Plant Cell Advance Online Publication Published on September 17, 2002; 10.1105/tpc.004564
Received May 16, 2002
Accepted July 26, 2002
Different Regulatory Regions Are Required for the Vernalization-Induced Repression
of FLOWERING LOCUS C and for the Epigenetic Maintenance of Repression
Candice C. Sheldon 1, Anna B. Conn 1, Elizabeth S. Dennis 1*, and W. James Peacock 1
1
Commonwealth Scientific and Industrial Research Organization, Plant Industry, Canberra,
Australian Capital Territory 2601, Australia
* To whom correspondence should be addressed. E-mail: liz.dennis{at}csiro.au.
Vernalization, the promotion of flowering by a prolonged period of low temperature,
results in repression of the floral repressor FLOWERING LOCUS C (FLC
) and in early flowering. This repression bears the hallmark of an epigenetic
event: the low expression state is maintained over many cell division cycles, but
expression is derepressed in progeny. We show that the two stages of the response
of FLC to vernalization, the repression of FLC and the maintenance
of the repression during growth at normal temperatures after vernalization, are mediated
through different regions of the FLC gene. Both promoter and intragenic
regions are required for the responses. We also identify a 75-bp region in the
FLC promoter that, in addition to intragenic sequences, is required for expression
in nonvernalized plants.
This article has been cited by other articles:

|
 |

|
 |
 
F. Liu, S. Marquardt, C. Lister, S. Swiezewski, and C. Dean
Targeted 3' Processing of Antisense Transcripts Triggers Arabidopsis FLC Chromatin Silencing
Science,
January 1, 2010;
327(5961):
94 - 97.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Tamada, J.-Y. Yun, S. c. Woo, and R. M. Amasino
ARABIDOPSIS TRITHORAX-RELATED7 Is Required for Methylation of Lysine 4 of Histone H3 and for Transcriptional Activation of FLOWERING LOCUS C
PLANT CELL,
October 1, 2009;
21(10):
3257 - 3269.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Luo, B. G. Durgin, N. Watanabe, and E. Lam
Defining the Functional Network of Epigenetic Regulators in Arabidopsis thaliana
Mol Plant,
July 1, 2009;
2(4):
661 - 674.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. N. Oliver, E. J. Finnegan, E. S. Dennis, W. J. Peacock, and B. Trevaskis
Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene
PNAS,
May 19, 2009;
106(20):
8386 - 8391.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. De Lucia, P. Crevillen, A. M. E. Jones, T. Greb, and C. Dean
Inaugural Article: A PHD-Polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization
PNAS,
November 4, 2008;
105(44):
16831 - 16836.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Lazaro, A. Gomez-Zambrano, L. Lopez-Gonzalez, M. Pineiro, and J. A. Jarillo
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.,
February 21, 2008;
(2008)
erm332v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. C. Sheldon, M. J. Hills, C. Lister, C. Dean, E. S. Dennis, and W. J. Peacock
Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization
PNAS,
February 12, 2008;
105(6):
2214 - 2219.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Calonje, R. Sanchez, L. Chen, and Z. R. Sung
EMBRYONIC FLOWER1 Participates in Polycomb Group-Mediated AG Gene Silencing in Arabidopsis
PLANT CELL,
February 1, 2008;
20(2):
277 - 291.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Domagalska, F. M. Schomburg, R. M. Amasino, R. D. Vierstra, F. Nagy, and S. J. Davis
Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering
Development,
August 1, 2007;
134(15):
2841 - 2850.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Pei, L. Niu, F. Lu, C. Liu, J. Zhai, X. Kong, and X. Cao
Mutations in the Type II Protein Arginine Methyltransferase AtPRMT5 Result in Pleiotropic Developmental Defects in Arabidopsis
Plant Physiology,
August 1, 2007;
144(4):
1913 - 1923.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Reeves, Y. He, R. J. Schmitz, R. M. Amasino, L. W. Panella, and C. M. Richards
Evolutionary Conservation of the FLOWERING LOCUS C-Mediated Vernalization Response: Evidence From the Sugar Beet (Beta vulgaris)
Genetics,
May 1, 2007;
176(1):
295 - 307.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Shindo, C. Lister, P. Crevillen, M. Nordborg, and C. Dean
Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response.
Genes & Dev.,
November 15, 2006;
20(22):
3079 - 3083.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kim, K. Choi, C. Park, H.-J. Hwang, and I. Lee
SUPPRESSOR OF FRIGIDA4, Encoding a C2H2-Type Zinc Finger Protein, Represses Flowering by Transcriptional Activation of Arabidopsis FLOWERING LOCUS C
PLANT CELL,
November 1, 2006;
18(11):
2985 - 2998.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Sung and R. M. Amasino
Molecular genetic studies of the memory of winter
J. Exp. Bot.,
October 1, 2006;
57(13):
3369 - 3377.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Corbesier and G. Coupland
The quest for florigen: a review of recent progress
J. Exp. Bot.,
October 1, 2006;
57(13):
3395 - 3403.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Guyomarc'h, M. Benhamed, G. Lemonnier, J.-P. Renou, D.-X. Zhou, and M. Delarue
MGOUN3: evidence for chromatin-mediated regulation of FLC expression
J. Exp. Bot.,
June 1, 2006;
57(9):
2111 - 2119.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Wang, L. Tian, H.-S. Lee, and Z. J. Chen
Nonadditive Regulation of FRI and FLC Loci Mediates Flowering-Time Variation in Arabidopsis Allopolyploids
Genetics,
June 1, 2006;
173(2):
965 - 974.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Searle, Y. He, F. Turck, C. Vincent, F. Fornara, S. Krober, R. A. Amasino, and G. Coupland
The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis.
Genes & Dev.,
April 1, 2006;
20(7):
898 - 912.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Martin-Trillo, A. Lazaro, R. S. Poethig, C. Gomez-Mena, M. A. Pineiro, J. M. Martinez-Zapater, and J. A. Jarillo
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,
April 1, 2006;
133(7):
1241 - 1252.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Mylne, L. Barrett, F. Tessadori, S. Mesnage, L. Johnson, Y. V. Bernatavichute, S. E. Jacobsen, P. Fransz, and C. Dean
LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC
PNAS,
March 28, 2006;
103(13):
5012 - 5017.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Grennan
Variations on a Theme. Regulation of Flowering Time in Arabidopsis
Plant Physiology,
February 1, 2006;
140(2):
399 - 400.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-M. Jeong, J.-H. Mun, I. Lee, J. C. Woo, C. B. Hong, and S.-G. Kim
Distinct Roles of the First Introns on the Expression of Arabidopsis Profilin Gene Family Members
Plant Physiology,
January 1, 2006;
140(1):
196 - 209.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Kooiker, C. A. Airoldi, A. Losa, P. S. Manzotti, L. Finzi, M. M. Kater, and L. Colombo
BASIC PENTACYSTEINE1, a GA Binding Protein That Induces Conformational Changes in the Regulatory Region of the Homeotic Arabidopsis Gene SEEDSTICK
PLANT CELL,
March 1, 2005;
17(3):
722 - 729.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S.-I Lin, J.-G. Wang, S.-Y. Poon, C.-l. Su, S.-S. Wang, and T.-J. Chiou
Differential Regulation of FLOWERING LOCUS C Expression by Vernalization in Cabbage and Arabidopsis
Plant Physiology,
March 1, 2005;
137(3):
1037 - 1048.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Werner, J. O. Borevitz, N. Warthmann, G. T. Trainer, J. R. Ecker, J. Chory, and D. Weigel
Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation
PNAS,
February 15, 2005;
102(7):
2460 - 2465.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. C. Moore, S. R. Grant, and M. D. Purugganan
Molecular Population Genetics of Redundant Floral-Regulatory Genes in Arabidopsis thaliana
Mol. Biol. Evol.,
January 1, 2005;
22(1):
91 - 103.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Liu, Y. He, R. Amasino, and X. Chen
siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis
Genes & Dev.,
December 1, 2004;
18(23):
2873 - 2878.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. L. Caicedo, J. R. Stinchcombe, K. M. Olsen, J. Schmitt, and M. D. Purugganan
Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait
PNAS,
November 2, 2004;
101(44):
15670 - 15675.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. R. Henderson and C. Dean
Control of Arabidopsis flowering: the chill before the bloom
Development,
August 15, 2004;
131(16):
3829 - 3838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Ferrario, J. Busscher, J. Franken, T. Gerats, M. Vandenbussche, G. C. Angenent, and R. G.H. Immink
Ectopic Expression of the Petunia MADS Box Gene UNSHAVEN Accelerates Flowering and Confers Leaf-Like Characteristics to Floral Organs in a Dominant-Negative Manner
PLANT CELL,
June 1, 2004;
16(6):
1490 - 1505.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Jack
Molecular and Genetic Mechanisms of Floral Control
PLANT CELL,
June 1, 2004;
16(suppl_1):
S1 - S17.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. K. Boss, R. M. Bastow, J. S. Mylne, and C. Dean
Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting
PLANT CELL,
June 1, 2004;
16(suppl_1):
S18 - S31.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. MYLNE, T. GREB, C. LISTER, and C. DEAN
Epigenetic Regulation in the Control of Flowering
Cold Spring Harb Symp Quant Biol,
January 1, 2004;
69(0):
457 - 464.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. He, S. D. Michaels, and R. M. Amasino
Regulation of Flowering Time by Histone Acetylation in Arabidopsis
Science,
December 5, 2003;
302(5651):
1751 - 1754.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-S. Noh and R. M. Amasino
PIE1, an ISWI Family Gene, Is Required for FLC Activation and Floral Repression in Arabidopsis
PLANT CELL,
July 1, 2003;
15(7):
1671 - 1682.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gazzani, A. R. Gendall, C. Lister, and C. Dean
Analysis of the Molecular Basis of Flowering Time Variation in Arabidopsis Accessions
Plant Physiology,
June 1, 2003;
132(2):
1107 - 1114.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
O. J. Ratcliffe, R. W. Kumimoto, B. J. Wong, and J. L. Riechmann
Analysis of the Arabidopsis MADS AFFECTING FLOWERING Gene Family: MAF2 Prevents Vernalization by Short Periods of Cold
PLANT CELL,
May 1, 2003;
15(5):
1159 - 1169.
[Abstract]
[Full Text]
|
 |
|
|
|