Circadian clock function in Arabidopsis thaliana: time beyond transcription.

The past decade has seen a remarkable advance in our understanding of the plant circadian system, mostly in Arabidopsis thaliana. It is now well established that Arabidopsis clock genes and their protein products operate through autoregulatory feedback loops that promote rhythmic oscillations in cellular, metabolic and physiological activities. This article reviews recent studies that have provided evidence for new mechanisms of clock organization and function. These mechanisms include protein-protein interactions and the regulation of protein stability, which, together, directly connect light signalling to the Arabidopsis circadian system. Evidence of rhythmic changes in chromatin structure has also opened new and exciting ways for regulation of clock gene expression. All of these mechanisms ensure an appropriate synchronization with the environment, which is crucial for successful plant growth and development.

[1]  T. Mizuno,et al.  Rhythmic and light-inducible appearance of clock-associated pseudo-response regulator protein PRR9 through programmed degradation in the dark in Arabidopsis thaliana. , 2007, Plant & cell physiology.

[2]  D. Virshup,et al.  Post-translational modifications regulate the ticking of the circadian clock , 2007, Nature Reviews Molecular Cell Biology.

[3]  S. Kay,et al.  A Role for LKP2 in the Circadian Clock of Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010332. , 2001, The Plant Cell Online.

[4]  D. E. Somers,et al.  Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[6]  R. D. Rudic,et al.  Histone Acetyltransferase-dependent Chromatin Remodeling and the Vascular Clock* , 2004, Journal of Biological Chemistry.

[7]  P. Más,et al.  Altered oscillator function affects clock resonance and is responsible for the reduced day-length sensitivity of CKB4 overexpressing plants. , 2007, The Plant journal : for cell and molecular biology.

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

[9]  K. David,et al.  Arabidopsis GIGANTEA protein is post‐transcriptionally regulated by light and dark , 2006, FEBS letters.

[10]  Takeshi Mizuno,et al.  The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. Characterization with APRR1-overexpressing plants. , 2002, Plant & cell physiology.

[11]  D. E. Somers,et al.  ZEITLUPE Encodes a Novel Clock-Associated PAS Protein from Arabidopsis , 2000, Cell.

[12]  Takao Kondo,et al.  ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria , 2007, Proceedings of the National Academy of Sciences.

[13]  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.

[14]  E. Tobin,et al.  Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Neil Dalchau,et al.  Modulation of environmental responses of plants by circadian clocks. , 2007, Plant, cell & environment.

[16]  Takanobu Nakazawa,et al.  microRNA Modulation of Circadian-Clock Period and Entrainment , 2007, Neuron.

[17]  Y. Sakaki,et al.  Structural and functional analysis of 3' untranslated region of mouse Period1 mRNA. , 2003, Biochemical and biophysical research communications.

[18]  Tsuyoshi Mizoguchi,et al.  LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. , 2002, Developmental cell.

[19]  S. Kay,et al.  Living by the calendar: how plants know when to flower , 2003, Nature Reviews Molecular Cell Biology.

[20]  A. Webb,et al.  Circadian and Diurnal Calcium Oscillations Encode Photoperiodic Information in Arabidopsis , 2004, The Plant Cell Online.

[21]  E. Tobin,et al.  Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  P. Hardin,et al.  Circadian rhythms from multiple oscillators: lessons from diverse organisms , 2005, Nature Reviews Genetics.

[23]  G. Coupland,et al.  The Molecular Basis of Diversity in the Photoperiodic Flowering Responses of Arabidopsis and Rice , 2004, Plant Physiology.

[24]  S. Kay,et al.  Molecular bases of circadian rhythms. , 2001, Annual review of cell and developmental biology.

[25]  K. Luger.  Structure and dynamic behavior of nucleosomes. , 2003, Current opinion in genetics & development.

[26]  C. Robertson McClung,et al.  Plant Circadian Rhythms , 2006, The Plant Cell Online.

[27]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[28]  Nicolas Cermakian,et al.  Molecular Circadian Rhythms in Central and Peripheral Clocks in Mammals , 2007, Chronobiology international.

[29]  S. Kay,et al.  PRR7 protein levels are regulated by light and the circadian clock in Arabidopsis. , 2007, The Plant journal : for cell and molecular biology.

[30]  C. R. McClung,et al.  Circadian Control of Messenger RNA Stability. Association with a Sequence-Specific Messenger RNA Decay Pathway1[w] , 2005, Plant Physiology.

[31]  J. Dunlap,et al.  Temperature-modulated alternative splicing and promoter use in the Circadian clock gene frequency. , 2005, Molecular biology of the cell.

[32]  B. Bartel,et al.  FKF1, a Clock-Controlled Gene that Regulates the Transition to Flowering in Arabidopsis , 2000, Cell.

[33]  M. Ishiura,et al.  PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock , 2005, Genes to cells : devoted to molecular & cellular mechanisms.

[34]  C. Johnson,et al.  Clock Evolution and Adaptation: Whence and Whither? , 2007 .

[35]  I. Edery,et al.  Splicing of the period Gene 3′-Terminal Intron Is Regulated by Light, Circadian Clock Factors, and Phospholipase C , 2004, Molecular and Cellular Biology.

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

[37]  M. Brunner,et al.  Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. , 2006, Genes & development.

[38]  K. Apel,et al.  The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. , 2003, The Plant journal : for cell and molecular biology.

[39]  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.

[40]  R. Green,et al.  Regulation of output from the plant circadian clock , 2007, The FEBS journal.

[41]  E. Tobin,et al.  The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Ueli Schibler,et al.  Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions , 2006, Nature Genetics.

[43]  Dmitri A. Nusinow,et al.  FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis , 2007, Science.

[44]  P. Más,et al.  Circadian clock signaling in Arabidopsis thaliana: from gene expression to physiology and development. , 2005, The International journal of developmental biology.

[45]  Paolo Sassone-Corsi,et al.  Circadian Regulator CLOCK Is a Histone Acetyltransferase , 2006, Cell.

[46]  D. E. Somers,et al.  Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana , 2003, Nature.

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

[48]  J. Cherry,et al.  Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: Rapid decay is associated with a group of touch- and specific clock-controlled genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Kyong-Tai Kim,et al.  Essential Role of 3′-Untranslated Region-mediated mRNA Decay in Circadian Oscillations of Mouse Period3 mRNA* , 2006, Journal of Biological Chemistry.

[50]  M. Grunstein,et al.  Functions of site-specific histone acetylation and deacetylation. , 2007, Annual review of biochemistry.

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

[52]  Karine David,et al.  ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. , 2007, Nature.

[53]  S. Kay,et al.  FKF1 F-Box Protein Mediates Cyclic Degradation of a Repressor of CONSTANS in Arabidopsis , 2005, Science.

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

[55]  Katharine E. Hubbard,et al.  How plants tell the time. , 2006, The Biochemical journal.

[56]  T. Kiba,et al.  Targeted Degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL Complex Regulates Clock Function and Photomorphogenesis in Arabidopsis thaliana[W] , 2007, The Plant Cell Online.

[57]  C. Johnson,et al.  Dark-Stimulated Calcium Ion Fluxes in the Chloroplast Stroma and Cytosol Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000653. , 2002, The Plant Cell Online.

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

[59]  Endogenous plant rhythms , 2006 .

[60]  I. Carré,et al.  DET1 regulates the proteasomal degradation of LHY, a component of the Arabidopsis circadian clock , 2005, Plant Molecular Biology.

[61]  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.

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

[63]  Steven M. Reppert,et al.  Rhythmic histone acetylation underlies transcription in the mammalian circadian clock , 2003, Nature.

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

[65]  P. Más,et al.  A Functional Link between Rhythmic Changes in Chromatin Structure and the Arabidopsis Biological Clock[W] , 2007, The Plant Cell Online.

[66]  Jorge Gonçalves,et al.  The Arabidopsis Circadian Clock Incorporates a cADPR-Based Feedback Loop , 2007, Science.

[67]  E. Tobin,et al.  CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  M. W. Young,et al.  Posttranscriptional and Posttranslational Regulation of Clock Genes , 2004, Journal of biological rhythms.

[69]  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.

[70]  Anthony Hall,et al.  ELF4 Is Required for Oscillatory Properties of the Circadian Clock1[W] , 2007, Plant Physiology.

[71]  S. Kay,et al.  PRR3 Is a Vascular Regulator of TOC1 Stability in the Arabidopsis Circadian Clock[W][OA] , 2007, The Plant Cell Online.

[72]  Takao Kondo,et al.  No Transcription-Translation Feedback in Circadian Rhythm of KaiC Phosphorylation , 2005, Science.

[73]  Michael W Young,et al.  Interplay of circadian clocks and metabolic rhythms. , 2006, Annual review of genetics.

[74]  D. Weigel,et al.  Move on up, it's time for change--mobile signals controlling photoperiod-dependent flowering. , 2007, Genes & development.

[75]  S. Daan,et al.  Assembling a Clock for All Seasons: Are There M and E Oscillators in the Genes? , 2001, Journal of biological rhythms.

[76]  R. Green,et al.  CIRCADIAN CLOCK ASSOCIATED1 Transcript Stability and the Entrainment of the Circadian Clock in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[77]  P. Más,et al.  The proteasome-dependent degradation of CKB4 is regulated by the Arabidopsis biological clock. , 2006, The Plant journal : for cell and molecular biology.

[78]  Norio Iijima,et al.  Circadian and Light-Induced Transcription of Clock Gene Per1 Depends on Histone Acetylation and Deacetylation , 2004, Molecular and Cellular Biology.

[79]  T. Mizuno,et al.  Pseudo-Response Regulators (PRRs) or True Oscillator Components (TOCs). , 2005, Plant & cell physiology.

[80]  T. Mizoguchi,et al.  Kinase and phosphatase: the cog and spring of the circadian clock. , 2006, International review of cytology.