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PLANT CELL 15 (5): 1159-1169

Copyright © 2003 by the American Society of Plant Physiologists.

Analysis of the Arabidopsis MADS AFFECTING FLOWERING Gene Family: MAF2 Prevents Vernalization by Short Periods of Cold

Oliver J. Ratcliffe1, Roderick W. Kumimoto, Becky J. Wong, and José Luis Riechmann2

Mendel Biotechnology, Inc., Hayward, California 94545

1 To whom correspondence should be addressed. E-mail oratclif{at}; fax 510-264-0254

Abstract: The 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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Plant Physiology 153, 821-831
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Plant Physiology 151, 1476-1485
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Mol Plant 2, 565-577
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Plant Physiology 148, 1681-1694
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Y. Cao, Y. Dai, S. Cui, and L. Ma (2008)
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   Abstract »    Full Text »    PDF »
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J. Exp. Bot.
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L. Xu, Z. Zhao, A. Dong, L. Soubigou-Taconnat, J.-P. Renou, A. Steinmetz, and W.-H. Shen (2008)
Mol. Cell. Biol. 28, 1348-1360
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J. Exp. Bot. 59, 225-234
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Plant Cell Physiol. 49, 191-200
   Abstract »    Full Text »    PDF »
Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana.
R. J. Schmitz, S. Sung, and R. M. Amasino (2008)
PNAS 105, 411-416
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P. A. Reeves, Y. He, R. J. Schmitz, R. M. Amasino, L. W. Panella, and C. M. Richards (2007)
Genetics 176, 295-307
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X. M. Xu, A. Rose, S. Muthuswamy, S. Y. Jeong, S. Venkatakrishnan, Q. Zhao, and I. Meier (2007)
PLANT CELL 19, 1537-1548
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W. Deng, C. Liu, Y. Pei, X. Deng, L. Niu, and X. Cao (2007)
Plant Physiology 143, 1660-1668
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SEF, a New Protein Required for Flowering Repression in Arabidopsis, Interacts with PIE1 and ARP6.
R. March-Diaz, M. Garcia-Dominguez, F. J. Florencio, and J. C. Reyes (2007)
Plant Physiology 143, 893-901
   Abstract »    Full Text »    PDF »
Repression of Flowering in Arabidopsis Requires Activation of FLOWERING LOCUS C Expression by the Histone Variant H2A.Z.
R. B. Deal, C. N. Topp, E. C. McKinney, and R. B. Meagher (2007)
PLANT CELL 19, 74-83
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A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis.
S. Sung, R. J. Schmitz, and R. M. Amasino (2006)
Genes & Dev. 20, 3244-3248
   Abstract »    Full Text »    PDF »
FRIGIDA LIKE 2 Is a Functional Allele in Landsberg erecta and Compensates for a Nonsense Allele of FRIGIDA LIKE 1.
M. R. Schlappi (2006)
Plant Physiology 142, 1728-1738
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SUPPRESSOR OF FRIGIDA4, Encoding a C2H2-Type Zinc Finger Protein, Represses Flowering by Transcriptional Activation of Arabidopsis FLOWERING LOCUS C.
S. Kim, K. Choi, C. Park, H.-J. Hwang, and I. Lee (2006)
PLANT CELL 18, 2985-2998
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T. Shimada, Y. Koumoto, L. Li, M. Yamazaki, M. Kondo, M. Nishimura, and I. Hara-Nishimura (2006)
Plant Cell Physiol. 47, 1187-1194
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Highly Specific Gene Silencing by Artificial MicroRNAs in Arabidopsis.
R. Schwab, S. Ossowski, M. Riester, N. Warthmann, and D. Weigel (2006)
PLANT CELL 18, 1121-1133
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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.
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Development 133, 1241-1252
   Abstract »    Full Text »    PDF »
AtVAM3 is Required for Normal Specification of Idioblasts, Myrosin Cells.
H. Ueda, C. Nishiyama, T. Shimada, Y. Koumoto, Y. Hayashi, M. Kondo, T. Takahashi, I. Ohtomo, M. Nishimura, and I. Hara-Nishimura (2006)
Plant Cell Physiol. 47, 164-175
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Establishment of the Vernalization-Responsive, Winter-Annual Habit in Arabidopsis Requires a Putative Histone H3 Methyl Transferase.
S. Y. Kim, Y. He, Y. Jacob, Y.-S. Noh, S. Michaels, and R. Amasino (2005)
PLANT CELL 17, 3301-3310
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R. B. Deal, M. K. Kandasamy, E. C. McKinney, and R. B. Meagher (2005)
PLANT CELL 17, 2633-2646
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SUPPRESSOR OF FRIGIDA3 Encodes a Nuclear ACTIN-RELATED PROTEIN6 Required for Floral Repression in Arabidopsis.
K. Choi, S. Kim, S. Y. Kim, M. Kim, Y. Hyun, H. Lee, S. Choe, S.-G. Kim, S. Michaels, and I. Lee (2005)
PLANT CELL 17, 2647-2660
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J. D. Werner, J. O. Borevitz, N. Warthmann, G. T. Trainer, J. R. Ecker, J. Chory, and D. Weigel (2005)
PNAS 102, 2460-2465
   Abstract »    Full Text »    PDF »
PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis.
Y. He, M. R. Doyle, and R. M. Amasino (2004)
Genes & Dev. 18, 2774-2784
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Ann. Bot. 94, 717-724
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B. Noh, S.-H. Lee, H.-J. Kim, G. Yi, E.-A. Shin, M. Lee, K.-J. Jung, M. R. Doyle, R. M. Amasino, and Y.-S. Noh (2004)
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D. G. Bielenberg, Y. Wang, S. Fan, G. L. Reighard, R. Scorza, and A. G. Abbott (2004)
J. Hered. 95, 436-444
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I. R. Henderson and C. Dean (2004)
Development 131, 3829-3838
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PLANT CELL 16, 1536-1549
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PLANT CELL 16, S18-S31
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Extensive Phenotypic Variation in Early Flowering Mutants of Arabidopsis.
S. Pouteau, V. Ferret, V. Gaudin, D. Lefebvre, M. Sabar, G. Zhao, and F. Prunus (2004)
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Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny.
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