1073/pnas.90.1.287
[7]
Chandler, J., Wilson, A., and Dean, C. (1996). Arabidopsis mutants showing an altered response to vernalization. Plant J.  10  ,  637–644. 10.1046/j.1365-313x.1996.10040637.x
[8]
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. 10.1007/bf00277351
[9]
Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J.  16  ,  735–743. 10.1046/j.1365-313x.1998.00343.x
[10]
Gendall, A.R., Levy, Y.Y., Wilson, A., and Dean, C. (2001). The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell  107  ,  525–535. 10.1016/s0092-8674(01)00573-6
[11]
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. 10.1093/emboj/cdf432
[12]
Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C. (2000). Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science  290  ,  344–347. 10.1126/science.290.5490.344
[13]
Jones, A., Davies, H.M., and Voelker, T.A. (1995). Palmitoyl-acyl carrier protein (ACP) thioesterase and the evolutionary origin of plant acyl-ACP thioesterases. Plant Cell  7  ,  359–371.
[14]
Koornneef, M., Alonso-Blanco, C., Blankestijn-de Vries, H., Hanhart, C.J., and Peeters, A.J. (1998a). Genetic interactions among late-flowering mutants of Arabidopsis. Genetics  148  ,  885–892. 10.1093/genetics/148.2.885
[15]
Koornneef, M., Alonso-Blanco, C., Peeters, A.J.M., and Soppe, W. (1998b). Genetic control of flowering time in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol.  49  ,  345–370. 10.1146/annurev.arplant.49.1.345
[16]
Koornneef, M., Blankestijn-de Vries, H., Hanhart, C., Soppe, W., and Peeters, A.J. (1994). The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J.  6  ,  911–919. 10.1046/j.1365-313x.1994.6060911.x
[17]
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. 10.1007/bf00264213
[18]
Lee, H., Suh, S.-S., Park, E., Cho, E., Ahn, J.H., Kim, S.-G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev.  14  ,  2366–2376. 10.1101/gad.813600
[19]
Lee, I., Bleecker, A., and Amasino, R. (1993). Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet.  237  ,  171–176. 10.1007/bf00282798
[20]
Lee, I., Michaels, S.D., Masshardt, A.S., and Amasino, R.M. (1994). The late-flowering phenotype of FRIGIDA and mutations in LUMINI-DEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J.  6  ,  903–909. 10.1046/j.1365-313x.1994.6060903.x
[21]
Levy, Y.Y., and Dean, C. (1998). The transition to flowering. Plant Cell  10  ,  1973–1990.
[22]
Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R., and Dean, C. (2002). Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science  297  ,  243–246. 10.1126/science.1072147
[23]
Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C., and Dean, C. (1997). FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell  89  ,  737–745. 10.1016/s0092-8674(00)80256-1
[24]
Macknight, R., Duroux, M., Laurie, R., Dijkwel, P., Simpson, G., and Dean, C. (2002). Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell  14  ,  877–888. 10.1105/tpc.010456
[25]
Martinez-Zapater, J.M., Coupland, G., Dean, C., and Koornneef, M. (1994). The transition to flowering in Arabidopsis. In Arabidopsis, E.M. Meyerowitz and C.R. Somerville, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 403–433.
[26]
Martinez-Zapater, J.M., and Somerville, C.R. (1990). Effect of light quality and vernalization on late flowering mutants of Arabidopsis thaliana. Plant Physiol.  92  ,  770–776. 10.1104/pp.92.3.770
[27]
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. 10.1105/tpc.11.5.949
[28]
Michaels, S.D., and Amasino, R.M. (2000). Memories of winter: Vernalization and the competence to flower. Plant Cell Environ.  23  ,  1145–1153. 10.1046/j.1365-3040.2000.00643.x
[29]
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. 10.1105/tpc.13.4.935
[30]
Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant.  15  ,  473  –497.
[31]
Napp-Zinn, K. (1957). Untersuchungen zur genetik des kaltebedurfnisses bei Arabidopsis thaliana (L.) Heynh. Z. Indukt. Abstammungs Vererbungsl.  88  ,  253–285.
[32]
Onouchi, H., Igeño, M.I., Perilleux, C., Graves, K., and Coupland, G. (2000). Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell  12  ,  885–900. 10.1105/tpc.12.6.885
[33]
Page, T., Macknight, R., Yang, C.H., and Dean, C. (1999). Genetic interactions of the Arabidopsis flowering time gene FCA with genes regulating floral initiation. Plant J.  17  ,  231–239. 10.1046/j.1365-313x.1999.00364.x
[34]
Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L., and Riechmann, J.L. (2001). Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol.  126  ,  122–132. 10.1104/pp.126.1.122
[35]
Ratcliffe, O.J., and Riechmann, J.L. (2002). Arabidopsis transcription factors and the regulation of flowering time: A genomic perspective. Curr. Issues Mol. Biol.  4  ,  77–91.
[36]
Reeves, P.H., and Coupland, G. (2000). Response of plant development to environment: Control of flowering by daylength and temperature. Curr. Opin. Plant Biol.  3  ,  37–42. 10.1016/s1369-5266(99)00041-2
[37]
Reeves, P.H., Murtas, G., Dash, S., and Coupland, G. (2002). Early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC. Development  129  ,  5349–5361. 10.1242/dev.00113
[38]
Rouse, D.T., Sheldon, C.C., Bagnall, D.J., Peacock, W.J., and Dennis, E.S. (2002). FLC, a repressor of flowering, is regulated by genes in different inductive pathways. Plant J.  29  ,  183–191. 10.1046/j.0960-7412.2001.01210.x
[39]
Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science  288  ,  1613–1616. 10.1126/science.288.5471.1613
[40]
Sanda, S.L., and Amasino, R.M. (1996). Interaction of FLC and late-flowering mutations in Arabidopsis thaliana. Mol. Gen. Genet.  251  ,  69–74.
[41]
Schomburg, F.M., Patton, D.A., Meinke, D.W., and Amasino, R.M. (2001). FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell  13  ,  1427–1436.
[42]
Scortecci, K.C., Michaels, S.D., and Amasino, R.M. (2001). Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J.  26  ,  229–236. 10.1046/j.1365-313x.2001.01024.x
[43]
Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and Dennis, E.S. (1999). The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell  11  ,  445–458. 10.1105/tpc.11.3.445
[44]
Sheldon, C.C., Conn, A.B., Dennis, E.S., and Peacock, W.J. (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. 10.1105/tpc.004564
[45]
Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J., and Dennis, E.S. (2000). The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA  97  ,  3753–3758. 10.1073/pnas.97.7.3753
[46]
Simpson, G.G., and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time? Science  296  ,  285–289. 10.1126/science.296.5566.285
[47]
Simpson, G.G., Gendall, A.R., and Dean, C. (1999). When to switch to flowering. Annu. Rev. Cell Dev. Biol.  15  ,  519–550. 10.1146/annurev.cellbio.15.1.519
[48]
Vince-Prue, D. (1975). Vernalization. In Photoperiodism in Plants. (London: McGraw-Hill), pp. 263–291.
[49]
Zhang, H., and van Nocker, S. (2002). The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C. Plant J.  31  ,  663–673. 10.1046/j.1365-313x.2002.01380.x
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Published
May 01, 2003
Vol/Issue
15(5)
Pages
1159-1169
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Oliver J. Ratcliffe, Roderick W. Kumimoto, Becky J. Wong, et al. (2003). Analysis of the ArabidopsisMADS AFFECTING FLOWERINGGene Family:MAF2Prevents Vernalization by Short Periods of Cold [W]. The Plant Cell, 15(5), 1159-1169. https://doi.org/10.1105/tpc.009506