Circadian clock signaling in Arabidopsis thaliana: from gene expression to physiology and development.

The daily rotation of the earth on its axis leads to predictable periodic fluctuations of environmental conditions. Accordingly, most organisms have evolved an internal timing mechanism, the circadian clock, which is able to recognize these 24-hour rhythmic oscillations. In plants, the temporal synchronization of physiology with the environment is essential for successful plant growth and development. The intimate connection between light signaling pathways and the circadian oscillator allows the anticipation of the environmental transitions and the measurement of day-length as an indicator of changing seasons. In recent years, significant advances have been made in the genetic and molecular dissection of the plant circadian system, mostly in Arabidopsis thaliana. The overall plant clock organization is highly complex; the system seems to include several input pathways, tightly regulated central oscillators and a myriad of outputs. The molecular cloning and characterization of a number of clock components has greatly improved our view of the plant central oscillator and additional players will most likely come into place very soon. Molecular mechanisms underlying circadian clock function are also beginning to be characterized. The emerging model relies on negative feedback loops at the core of the oscillator. Additional levels of post-transcriptional and post-translational regulation also contribute to the generation and maintenance of the rhythms. Globally, these studies have shed new light on how the clock coordinates plant physiology and development with the daily and seasonal environmental cycles.

[1]  E. Tobin,et al.  All in good time: the Arabidopsis circadian clock. , 2000, Trends in plant science.

[2]  J. Casal,et al.  Temperature-dependent internode elongation in vegetative plants of Arabidopsis thaliana lacking phytochrome B and cryptochrome 1 , 2000, Planta.

[3]  D. E. Somers,et al.  Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. , 1999, Science.

[4]  Takashi Araki,et al.  Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. , 2002, Plant & cell physiology.

[5]  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.

[6]  I. Edery.  Role of posttranscriptional regulation in circadian clocks: lessons from Drosophila. , 1999, Chronobiology international.

[7]  E. Huq,et al.  GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Yanovsky,et al.  A quadruple photoreceptor mutant still keeps track of time , 2000, Current Biology.

[9]  Michael F. Covington,et al.  ELF3 Encodes a Circadian Clock–Regulated Nuclear Protein That Functions in an Arabidopsis PHYB Signal Transduction Pathway , 2001, The Plant Cell Online.

[10]  D. E. Somers,et al.  Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. , 1998, Science.

[11]  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.

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

[13]  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.

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

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

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

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

[18]  A. Millar,et al.  Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. , 1999, The Plant journal : for cell and molecular biology.

[19]  G. Coupland,et al.  GIGANTEA: a circadian clock‐controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane‐spanning domains , 1999, The EMBO journal.

[20]  C. R. McClung,et al.  Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock , 2003, Science.

[21]  S. Kay,et al.  Functional interaction of phytochrome B and cryptochrome 2 , 2000, Nature.

[22]  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.

[23]  G. Coupland,et al.  Induction of flowering by seasonal changes in photoperiod , 2004, The EMBO journal.

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

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

[26]  A. Millar,et al.  Independent action of ELF3 and phyB to control hypocotyl elongation and flowering time. , 2000, Plant physiology.

[27]  T. Mizuno.  Plant response regulators implicated in signal transduction and circadian rhythm. , 2004, Current opinion in plant biology.

[28]  S. Golden,et al.  Resonating circadian clocks enhance fitness in cyanobacteria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  G. Coupland,et al.  Control of flowering time: interacting pathways as a basis for diversity. , 2002, The Plant cell.

[30]  S. Kay,et al.  Cryptochromes Are Required for Phytochrome Signaling to the Circadian Clock but Not for Rhythmicity , 2000, Plant Cell.

[31]  J. Ecker,et al.  An Arabidopsis circadian clock component interacts with both CRY1 and phyB , 2001, Nature.

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

[33]  T. Mizuno,et al.  Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. , 2000, Plant & cell physiology.

[34]  A. Millar,et al.  The Circadian Clock That Controls Gene Expression in Arabidopsis Is Tissue Specific1 , 2002, Plant Physiology.

[35]  Michael F. Covington,et al.  ELF 3 Encodes a Circadian Clock – Regulated Nuclear Protein That Functions in an Arabidopsis PHYB Signal Transduction Pathway , 2001 .

[36]  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.

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

[38]  D. Ravenscroft,et al.  Photoreceptor Regulation of CONSTANS Protein in Photoperiodic Flowering , 2004, Science.

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

[40]  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.

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

[42]  C Robertson McClung,et al.  CIRCADIAN RHYTHMS IN PLANTS. , 2003, Annual review of plant physiology and plant molecular biology.

[43]  R. Simon,et al.  The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors , 1995, Cell.

[44]  J. Chory,et al.  Activation tagging of the floral inducer FT. , 1999, Science.

[45]  K. Morris,et al.  Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J. Chory,et al.  The Arabidopsis SRR1 gene mediates phyB signaling and is required for normal circadian clock function. , 2003, Genes & development.

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

[48]  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.

[49]  A. Dickson.  On Evolution , 1884, Science.

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

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

[52]  G. Coupland,et al.  Shedding light on the circadian clock and the photoperiodic control of flowering. , 2003, Current opinion in plant biology.

[53]  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.

[54]  C. R. McClung,et al.  SPINDLY and GIGANTEA Interact and Act in Arabidopsis thaliana Pathways Involved in Light Responses, Flowering, and Rhythms in Cotyledon Movements , 2004, The Plant Cell Online.

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

[56]  Lin Sun,et al.  A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. , 1997, The Plant cell.

[57]  S. Kay,et al.  Time zones: a comparative genetics of circadian clocks , 2001, Nature Reviews Genetics.

[58]  S. Kay,et al.  FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis , 2003, Nature.

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

[60]  F. Tamanini,et al.  Nucleocytoplasmic shuttling and mCRY‐dependent inhibition of ubiquitylation of the mPER2 clock protein , 2002, The EMBO journal.

[61]  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.

[62]  Z. Schwarz‐Sommer,et al.  Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. , 2000, Science.

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

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

[65]  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.

[66]  Andrew J Millar,et al.  Input signals to the plant circadian clock. , 2003, Journal of experimental botany.

[67]  J. Dunlap,et al.  Genetic and molecular analysis of circadian rhythms in Neurospora. , 2001, Annual review of physiology.

[68]  C. Johnson.  Endogenous timekeepers in photosynthetic organisms. , 2001, Annual review of physiology.

[69]  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.

[70]  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.

[71]  S. Kay,et al.  Circadian photoperception. , 2001, Annual review of physiology.

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

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

[74]  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.

[75]  M. Tyers,et al.  The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. , 1999, Progress in biophysics and molecular biology.

[76]  K. Halliday,et al.  Changes in Photoperiod or Temperature Alter the Functional Relationships between Phytochromes and Reveal Roles for phyD and phyE1 , 2003, Plant Physiology.

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

[78]  J. Dunlap.  Molecular Bases for Circadian Clocks , 1999, Cell.

[79]  G. Coupland,et al.  The Evolution of CONSTANS-Like Gene Families in Barley, Rice, and Arabidopsis1 , 2003, Plant Physiology.

[80]  Christopher R. Jones,et al.  An hPer2 Phosphorylation Site Mutation in Familial Advanced Sleep Phase Syndrome , 2001, Science.

[81]  L. Mcintosh,et al.  Isolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering. , 2001, Plant physiology.

[82]  Y. Kobayashi,et al.  A pair of related genes with antagonistic roles in mediating flowering signals. , 1999, Science.

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

[84]  Robert J. Schaffer,et al.  Microarray Analysis of Diurnal and Circadian-Regulated Genes in Arabidopsis , 2001, The Plant Cell.

[85]  Andrew J Millar,et al.  The Circadian Clock. A Plant's Best Friend in a Spinning World1 , 2003, Plant Physiology.

[86]  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.

[87]  I. Edery,et al.  Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime , 2002, Nature.

[88]  François Rouyer,et al.  The F-box protein Slimb controls the levels of clock proteins Period and Timeless , 2002, Nature.

[89]  J. Dunlap.  Kinases and circadian clocks: per goes it alone. , 2004, Developmental Cell.

[90]  M. Yano,et al.  Hd1, a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS , 2000, Plant Cell.

[91]  Z. Peng,et al.  Reciprocal regulation of , 1996 .

[92]  S. Kay,et al.  Molecular basis of seasonal time measurement in Arabidopsis , 2002, Nature.