ELF4 Is Required for Oscillatory Properties of the Circadian Clock1[W]

Circadian clocks are required to coordinate metabolism and physiology with daily changes in the environment. Such clocks have several distinctive features, including a free-running rhythm of approximately 24 h and the ability to entrain to both light or temperature cycles (zeitgebers). We have previously characterized the EARLY FLOWERING4 (ELF4) locus of Arabidopsis (Arabidopsis thaliana) as being important for robust rhythms. Here, it is shown that ELF4 is necessary for at least two core clock functions: entrainment to an environmental cycle and rhythm sustainability under constant conditions. We show that elf4 demonstrates clock input defects in light responsiveness and in circadian gating. Rhythmicity in elf4 could be driven by an environmental cycle, but an increased sensitivity to light means the circadian system of elf4 plants does not entrain normally. Expression of putative core clock genes and outputs were characterized in various ELF4 backgrounds to establish the molecular network of action. ELF4 was found to be intimately associated with the CIRCADIAN CLOCK-ASSOCIATED1 (CCA1)/LONG ELONGATED HYPOCOTYL (LHY)-TIMING OF CAB EXPRESSION1 (TOC1) feedback loop because, under free run, ELF4 is required to regulate the expression of CCA1 and TOC1 and, further, elf4 is locked in the evening phase of this feedback loop. ELF4, therefore, can be considered a component of the central CCA1/LHY-TOC1 feedback loop in the plant circadian clock.

[1]  Francis J Doyle,et al.  A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9 , 2006, Molecular systems biology.

[2]  S. Kay,et al.  Quantitative Analysis of Drosophila period Gene Transcription in Living Animals , 1997, Journal of biological rhythms.

[3]  C. R. McClung,et al.  Phase-Specific Circadian Clock Regulatory Elements in Arabidopsis1 , 2002, Plant Physiology.

[4]  M. Brunner,et al.  Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator. , 2006, Genes & development.

[5]  A. Millar,et al.  Circadian genetics in the model higher plant, Arabidopsis thaliana. , 2005, Methods in enzymology.

[6]  D. Bell-Pedersen,et al.  Assignment of an essential role for the Neurospora frequency gene in circadian entrainment to temperature cycles. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Michael F. Covington,et al.  ELF3 Modulates Resetting of the Circadian Clock in Arabidopsis , 2001, The Plant Cell Online.

[8]  I. Carré,et al.  Light‐regulated translation mediates gated induction of the Arabidopsis clock protein LHY , 2003, The EMBO journal.

[9]  M. Ni.  Integration of light signaling with photoperiodic flowering and circadian rhythm , 2005, Cell Research.

[10]  A. Hall,et al.  Functional independence of circadian clocks that regulate plant gene expression , 2000, Current Biology.

[11]  Peter Ruoff,et al.  The relationship between FRQ-protein stability and temperature compensation in the Neurospora circadian clock. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. E. Somers,et al.  Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. , 2000, Science.

[13]  Chentao Lin.  Blue Light Receptors and Signal Transduction Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000646. , 2002, The Plant Cell Online.

[14]  D. E. Somers,et al.  Conditional Circadian Dysfunction of the Arabidopsis early-flowering 3 Mutant , 1996, Science.

[15]  G. Coupland,et al.  Distinct Roles of GIGANTEA in Promoting Flowering and Regulating Circadian Rhythms in Arabidopsis , 2005, The Plant Cell Online.

[16]  M. Merrow,et al.  Entrainment of the Neurospora Circadian Clock , 2006, Chronobiology international.

[17]  K. Apel,et al.  AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. E. Somers,et al.  The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. , 1998, Development.

[19]  Jose L Pruneda-Paz,et al.  LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Hitoshi Onouchi,et al.  CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis , 2001, Nature.

[21]  Paul E. Brown,et al.  Extension of a genetic network model by iterative experimentation and mathematical analysis , 2005, Molecular systems biology.

[22]  Steve A. Kay,et al.  Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock , 2001, Science.

[23]  M. Mann,et al.  Phosphotyrosine interactome of the ErbB-receptor kinase family , 2005, Molecular systems biology.

[24]  P. Quail,et al.  EARLY FLOWERING 4 Functions in Phytochrome B-Regulated Seedling De-Etiolation1 , 2003, Plant Physiology.

[25]  D. E. Somers,et al.  The F-Box Protein ZEITLUPE Confers Dosage-Dependent Control on the Circadian Clock, Photomorphogenesis, and Flowering Time Online version contains Web-only data. , 2004, The Plant Cell Online.

[26]  Anthony Hall,et al.  Disruption of Hepatic Leptin Signaling Protects Mice From Age- and Diet-Related Glucose Intolerance , 2010, Diabetes.

[27]  C Robertson McClung,et al.  Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  P. Quail,et al.  ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. , 2005, The Plant journal : for cell and molecular biology.

[29]  C. R. McClung,et al.  What makes the Arabidopsis clock tick on time? A review on entrainment , 2005 .

[30]  C Robertson McClung,et al.  PSEUDO-RESPONSE REGULATOR 7 and 9 Are Partially Redundant Genes Essential for the Temperature Responsiveness of the Arabidopsis Circadian Clock , 2005, The Plant Cell Online.

[31]  E. Tobin,et al.  Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants1 , 2002, Plant Physiology.

[32]  R. Gomer,et al.  Two Circadian Timing Circuits in Neurospora crassa Cells Share Components and Regulate Distinct Rhythmic Processes , 2006, Journal of biological rhythms.

[33]  D. E. Somers,et al.  Arabidopsis FHY3 Specifically Gates Phytochrome Signaling to the Circadian Clock[W] , 2006, The Plant Cell Online.

[34]  Anthony Hall,et al.  The TIME FOR COFFEE Gene Maintains the Amplitude and Timing of Arabidopsis Circadian Clocks Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013730. , 2003, The Plant Cell Online.

[35]  S. Kay,et al.  Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Kay,et al.  A novel circadian phenotype based on firefly luciferase expression in transgenic plants. , 1992, The Plant cell.

[37]  C. Strayer,et al.  Circadian clock mutants in Arabidopsis identified by luciferase imaging , 1995, Science.

[38]  A. Hall,et al.  Distinct regulation of CAB and PHYB gene expression by similar circadian clocks. , 2002, The Plant journal : for cell and molecular biology.

[39]  Martin Straume,et al.  Quantitative Analyses of Circadian Gene Expression in Mammalian Cell Cultures , 2006, PLoS Comput. Biol..

[40]  Andrew J. Millar,et al.  The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana , 2002, Nature.

[41]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[42]  Arabidopsis FHY3 Specifically Gates Phytochrome Signaling to the Circadian Clock[W] , 2006, The Plant Cell Online.

[43]  R. Vierstra,et al.  The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. , 2001, Plant physiology.

[44]  Joanna Putterill,et al.  The late elongated hypocotyl Mutation of Arabidopsis Disrupts Circadian Rhythms and the Photoperiodic Control of Flowering , 1998, Cell.

[45]  Zhi-Yong Wang,et al.  Constitutive Expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) Gene Disrupts Circadian Rhythms and Suppresses Its Own Expression , 1998, Cell.

[46]  E. M. Meyerowitz,et al.  Arabidopsis thaliana , 2022, CABI Compendium.

[47]  Takeshi Mizuno,et al.  The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana. , 2002, Plant & cell physiology.

[48]  Till Roenneberg,et al.  Assignment of circadian function for the Neurospora clock gene frequency , 1999, Nature.

[49]  P. Lakin-Thomas.  Circadian clock genes frequency and white collar-1 are not essential for entrainment to temperature cycles in Neurospora crassa. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Anthony Hall,et al.  Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage , 2005, Science.

[51]  David Alabadí,et al.  Dual Role of TOC1 in the Control of Circadian and Photomorphogenic Responses in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006734. , 2003, The Plant Cell Online.

[52]  D. R. Wagner,et al.  EARLY FLOWERING3 Encodes a Novel Protein That Regulates Circadian Clock Function and Flowering in Arabidopsis , 2001, The Plant Cell Online.

[53]  Elise A. Kikis,et al.  ELF 4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA 1 and LHY , 2005 .

[54]  Anthony Hall,et al.  The ELF3 zeitnehmer regulates light signalling to the circadian clock , 2000, Nature.

[55]  Stacey L. Harmer,et al.  Overlapping and Distinct Roles of PRR7 and PRR9 in the Arabidopsis Circadian Clock , 2005, Current Biology.

[56]  Eberhard Schäfer,et al.  Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. , 2002, Annual review of plant biology.

[57]  Stacey L. Harmer,et al.  Critical Role for CCA1 and LHY in Maintaining Circadian Rhythmicity in Arabidopsis , 2002, Current Biology.

[58]  P. Quail,et al.  Phytochrome photosensory signalling networks , 2002, Nature Reviews Molecular Cell Biology.