FLOWERING LOCUS C-dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways

Salathia, Neeraj; Davis, Seth J.; Lynn, James R.; Michaels, Scott D.; Amasino, Richard M.; Millar, Andrew J.

doi:10.1186/1471-2229-6-10

Title: FLOWERING LOCUS C-dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways

Journal Article · Wed May 31 00:00:00 EDT 2006 · BMC Plant Biology

DOI:https://doi.org/10.1186/1471-2229-6-10· OSTI ID:1626506

Salathia, Neeraj ^[1]; Davis, Seth J. ^[2]; Lynn, James R. ^[3]; Michaels, Scott D. ^[4]; Amasino, Richard M. ^[5]; Millar, Andrew J. ^[6]

Univ. of Warwick, Coventry (United Kingdom). Dept. of Biological Sciences; Harvard Univ., Cambridge, MA (United States). Bauer Center for Genomics Research
Univ. of Warwick, Coventry (United Kingdom). Dept. of Biological Sciences; Max Planck Inst. for Plant Breeding Research, Cologne (Germany). Dept. fo Plant Developmental Biology
Warwick HRI, Wellesbourne, Warwick (United Kingdom)
Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry; Indiana Univ., Bloomington, IN (United States). Dept. of Biology
Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
Univ. of Warwick, Coventry (United Kingdom). Dept. of Biological Sciences; Univ. of Edinburgh, Scotland (United Kingdom). School of Biological Sciences

Background: The circadian system drives pervasive biological rhythms in plants. Circadian clocks integrate endogenous timing information with environmental signals, in order to match rhythmic outputs to the local day/night cycle. Multiple signaling pathways affect the circadian system, in ways that are likely to be adaptively significant. Our previous studies of natural genetic variation in Arabidopsis thaliana accessions implicated FLOWERING LOCUS C (FLC) as a circadian-clock regulator. The MADS-box transcription factor FLC is best known as a regulator of flowering time. Its activity is regulated by many regulatory genes in the "autonomous" and vernalization-dependent flowering pathways. We tested whether these same pathways affect the circadian system. Results: Genes in the autonomous flowering pathway, including FLC, were found to regulate circadian period in Arabidopsis. The mechanisms involved are similar, but not identical, to the control of flowering time. By mutant analyses, we demonstrate a graded effect of FLC expression upon circadian period. Related MADS-box genes had less effect on clock function. We also reveal an unexpected vernalization-dependent alteration of periodicity. Conclusion: This study has aided in the understanding of FLC's role in the clock, as it reveals that the network affecting circadian timing is partially overlapping with the floral-regulatory network. We also show a link between vernalization and circadian period. This finding may be of ecological relevance for developmental programing in other plant species.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF)

Grant/Contract Number:: 0133663; 0209786

OSTI ID:: 1626506

Journal Information:: BMC Plant Biology, Vol. 6, Issue 1; ISSN 1471-2229

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

C IRCADIAN R HYTHMS IN P LANTS McClung, C. Robertson Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev.arplant.52.1.139	journal	June 2001
Multiple Pathways in the Decision to Flower: Enabling, Promoting, and Resetting Boss, P. K. THE PLANT CELL ONLINE, Vol. 16, Issue suppl_1 https://doi.org/10.1105/tpc.015958	journal	March 2004
Time zones: a comparative genetics of circadian clocks Young, Michael W.; Kay, Steve A. Nature Reviews Genetics, Vol. 2, Issue 9 https://doi.org/10.1038/35088576	journal	September 2001
The Circadian Clock. A Plant's Best Friend in a Spinning World Eriksson, Maria E.; Millar, Andrew J. Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.103.022343	journal	June 2003
Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock Harmer, S. L.; Hogenesch, J. B.; Straume, M. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2110	journal	December 2000
The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana Somers, D. E.; Webb, A. A.; Pearson, M. Development, Vol. 125, Issue 3 https://doi.org/10.1242/dev.125.3.485	journal	February 1998
Natural Allelic Variation in the Temperature-Compensation Mechanisms of the Arabidopsis thaliana Circadian ClockSequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY685131 and AY685132. Edwards, Kieron D.; Lynn, James R.; Gyula, Péter Genetics, Vol. 170, Issue 1 https://doi.org/10.1534/genetics.104.035238	journal	May 2005
Natural allelic variation identifies new genes in the Arabidopsis circadian system Swarup, Kamal; Alonso-Blanco, Carlos; Lynn, James R. The Plant Journal, Vol. 20, Issue 1 https://doi.org/10.1046/j.1365-313X.1999.00577.x	journal	October 1999
Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock Michael, T. P. Science, Vol. 302, Issue 5647 https://doi.org/10.1126/science.1082971	journal	November 2003
Analysis of the Molecular Basis of Flowering Time Variation in Arabidopsis Accessions Gazzani, Silvia; Gendall, Anthony R.; Lister, Clare Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.103.021212	journal	June 2003
Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis Michaels, Scott D.; He, Yuehui; Scortecci, Katia C. Proceedings of the National Academy of Sciences, Vol. 100, Issue 17 https://doi.org/10.1073/pnas.1531467100	journal	August 2003
Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population: AFLP based linkage map of Arabidopsis Alonso-Blanco, Carlos; Peeters, Anton J. M.; Koornneef, Maarten The Plant Journal, Vol. 14, Issue 2 https://doi.org/10.1046/j.1365-313X.1998.00115.x	journal	April 1998
Vernalization and epigenetics: how plants remember winter Sung, Sibum; Amasino, Richard M. Current Opinion in Plant Biology, Vol. 7, Issue 1 https://doi.org/10.1016/j.pbi.2003.11.010	journal	February 2004
FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering Michaels, Scott D.; Amasino, Richard M. The Plant Cell, Vol. 11, Issue 5 https://doi.org/10.1105/tpc.11.5.949	journal	May 1999
Loss of FLOWERING LOCUS C Activity Eliminates the Late-Flowering Phenotype of FRIGIDA and Autonomous Pathway Mutations but Not Responsiveness to Vernalization Michaels, Scott D.; Amasino, Richard M. The Plant Cell, Vol. 13, Issue 4 https://doi.org/10.1105/tpc.13.4.935	journal	April 2001
The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation Sheldon, Candice C.; Burn, Joanne E.; Perez, Pascual P. The Plant Cell, Vol. 11, Issue 3 https://doi.org/10.1105/tpc.11.3.445	journal	March 1999
The Need for Winter in the Switch to Flowering Henderson, Ian R.; Shindo, Chikako; Dean, Caroline Annual Review of Genetics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.genet.37.110801.142640	journal	December 2003
FCA, a Gene Controlling Flowering Time in Arabidopsis, Encodes a Protein Containing RNA-Binding Domains Macknight, Richard; Bancroft, Ian; Page, Tania Cell, Vol. 89, Issue 5 https://doi.org/10.1016/S0092-8674(00)80256-1	journal	May 1997
FY Is an RNA 3′ End-Processing Factor that Interacts with FCA to Control the Arabidopsis Floral Transition Simpson, Gordon G.; Dijkwel, Paul P.; Quesada, Victor Cell, Vol. 113, Issue 6 https://doi.org/10.1016/S0092-8674(03)00425-2	journal	June 2003
Autoregulation of FCA pre-mRNA processing controls Arabidopsis flowering time Quesada, V. The EMBO Journal, Vol. 22, Issue 12 https://doi.org/10.1093/emboj/cdg305	journal	June 2003
Isolation of LUMINIDEPENDENS: a gene involved in the control of flowering time in Arabidopsis. Lee, I.; Aukerman, M. J.; Gore, S. L. The Plant Cell, Vol. 6, Issue 1 https://doi.org/10.1105/tpc.6.1.75	journal	January 1994
Flowering on time: genes that regulate the floral transition Blázquez, Miguel; Koornneef, Maarten; Putterill, Jo EMBO reports, Vol. 2, Issue 12 https://doi.org/10.1093/embo-reports/kve254	journal	December 2001
A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana Koornneef, M.; Hanhart, C. J.; van der Veen, J. H. Molecular and General Genetics MGG, Vol. 229, Issue 1 https://doi.org/10.1007/BF00264213	journal	September 1991
Regulation of flowering time by FVE, a retinoblastoma-associated protein Ausín, Israel; Alonso-Blanco, Carlos; Jarillo, José A. Nature Genetics, Vol. 36, Issue 2 https://doi.org/10.1038/ng1295	journal	January 2004
Arabidopsis late-flowering fve mutants are affected in both vegetative and reproductive development Martinez-Zapater, Jose M.; Jarillo, Jose A.; Cruz-Alvarez, Marilyn The Plant Journal, Vol. 7, Issue 4 https://doi.org/10.1046/j.1365-313X.1995.7040543.x	journal	April 1995
FPA, a Gene Involved in Floral Induction in Arabidopsis, Encodes a Protein Containing RNA-Recognition Motifs Schomburg, F. M. THE PLANT CELL ONLINE, Vol. 13, Issue 6 https://doi.org/10.1105/tpc.13.6.1427	journal	June 2001
FLC, a repressor of flowering, is regulated by genes in different inductive pathways Rouse, Dean T.; Sheldon, Candice C.; Bagnall, David J. The Plant Journal, Vol. 29, Issue 2 https://doi.org/10.1046/j.0960-7412.2001.01210.x	journal	January 2002
Gibberellin response mutants identified by luciferase imaging Meier, Carsten; Bouquin, Thomas; Nielsen, Mads Eggert The Plant Journal, Vol. 25, Issue 5 https://doi.org/10.1046/j.1365-313x.2001.00980.x	journal	December 2001
The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis Lee, H. Genes & Development, Vol. 14, Issue 18 https://doi.org/10.1101/gad.813600	journal	September 2000
Mutagenesis of Plants Overexpressing CONSTANS Demonstrates Novel Interactions among Arabidopsis Flowering-Time Genes Onouchi, Hitoshi; Igeño, M. Isabel; Périlleux, Claire The Plant Cell, Vol. 12, Issue 6 https://doi.org/10.1105/tpc.12.6.885	journal	June 2000
Regulation of Flowering in Arabidopsis by an FLCHomologue Ratcliffe, Oliver J.; Nadzan, Greg C.; Reuber, T. Lynne Plant Physiology, Vol. 126, Issue 1 https://doi.org/10.1104/pp.126.1.122	journal	May 2001
Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana Scortecci, Katia; Michaels, Scott D.; Amasino, Richard M. Plant Molecular Biology, Vol. 52, Issue 5, p. 915-922 https://doi.org/10.1023/A:1025426920923	journal	January 2003
Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis Hartmann, Ulrike; Hohmann, Susanne; Nettesheim, Klaus The Plant Journal, Vol. 21, Issue 4 https://doi.org/10.1046/j.1365-313x.2000.00682.x	journal	February 2000
Vernalization requires epigenetic silencing of FLC by histone methylation Bastow, Ruth; Mylne, Joshua S.; Lister, Clare Nature, Vol. 427, Issue 6970 https://doi.org/10.1038/nature02269	journal	January 2004
AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization: AGL24 acts as a promoter of flowering in Arabidopsis Michaels, Scott D.; Ditta, Gary; Gustafson-Brown, Cindy The Plant Journal, Vol. 33, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01671.x	journal	February 2003
Winter disruption of the circadian clock in chestnut Ramos, Alberto; Pérez-Solís, Estefanía; Ibáñez, Cristian Proceedings of the National Academy of Sciences, Vol. 102, Issue 19 https://doi.org/10.1073/pnas.0408549102	journal	April 2005
PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis He, Y. Genes & Development, Vol. 18, Issue 22 https://doi.org/10.1101/gad.1244504	journal	November 2004
A thermosensory pathway controlling flowering time in Arabidopsis thaliana Blázquez, Miguel A.; Ahn, Ji Hoon; Weigel, Detlef Nature Genetics, Vol. 33, Issue 2 https://doi.org/10.1038/ng1085	journal	January 2003
Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis Roden, Laura C.; Song, Hae-Ryong; Jackson, Stephen Proceedings of the National Academy of Sciences, Vol. 99, Issue 20 https://doi.org/10.1073/pnas.192365599	journal	September 2002
Molecular basis of seasonal time measurement in Arabidopsis Yanovsky, Marcelo J.; Kay, Steve A. Nature, Vol. 419, Issue 6904 https://doi.org/10.1038/nature00996	journal	September 2002
The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis: SOC1 integrates vernalization and GA signals for flowering Moon, Jihyun; Suh, Sung-Suk; Lee, Horim The Plant Journal, Vol. 35, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01833.x	journal	August 2003
A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana Kim, Hyoun-Joung; Hyun, Youbong; Park, Jin-Young Nature Genetics, Vol. 36, Issue 2 https://doi.org/10.1038/ng1298	journal	January 2004
Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering: FLM is a MADS-box flowering repressor Scortecci, Katia C.; Michaels, Scott D.; Amasino, Richard M. The Plant Journal, Vol. 26, Issue 2 https://doi.org/10.1046/j.1365-313x.2001.01024.x	journal	April 2001
Genetic interactions of the Arabidopsis flowering time geneFCA,with genes regulating floral initiation Page, Tania; Macknight, Richard; Yang, Chang-Hsien The Plant Journal, Vol. 17, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.00364.x	journal	January 1999
Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis Dowson‐Day, Mandy J.; Millar, Andrew J. The Plant Journal, Vol. 17, Issue 1 https://doi.org/10.1046/j.1365-313X.1999.00353.x	journal	January 1999
The Regulation of Circadian Period by Phototransduction Pathways in Arabidopsis Millar, Andrew J.; Straume, Martin; Chory, Joanne Science, Vol. 267, Issue 5201 https://doi.org/10.1126/science.7855596	journal	February 1995
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Quantitative Analysis of Drosophila period Gene Transcription in Living Animals Plautz, Jeffrey D.; Straume, Martin; Stanewsky, Ralf Journal of Biological Rhythms, Vol. 12, Issue 3 https://doi.org/10.1177/074873049701200302	journal	June 1997
Recovery of inter-block information when block sizes are unequal Patterson, H. D.; Thompson, R. Biometrika, Vol. 58, Issue 3 https://doi.org/10.1093/biomet/58.3.545	journal	January 1971

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