Chromatin remodeling and alternative splicing: pre- and post-transcriptional regulation of the Arabidopsis circadian clock.

Circadian clocks are endogenous mechanisms that translate environmental cues into temporal information to generate the 24-h rhythms in metabolism and physiology. The circadian function relies on the precise regulation of rhythmic gene expression at the core of the oscillator, which temporally modulates the genome transcriptional activity in virtually all multicellular organisms examined to date. Emerging evidence in plants suggests a highly sophisticated interplay between the circadian patterns of gene expression and the rhythmic changes in chromatin remodeling and histone modifications. Alternative precursor messenger RNA (pre-mRNA) splicing has also been recently defined as a fundamental pillar within the circadian system, providing the required plasticity and specificity for fine-tuning the circadian clock. This review highlights the relationship between the plant circadian clock with both chromatin remodeling and alternative splicing and compares the similarities and divergences with analogous studies in animal circadian systems.

[1]  Z. Chen,et al.  Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids , 2008, Nature.

[2]  A. Kornblihtt,et al.  Alternative splicing adds a new loop to the circadian clock , 2011, Communicative & integrative biology.

[3]  Rossana Henriques,et al.  Circadian clock regulates dynamic chromatin modifications associated with Arabidopsis CCA1/LHY and TOC1 transcriptional rhythms. , 2012, Plant & cell physiology.

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

[5]  Paloma Mas,et al.  A methyl transferase links the circadian clock to the regulation of alternative splicing , 2010, Nature.

[6]  Steven A. Brown,et al.  PERIOD1-Associated Proteins Modulate the Negative Limb of the Mammalian Circadian Oscillator , 2005, Science.

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

[8]  R. Green,et al.  Evidence for the adaptive significance of circadian rhythms. , 2009, Ecology letters.

[9]  S. Kay,et al.  Global approaches for telling time: omics and the Arabidopsis circadian clock. , 2013, Seminars in cell & developmental biology.

[10]  Crisanto Gutierrez,et al.  A chromatin link that couples cell division to root epidermis patterning in Arabidopsis , 2007, Nature.

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

[12]  Steve A. Kay,et al.  Clocks not winding down: unravelling circadian networks , 2010, Nature Reviews Molecular Cell Biology.

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

[14]  Tao Liu,et al.  A Circadian Rhythm Orchestrated by Histone Deacetylase 3 Controls Hepatic Lipid Metabolism , 2011, Science.

[15]  Steven P. Gygi,et al.  Comprehensive proteomic analysis of the human spliceosome , 2002, Nature.

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

[17]  R. Costa.  Introduction: taking stock of circadian clock complexity , 2001 .

[18]  C. R. McClung,et al.  SKIP Is a Component of the Spliceosome Linking Alternative Splicing and the Circadian Clock in Arabidopsis[W] , 2012, Plant Cell.

[19]  Satchidananda Panda,et al.  Histone Lysine Demethylase JARID1a Activates CLOCK-BMAL1 and Influences the Circadian Clock , 2011, Science.

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

[21]  R. Reenan,et al.  The intricate relationship between RNA structure, editing, and splicing. , 2012, Seminars in cell & developmental biology.

[22]  Bing Li,et al.  The Role of Chromatin during Transcription , 2007, Cell.

[23]  J. Takahashi,et al.  Circadian Clock Feedback Cycle Through NAMPT-Mediated NAD+ Biosynthesis , 2009, Science.

[24]  J. Zhai,et al.  Mutations in the Type II Protein Arginine Methyltransferase AtPRMT5 Result in Pleiotropic Developmental Defects in Arabidopsis1[C][OA] , 2007, Plant Physiology.

[25]  Robert J. Schmitz,et al.  Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana , 2008, Proceedings of the National Academy of Sciences.

[26]  J. Workman,et al.  Signals and combinatorial functions of histone modifications. , 2011, Annual review of biochemistry.

[27]  John W. S. Brown,et al.  Alternative Splicing Mediates Responses of the Arabidopsis Circadian Clock to Temperature Changes[W] , 2012, Plant Cell.

[28]  Dan Li,et al.  Arabidopsis Floral Initiator SKB1 Confers High Salt Tolerance by Regulating Transcription and Pre-mRNA Splicing through Altering Histone H4R3 and Small Nuclear Ribonucleoprotein LSM4 Methylation[C][W] , 2011, Plant Cell.

[29]  K. Shinozaki,et al.  Arabidopsis HDA6 Regulates Locus-Directed Heterochromatin Silencing in Cooperation with MET1 , 2011, PLoS genetics.

[30]  K. Uchida,et al.  Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. , 2007, The Plant journal : for cell and molecular biology.

[31]  P. Sassone-Corsi,et al.  Circadian Control of the NAD+ Salvage Pathway by CLOCK-SIRT1 , 2009, Science.

[32]  Minyoung Lee,et al.  A Self-Regulatory Circuit of CIRCADIAN CLOCK-ASSOCIATED1 Underlies the Circadian Clock Regulation of Temperature Responses in Arabidopsis[W] , 2012, Plant Cell.

[33]  Xiaoyu Zhang.  The Epigenetic Landscape of Plants , 2008, Science.

[34]  K. Apel,et al.  Circadian clock-regulated expression of an RNA-binding protein in Arabidopsis: characterisation of a minimal promoter element , 1999, Molecular and General Genetics MGG.

[35]  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.

[36]  Y. Noh,et al.  Rhythmic oscillation of histone acetylation and methylation at the Arabidopsis central clock loci , 2012, Molecules and cells.

[37]  Colleen J Doherty,et al.  Circadian control of global gene expression patterns. , 2010, Annual review of genetics.

[38]  S. Brenner,et al.  Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements , 2007, Nature.

[39]  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.

[40]  Yamile Marquez,et al.  Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis , 2012, Genome research.

[41]  R. F. Luco,et al.  Epigenetics in Alternative Pre-mRNA Splicing , 2011, Cell.

[42]  Julie A. Law,et al.  SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis , 2010, Proceedings of the National Academy of Sciences.

[43]  Paolo Sassone-Corsi,et al.  The NAD+-Dependent Deacetylase SIRT1 Modulates CLOCK-Mediated Chromatin Remodeling and Circadian Control , 2008, Cell.

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

[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]  P. Más,et al.  Chromatin, photoperiod and the Arabidopsis circadian clock: a question of time. , 2008, Seminars in cell & developmental biology.

[47]  Downstream of the plant circadian clock: output pathways for the control of physiology and development. , 2011, Essays in biochemistry.

[48]  Paolo Sassone-Corsi,et al.  The histone methyltransferase MLL1 permits the oscillation of circadian gene expression , 2010, Nature Structural &Molecular Biology.

[49]  T. Mizuno,et al.  PSEUDO-RESPONSE REGULATORS 9, 7, and 5 Are Transcriptional Repressors in the Arabidopsis Circadian Clock[W][OA] , 2010, Plant Cell.

[50]  R. Klose,et al.  Dynamic protein methylation in chromatin biology , 2008, Cellular and Molecular Life Sciences.

[51]  Xing Wang Deng,et al.  Dynamic Landscapes of Four Histone Modifications during Deetiolation in Arabidopsis[W] , 2009, The Plant Cell Online.

[52]  K. Chong,et al.  SKB1‐mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis , 2007, The EMBO journal.

[53]  C. R. McClung,et al.  Network news: prime time for systems biology of the plant circadian clock. , 2010, Current opinion in genetics & development.

[54]  J. Takahashi,et al.  Transcriptional Architecture and Chromatin Landscape of the Core Circadian Clock in Mammals , 2012, Science.

[55]  P. Más,et al.  Mapping the Core of the Arabidopsis Circadian Clock Defines the Network Structure of the Oscillator , 2012, Science.

[56]  Michael F. Covington,et al.  Jumonji domain protein JMJD5 functions in both the plant and human circadian systems , 2010, Proceedings of the National Academy of Sciences.

[57]  Paul D. Shaw,et al.  An hnRNP-like RNA-binding protein affects alternative splicing by in vivo interaction with transcripts in Arabidopsis thaliana , 2012, Nucleic acids research.

[58]  A. Berr,et al.  Histone modifications in transcriptional activation during plant development. , 2011, Biochimica et biophysica acta.

[59]  Hwa Jung Lee,et al.  Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[60]  P. Más,et al.  Ordered changes in histone modifications at the core of the Arabidopsis circadian clock , 2012, Proceedings of the National Academy of Sciences.

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

[62]  L. Bruno,et al.  Histone H2B monoubiquitination is required to reach maximal transcript levels of circadian clock genes in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[63]  K. Shinozaki,et al.  Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. , 2008, Plant & cell physiology.

[64]  T. Nilsen,et al.  Expansion of the eukaryotic proteome by alternative splicing , 2010, Nature.

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

[66]  Felix Naef,et al.  Cold-Inducible RNA-Binding Protein Modulates Circadian Gene Expression Posttranscriptionally , 2012, Science.

[67]  C. Will,et al.  The Spliceosome: Design Principles of a Dynamic RNP Machine , 2009, Cell.

[68]  P. Más,et al.  Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation. , 2011, The Plant journal : for cell and molecular biology.

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

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

[71]  Steve A. Kay,et al.  The ELF4-ELF3-LUX Complex Links the Circadian Clock to Diurnal Control of Hypocotyl Growth , 2011, Nature.

[72]  P. Más,et al.  Circadian clock function in Arabidopsis thaliana: time beyond transcription. , 2008, Trends in cell biology.

[73]  Stéphane Robin,et al.  Integrative epigenomic mapping defines four main chromatin states in Arabidopsis , 2011, The EMBO journal.

[74]  Takeshi Mizuno,et al.  Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model , 2010, Molecular Systems Biology.

[75]  V. Kruys,et al.  The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylation-dependent mechanism and acts as a translational repressor. , 2007, Experimental cell research.

[76]  Anthony Hall,et al.  Ecological implications of plants ability to tell the time. , 2009, Ecology letters.

[77]  C. Weitz,et al.  A Molecular Mechanism for Circadian Clock Negative Feedback , 2011, Science.

[78]  D. Cane,et al.  The nonsense-mediated decay RNA surveillance pathway. , 2007, Annual review of biochemistry.

[79]  B. Williams,et al.  Mutation of Arabidopsis SPLICEOSOMAL TIMEKEEPER LOCUS1 Causes Circadian Clock Defects[W] , 2012, Plant Cell.

[80]  E. Tobin,et al.  The Jumonji C Domain-Containing Protein JMJ30 Regulates Period Length in the Arabidopsis Circadian Clock1[W][OA] , 2010, Plant Physiology.

[81]  R. Tóth,et al.  Plant development goes like clockwork. , 2010, Trends in genetics : TIG.

[82]  T. Imaizumi,et al.  Circadian clock-regulated physiological outputs: dynamic responses in nature. , 2013, Seminars in cell & developmental biology.

[83]  C. Kyriacou,et al.  Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[84]  Peng Cui,et al.  Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing , 2010, Proceedings of the National Academy of Sciences.

[85]  Florian Kreppel,et al.  SIRT1 Regulates Circadian Clock Gene Expression through PER2 Deacetylation , 2008, Cell.

[86]  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.

[87]  Irmtraud M. Meyer,et al.  Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis , 2008, Nucleic acids research.

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

[89]  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.

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

[91]  Siren R. Veflingstad,et al.  Emerging design principles in the Arabidopsis circadian clock. , 2013, Seminars in cell & developmental biology.

[92]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[93]  Steve A. Kay,et al.  Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor , 2012, Proceedings of the National Academy of Sciences.

[94]  D. Staiger,et al.  Spotlight on post-transcriptional control in the circadian system , 2010, Cellular and Molecular Life Sciences.

[95]  W. Barbazuk,et al.  Genome-wide analyses of alternative splicing in plants: opportunities and challenges. , 2008, Genome research.

[96]  R. Amasino,et al.  Regulation of Flowering Time by Histone Acetylation in Arabidopsis , 2003, Science.

[97]  A. Berr,et al.  Arabidopsis SET DOMAIN GROUP2 Is Required for H3K4 Trimethylation and Is Crucial for Both Sporophyte and Gametophyte Development[C][W] , 2010, Plant Cell.

[98]  T. Mockler,et al.  Unproductive alternative splicing and nonsense mRNAs: A widespread phenomenon among plant circadian clock genes , 2012, Biology Direct.

[99]  A. Millar,et al.  The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops , 2012, Molecular systems biology.

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

[101]  Shiyong Song,et al.  AtGRP7 is involved in the regulation of abscisic acid and stress responses in arabidopsis , 2006, Cellular & Molecular Biology Letters.

[102]  C. R. McClung,et al.  Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[103]  T. Kouzarides.  Chromatin Modifications and Their Function , 2007, Cell.

[104]  C Robertson McClung,et al.  Provided for Non-commercial Research and Educational Use Only. Not for Reproduction, Distribution or Commercial Use. the Genetics of Plant Clocks , 2022 .

[105]  Henry D. Priest,et al.  Genome-wide mapping of alternative splicing in Arabidopsis thaliana. , 2010, Genome research.

[106]  A. Kornblihtt,et al.  Alternative splicing at the right time , 2011, RNA biology.

[107]  Jason P. DeBruyne,et al.  The Polycomb Group Protein EZH2 Is Required for Mammalian Circadian Clock Function*♦ , 2006, Journal of Biological Chemistry.

[108]  Eric T. Wang,et al.  Alternative Isoform Regulation in Human Tissue Transcriptomes , 2008, Nature.

[109]  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.