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Plant Cell, Vol. 11, 949-956, May 1999, Copyright © 1999, American Society of Plant Physiologists
FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering
Scott D. Michaelsa and
Richard M. Amasinoa
a Department of Biochemistry, University of Wisconsin, Madison, Wisconsin 53706-1544
Correspondence to:
Richard M. Amasino, amasino{at}biochem.wisc.edu (E-mail), 608-262-3453 (fax)
Winter-annual ecotypes of Arabidopsis are relatively late flowering, unless the flowering of these ecotypes is promoted by exposure to cold (vernalization). This vernalization-suppressible, late-flowering phenotype results from the presence of dominant, late-flowering alleles at two loci, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC). In this study, we report that flc null mutations result in early flowering, demonstrating that the role of active FLC alleles is to repress flowering. FLC was isolated by positional cloning and found to encode a novel MADS domain protein. The levels of FLC mRNA are regulated positively by FRI and negatively by LUMINIDEPENDENS. FLC is also negatively regulated by vernalization. Overexpression of FLC from a heterologous promoter is sufficient to delay flowering in the absence of an active FRI allele. We propose that the level of FLC activity acts through a rheostat-like mechanism to control flowering time in Arabidopsis and that modulation of FLC expression is a component of the vernalization response.
Related articles in Plant Cell:
- Planned Parenthood in Arabidopsis: FLOWERING LOCUS C
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Plant Cell 1999 11: 763-764.
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|
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|

|
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|
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|
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|
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|
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|
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|

|
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|
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|
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|

|
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|
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|
 |
|

|
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|
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|
 |
|

|
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|
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|
 |
|

|
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|
 |
 
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[Full Text]
[PDF]
|
 |
|

|
 |

|
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[Full Text]
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|
 |
|

|
 |

|
 |
 
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[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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2985 - 2998.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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3379 - 3386.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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|
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|
 |

|
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[Abstract]
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|
 |
|

|
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|
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|
 |
|

|
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|
 |
 
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[Abstract]
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|
 |
|

|
 |

|
 |
 
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J. Exp. Bot.,
June 1, 2006;
57(9):
2111 - 2119.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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June 1, 2006;
173(2):
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[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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133(10):
1857 - 1869.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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133(9):
1693 - 1702.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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898 - 912.
[Abstract]
[Full Text]
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|
 |
|

|
 |

|
 |
 
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481 - 492.
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|
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|
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|
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