Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome

Critical to the maintenance of circadian rhythmicity is the cyclic expression of at least some components of the central oscillator. High-amplitude cycling of mRNA and protein abundance, protein phosphorylation and nuclear/cytoplasmic shuttling have all been implicated in the maintenance of circadian period. Here we use a newly characterized Arabidopsis suspension cell culture to establish that the rhythmic changes in the levels of the clock-associated F-box protein, ZTL, are posttranscriptionally controlled through different circadian phase-specific degradation rates. This proteolysis is proteasome dependent, implicating ZTL itself as substrate for ubiquitination. This demonstration of circadian phase-regulated degradation of an F-box protein, which itself controls circadian period, suggests a novel regulatory feedback mechanism among known circadian systems.

[1]  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.

[2]  Steven M. Reppert,et al.  Posttranslational Mechanisms Regulate the Mammalian Circadian Clock , 2001, Cell.

[3]  J. Christie,et al.  Phototropins 1 and 2: versatile plant blue-light receptors. , 2002, Trends in plant science.

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

[5]  P. Howley,et al.  Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. , 1998, Molecular cell.

[6]  A. Mccarthy.  Development , 1996, Current Opinion in Neurobiology.

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

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

[9]  L. Cooley,et al.  The kelch repeat superfamily of proteins: propellers of cell function. , 2000, Trends in cell biology.

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

[11]  J. Dunlap,et al.  White Collar-1, a Circadian Blue Light Photoreceptor, Binding to the frequency Promoter , 2002, Science.

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

[13]  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.

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

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

[16]  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.

[17]  J. Christie,et al.  LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[20]  P. Quail,et al.  Coordination of phytochrome levels in phyB mutants of Arabidopsis as revealed by apoprotein-specific monoclonal antibodies. , 1998, Genetics.

[21]  R. Amasino,et al.  Natural allelic variation identifies new genes in the Arabidopsis circadian system. , 1999, The Plant journal : for cell and molecular biology.

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

[23]  S. Kaeppler,et al.  Epigenetic aspects of somaclonal variation in plants , 2000, Plant Molecular Biology.

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

[25]  S. Kay,et al.  tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the arabidopsis circadian oscillator. , 2002, Developmental cell.

[26]  Xing Wang Deng,et al.  Targeted destabilization of HY5 during light-regulated development of Arabidopsis , 2000, Nature.

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

[28]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[29]  T. Kiyosue,et al.  LKP1 (LOV kelch protein 1): a factor involved in the regulation of flowering time in arabidopsis. , 2000, The Plant journal : for cell and molecular biology.

[30]  A. Sehgal,et al.  A role for the proteasome in the light response of the timeless clock protein. , 1999, Science.

[31]  M. Peter,et al.  Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A Hall,et al.  Circadian clock-regulated expression of phytochrome and cryptochrome genes in Arabidopsis. , 2001, Plant physiology.

[33]  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.

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

[35]  K. Gardner,et al.  PAS Domain-Mediated WC-1/WC-2 Interaction Is Essential for Maintaining the Steady-State Level of WC-1 and the Function of Both Proteins in Circadian Clock and Light Responses of Neurospora , 2002, Molecular and Cellular Biology.

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

[37]  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.

[38]  R. Deshaies.  SCF and Cullin/Ring H2-based ubiquitin ligases. , 1999, Annual review of cell and developmental biology.

[39]  W. Krek,et al.  The F‐box protein Skp2 is a ubiquitylation target of a Cul1‐based core ubiquitin ligase complex: evidence for a role of Cul1 in the suppression of Skp2 expression in quiescent fibroblasts , 2000, The EMBO journal.

[40]  K. Moffat,et al.  Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction , 2001, Proceedings of the National Academy of Sciences of the United States of America.