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PMID: 22917516 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Review

Complexity in the wiring and regulation of plant circadian networks.

Current biology : CB ·Vol. 22 ·No. 16 ·2012-08-21 ·Pages R648-57

Nagel DH, Kay SA

Abstract

Endogenous circadian rhythms regulate many aspects of an organism's behavior, physiology and development. These daily oscillations synchronize with the environment to generate robust rhythms, resulting in enhanced fitness and growth vigor in plants. Collective studies over the years have focused on understanding the transcription-based oscillator in Arabidopsis. Recent advances combining mechanistic data with genome-wide approaches have contributed significantly to a more comprehensive understanding of the molecular interactions within the oscillator, and with clock-controlled pathways. This review focuses on the regulatory mechanisms within the oscillator, highlighting key connections between new and existing components, and direct mechanistic links to downstream pathways that control overt rhythms in the whole plant.

MeSH Terms
Arabidopsis/physiology Circadian Clocks Circadian Rhythm Gene Expression Regulation, Plant Gene Regulatory Networks
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Nagel Dawn H
Section of Cell and Developmental Biology, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093, USA.
Kay Steve A
References (116)
116 references, click to expand
  1. Jumonji domain protein JMJD5 functions in both the plant and human circadian systems.
    Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21623-8 PMID: 21115819
  2. Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants.
    Plant Cell Physiol. 2008 Mar;49(3):481-7 PMID: 18202002
  3. Expansion of the eukaryotic proteome by alternative splicing.
    Nature. 2010 Jan 28;463(7280):457-63 PMID: 20110989
  4. The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots.
    Science. 2008 Dec 19;322(5909):1832-5 PMID: 19095940
  5. Regulation of output from the plant circadian clock.
    FEBS J. 2007 Jan;274(2):335-45 PMID: 17229141
  6. PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock.
    Plant Cell. 2010 Mar;22(3):594-605 PMID: 20233950
  7. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops.
    Mol Syst Biol. 2012 Mar 06;8:574 PMID: 22395476
  8. Ubiquitination of LHY by SINAT5 regulates flowering time and is inhibited by DET1.
    Biochem Biophys Res Commun. 2010 Jul 23;398(2):242-6 PMID: 20599732
  9. LIGHT-REGULATED WD1 and PSEUDO-RESPONSE REGULATOR9 form a positive feedback regulatory loop in the Arabidopsis circadian clock.
    Plant Cell. 2011 Feb;23(2):486-98 PMID: 21357491
  10. Isolation of circadian-associated genes in Brassica rapa by comparative genomics with Arabidopsis thaliana.
    Mol Cells. 2007 Apr 30;23(2):145-53 PMID: 17464190
  11. GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2011 Jul 12;108(28):11698-703 PMID: 21709243
  12. A role for casein kinase 2alpha in the Drosophila circadian clock.
    Nature. 2002 Dec 19-26;420(6917):816-20 PMID: 12447397
  13. The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabidopsis.
    PLoS Genet. 2010 Nov 04;6(11):e1001201 PMID: 21079791
  14. Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules.
    PLoS Genet. 2008 Feb;4(2):e14 PMID: 18248097
  15. Chromatin, photoperiod and the Arabidopsis circadian clock: a question of time.
    Semin Cell Dev Biol. 2008 Dec;19(6):554-9 PMID: 18708153
  16. PRR3 Is a vascular regulator of TOC1 stability in the Arabidopsis circadian clock.
    Plant Cell. 2007 Nov;19(11):3462-73 PMID: 18055606
  17. Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana.
    Plant Cell Physiol. 2011 Aug;52(8):1315-29 PMID: 21666227
  18. Resonating circadian clocks enhance fitness in cyanobacteria.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8660-4 PMID: 9671734
  19. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10387-92 PMID: 16006522
  20. DET1 regulates the proteasomal degradation of LHY, a component of the Arabidopsis circadian clock.
    Plant Mol Biol. 2005 Mar;57(5):761-71 PMID: 15988568
  21. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering.
    Cell. 1998 Jun 26;93(7):1219-29 PMID: 9657154
  22. Involvement of the protein kinase CK2 in the regulation of mammalian circadian rhythms.
    Sci Signal. 2009 Jun 02;2(73):ra26 PMID: 19491384
  23. EARLY FLOWERING3 encodes a novel protein that regulates circadian clock function and flowering in Arabidopsis.
    Plant Cell. 2001 Jun;13(6):1281-92 PMID: 11402160
  24. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids.
    Nature. 2009 Jan 15;457(7227):327-31 PMID: 19029881
  25. Post-translational modifications in circadian rhythms.
    Trends Biochem Sci. 2009 Oct;34(10):483-90 PMID: 19740663
  26. Signaling to the circadian clock: plasticity by chromatin remodeling.
    Curr Opin Cell Biol. 2007 Apr;19(2):230-7 PMID: 17317138
  27. Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination.
    Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):7251-6 PMID: 19359492
  28. The circadian system in higher plants.
    Annu Rev Plant Biol. 2009;60:357-77 PMID: 19575587
  29. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis.
    Nat Cell Biol. 2011 May;13(5):616-22 PMID: 21499259
  30. Genetic interactions among late-flowering mutants of Arabidopsis.
    Genetics. 1998 Feb;148(2):885-92 PMID: 9504934
  31. CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3292-7 PMID: 14978263
  32. Genomic analysis of circadian clock-, light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of auxin signaling in Arabidopsis.
    Plant Physiol. 2011 May;156(1):357-72 PMID: 21430186
  33. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.
    Nature. 2001 Apr 26;410(6832):1116-20 PMID: 11323677
  34. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.
    Genome Biol. 2008;9(8):R130 PMID: 18710561
  35. The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis.
    Cold Spring Harb Symp Quant Biol. 2007;72:353-63 PMID: 18419293
  36. Functional implication of the MYB transcription factor RVE8/LCL5 in the circadian control of histone acetylation.
    Plant J. 2011 Apr;66(2):318-29 PMID: 21205033
  37. Circadian rhythms from multiple oscillators: lessons from diverse organisms.
    Nat Rev Genet. 2005 Jul;6(7):544-56 PMID: 15951747
  38. Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2.
    New Phytol. 2009 Mar;181(4):808-819 PMID: 19140936
  39. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes.
    Plant Cell. 2012 Mar;24(3):961-81 PMID: 22408072
  40. KDM8, a H3K36me2 histone demethylase that acts in the cyclin A1 coding region to regulate cancer cell proliferation.
    Proc Natl Acad Sci U S A. 2010 May 25;107(21):9671-6 PMID: 20457893
  41. An expanding universe of circadian networks in higher plants.
    Trends Plant Sci. 2010 May;15(5):259-65 PMID: 20382065
  42. A complex genetic interaction between Arabidopsis thaliana TOC1 and CCA1/LHY in driving the circadian clock and in output regulation.
    Genetics. 2007 Jul;176(3):1501-10 PMID: 17483414
  43. Two new clock proteins, LWD1 and LWD2, regulate Arabidopsis photoperiodic flowering.
    Plant Physiol. 2008 Oct;148(2):948-59 PMID: 18676661
  44. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock.
    Science. 2009 Mar 13;323(5920):1481-5 PMID: 19286557
  45. Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing.
    Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):19114-9 PMID: 20956294
  46. Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model.
    Mol Syst Biol. 2010 Sep 21;6:416 PMID: 20865009
  47. Photoperiodic control of flowering: not only by coincidence.
    Trends Plant Sci. 2006 Nov;11(11):550-8 PMID: 17035069
  48. CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL function synergistically in the circadian clock of Arabidopsis.
    Plant Physiol. 2009 Jun;150(2):834-43 PMID: 19218364
  49. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis.
    EMBO J. 2002 May 15;21(10):2441-50 PMID: 12006496
  50. The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm.
    Plant Cell Physiol. 2003 Nov;44(11):1229-36 PMID: 14634161
  51. In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development.
    Plant Physiol. 2009 Mar;149(3):1462-77 PMID: 19091878
  52. TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana.
    Plant Cell. 2010 Dec;22(12):3921-34 PMID: 21183706
  53. Rhythmic growth explained by coincidence between internal and external cues.
    Nature. 2007 Jul 19;448(7151):358-61 PMID: 17589502
  54. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors.
    Plant J. 2008 Jan;53(2):312-23 PMID: 18047474
  55. Kinase and phosphatase: the cog and spring of the circadian clock.
    Int Rev Cytol. 2006;250:47-72 PMID: 16861063
  56. Circadian-controlled basic/helix-loop-helix factor, PIL6, implicated in light-signal transduction in Arabidopsis thaliana.
    Plant Cell Physiol. 2004 Aug;45(8):1078-86 PMID: 15356333
  57. Cell autonomous and cell-type specific circadian rhythms in Arabidopsis.
    Plant J. 2011 Nov;68(3):520-31 PMID: 21781194
  58. PHYTOCLOCK 1 encoding a novel GARP protein essential for the Arabidopsis circadian clock.
    Genes Cells. 2005 Oct;10(10):963-72 PMID: 16164597
  59. Post-translational regulation of the Arabidopsis circadian clock through selective proteolysis and phosphorylation of pseudo-response regulator proteins.
    J Biol Chem. 2008 Aug 22;283(34):23073-83 PMID: 18562312
  60. Evidence for the adaptive significance of circadian rhythms.
    Ecol Lett. 2009 Sep;12(9):970-81 PMID: 19566794
  61. Timing of plant immune responses by a central circadian regulator.
    Nature. 2011 Feb 3;470(7332):110-4 PMID: 21293378
  62. Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana.
    J Theor Biol. 2005 Jun 7;234(3):383-93 PMID: 15784272
  63. Targeted degradation of PSEUDO-RESPONSE REGULATOR5 by an SCFZTL complex regulates clock function and photomorphogenesis in Arabidopsis thaliana.
    Plant Cell. 2007 Aug;19(8):2516-30 PMID: 17693530
  64. JMJD5 Functions in concert with TOC1 in the arabidopsis circadian system.
    Plant Signal Behav. 2011 Mar;6(3):445-8 PMID: 21358285
  65. BROTHER OF LUX ARRHYTHMO is a component of the Arabidopsis circadian clock.
    Plant Cell. 2011 Mar;23(3):961-72 PMID: 21447790
  66. Temperature-modulated alternative splicing and promoter use in the Circadian clock gene frequency.
    Mol Biol Cell. 2005 Dec;16(12):5563-71 PMID: 16195340
  67. Phylogenetic footprint of the plant clock system in angiosperms: evolutionary processes of pseudo-response regulators.
    BMC Evol Biol. 2010 May 01;10:126 PMID: 20433765
  68. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog.
    Science. 2000 Aug 4;289(5480):768-71 PMID: 10926537
  69. PRR5 regulates phosphorylation, nuclear import and subnuclear localization of TOC1 in the Arabidopsis circadian clock.
    EMBO J. 2010 Jun 2;29(11):1903-15 PMID: 20407420
  70. Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis.
    Plant Cell. 2005 Jul;17(7):1926-40 PMID: 15923346
  71. The circadian clock that controls gene expression in Arabidopsis is tissue specific.
    Plant Physiol. 2002 Sep;130(1):102-10 PMID: 12226490
  72. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana.
    Nature. 2003 Dec 4;426(6966):567-70 PMID: 14654842
  73. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene.
    Plant Cell. 1997 Apr;9(4):491-507 PMID: 9144958
  74. Temporal repression of core circadian genes is mediated through EARLY FLOWERING 3 in Arabidopsis.
    Curr Biol. 2011 Jan 25;21(2):120-5 PMID: 21236675
  75. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering.
    Science. 2004 Feb 13;303(5660):1003-6 PMID: 14963328
  76. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock.
    Plant Cell. 2007 Jul;19(7):2111-23 PMID: 17616736
  77. A role for casein kinase 2 in the mechanism underlying circadian temperature compensation.
    Cell. 2009 May 15;137(4):749-60 PMID: 19450520
  78. Testing time: can ethanol-induced pulses of proposed oscillator components phase shift rhythms in Arabidopsis?
    J Biol Rhythms. 2008 Dec;23(6):463-71 PMID: 19060255
  79. Phase-specific circadian clock regulatory elements in Arabidopsis.
    Plant Physiol. 2002 Oct;130(2):627-38 PMID: 12376630
  80. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.
    Science. 2001 Aug 3;293(5531):880-3 PMID: 11486091
  81. F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression.
    Plant Cell. 2010 Mar;22(3):606-22 PMID: 20354196
  82. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.
    Science. 2005 Jul 22;309(5734):630-3 PMID: 16040710
  83. Does the core circadian clock in the moss Physcomitrella patens (Bryophyta) comprise a single loop?
    BMC Plant Biol. 2010 Jun 15;10:109 PMID: 20550695
  84. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression.
    Cell. 1998 Jun 26;93(7):1207-17 PMID: 9657153
  85. Long and short isoforms of Neurospora clock protein FRQ support temperature-compensated circadian rhythms.
    FEBS Lett. 2007 Dec 22;581(30):5759-64 PMID: 18037381
  86. Control of daily transcript oscillations in Drosophila by light and the circadian clock.
    PLoS Genet. 2006 Mar;2(3):e39 PMID: 16565745
  87. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis.
    Plant J. 1999 Jan;17(1):63-71 PMID: 10069068
  88. ELF3 recruitment to the PRR9 promoter requires other Evening Complex members in the Arabidopsis circadian clock.
    Plant Signal Behav. 2012 Feb;7(2):170-3 PMID: 22307044
  89. Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark.
    FEBS Lett. 2006 Feb 20;580(5):1193-7 PMID: 16457821
  90. Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf.
    Proc Natl Acad Sci U S A. 2012 Apr 24;109(17):6757-62 PMID: 22496591
  91. Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock.
    Mol Cell. 2011 Sep 2;43(5):703-12 PMID: 21884973
  92. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor.
    Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):3167-72 PMID: 22315425
  93. Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21211-6 PMID: 21097700
  94. Genome-wide mapping of alternative splicing in Arabidopsis thaliana.
    Genome Res. 2010 Jan;20(1):45-58 PMID: 19858364
  95. The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose.
    Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):5104-9 PMID: 21383174
  96. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock.
    Curr Biol. 2005 Jan 11;15(1):47-54 PMID: 15649364
  97. LUX ARRHYTHMO encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock.
    Curr Biol. 2011 Jan 25;21(2):126-33 PMID: 21236673
  98. ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY.
    Plant J. 2005 Oct;44(2):300-13 PMID: 16212608
  99. Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote ostreococcus.
    Plant Cell. 2009 Nov;21(11):3436-49 PMID: 19948792
  100. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors.
    Plant Cell. 2004 Nov;16(11):3033-44 PMID: 15486100
  101. Modulation of environmental responses of plants by circadian clocks.
    Plant Cell Environ. 2007 Mar;30(3):333-349 PMID: 17263778
  102. ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light.
    Nature. 2007 Sep 20;449(7160):356-60 PMID: 17704763
  103. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana.
    Nature. 2002 Sep 5;419(6902):74-7 PMID: 12214234
  104. Circadian rhythms confer a higher level of fitness to Arabidopsis plants.
    Plant Physiol. 2002 Jun;129(2):576-84 PMID: 12068102
  105. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana.
    Development. 1998 Feb;125(3):485-94 PMID: 9425143
  106. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock.
    PLoS Genet. 2011 Mar;7(3):e1001350 PMID: 21483796
  107. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator.
    Science. 2012 Apr 6;336(6077):75-9 PMID: 22403178
  108. A methyl transferase links the circadian clock to the regulation of alternative splicing.
    Nature. 2010 Nov 4;468(7320):112-6 PMID: 20962777
  109. Circadian clock function in Arabidopsis thaliana: time beyond transcription.
    Trends Cell Biol. 2008 Jun;18(6):273-81 PMID: 18468438
  110. Circadian clock mutants in Arabidopsis identified by luciferase imaging.
    Science. 1995 Feb 24;267(5201):1161-3 PMID: 7855595
  111. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth.
    Nature. 2011 Jul 13;475(7356):398-402 PMID: 21753751
  112. The Jumonji C domain-containing protein JMJ30 regulates period length in the Arabidopsis circadian clock.
    Plant Physiol. 2011 Feb;155(2):906-15 PMID: 21139085
  113. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains.
    EMBO J. 1999 Sep 1;18(17):4679-88 PMID: 10469647
  114. A role for protein kinase casein kinase2 α-subunits in the Arabidopsis circadian clock.
    Plant Physiol. 2011 Nov;157(3):1537-45 PMID: 21900482
  115. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock.
    Plant Cell. 2012 Feb;24(2):428-43 PMID: 22327739
  116. The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis.
    Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12362-6 PMID: 10535927
Article Info
Journal
Current biology : CB
Abbr.
Curr Biol
ISSN
1879-0445
DOI
10.1016/j.cub.2012.07.025
Published
2012-08-21
Pages
R648-57
Language
English
Region
England
NLM ID
9107782
PMCID
PMC3427731
Subset
IM
Grants
NIGMS NIH HHS · F32GM090378 · United States
NIGMS NIH HHS · R01 GM067837 · United States
NIGMS NIH HHS · F32 GM090375 · United States
NIGMS NIH HHS · GM067837 · United States
NIGMS NIH HHS · R01 GM056006 · United States
NIGMS NIH HHS · GM056006 · United States
Corrections
ErratumIn
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External Links
PubMed source DOI: 10.1016/j.cub.2012.07.025 PMC Full Text View journal details
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