Home LiteratureArticle Details
PMID: 27663772 Published · epublish English Journal Article Review

The Plant Circadian Clock: From a Simple Timekeeper to a Complex Developmental Manager.

Cold Spring Harbor perspectives in biology ·Vol. 8 ·No. 12 ·2016-12-01

Sanchez SE, Kay SA

Abstract

The plant circadian clock allows organisms to anticipate the predictable changes in the environment by adjusting their developmental and physiological traits. In the last few years, it was determined that responses known to be regulated by the oscillator are also able to modulate clock performance. These feedback loops and their multilayer communications create a complex web, and confer on the clock network a role that exceeds the measurement of time. In this article, we discuss the current knowledge of the wiring of the clock, including the interplay with metabolism, hormone, and stress pathways in the model species Arabidopsis thaliana We outline the importance of this system in crop agricultural traits, highlighting the identification of natural alleles that alter the pace of the timekeeper. We report evidence supporting the understanding of the circadian clock as a master regulator of plant life, and we hypothesize on its relevant role in the adaptability to the environment and the impact on the fitness of most organisms.

MeSH Terms
Arabidopsis/genetics,physiology Circadian Clocks Gene Expression Regulation, Plant Genes, Plant
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sanchez Sabrina E
Department of Cell and Molecular Biology, The Scripps Research Institute, La Jolla, California 92093.
Kay Steve A
Department of Cell and Molecular Biology, The Scripps Research Institute, La Jolla, California 92093.
References (124)
124 references, click to expand
  1. Functional characterization of CCA1/LHY homolog genes, PpCCA1a and PpCCA1b, in the moss Physcomitrella patens.
    Plant J. 2009 Nov;60(3):551-63 PMID: 19624471
  2. GIGANTEA - an emerging story.
    Front Plant Sci. 2015 Jan 26;6:8 PMID: 25674098
  3. HvLUX1 is a candidate gene underlying the early maturity 10 locus in barley: phylogeny, diversity, and interactions with the circadian clock and photoperiodic pathways.
    New Phytol. 2013 Sep;199(4):1045-59 PMID: 23731278
  4. The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function.
    Plant Cell Physiol. 2005 Apr;46(4):609-19 PMID: 15695441
  5. Circadian control of chloroplast transcription by a nuclear-encoded timing signal.
    Science. 2013 Mar 15;339(6125):1316-9 PMID: 23493713
  6. Structure and function of Rubisco.
    Plant Physiol Biochem. 2008 Mar;46(3):275-91 PMID: 18294858
  7. Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis.
    Plant J. 2009 Feb;57(3):400-12 PMID: 18826427
  8. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.
    Science. 2000 Dec 15;290(5499):2110-3 PMID: 11118138
  9. The Arabidopsis circadian clock incorporates a cADPR-based feedback loop.
    Science. 2007 Dec 14;318(5857):1789-92 PMID: 18084825
  10. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3330-4 PMID: 11854454
  11. Wheels within wheels: the plant circadian system.
    Trends Plant Sci. 2014 Apr;19(4):240-9 PMID: 24373845
  12. Interactions between circadian and hormonal signalling in plants.
    Plant Mol Biol. 2009 Mar;69(4):419-27 PMID: 18855103
  13. Nutrient homeostasis within the plant circadian network.
    Front Plant Sci. 2015 Apr 29;6:299 PMID: 25972889
  14. Iron is involved in the maintenance of circadian period length in Arabidopsis.
    Plant Physiol. 2013 Mar;161(3):1409-20 PMID: 23307650
  15. A single locus confers tolerance to continuous light and allows substantial yield increase in tomato.
    Nat Commun. 2014 Aug 05;5:4549 PMID: 25093373
  16. TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock.
    Plant Cell. 2007 May;19(5):1522-36 PMID: 17496120
  17. 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
  18. HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock.
    Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):16172-7 PMID: 25352668
  19. Multiple phytohormones influence distinct parameters of the plant circadian clock.
    Genes Cells. 2006 Dec;11(12):1381-92 PMID: 17121545
  20. Genome-wide identification of CCA1 targets uncovers an expanded clock network in Arabidopsis.
    Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):E4802-10 PMID: 26261339
  21. Photosynthetic entrainment of the Arabidopsis thaliana circadian clock.
    Nature. 2013 Oct 31;502(7473):689-92 PMID: 24153186
  22. Circadian control of jasmonates and salicylates: the clock role in plant defense.
    Plant Signal Behav. 2013 Feb;8(2):e23123 PMID: 23299428
  23. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis.
    Proc Natl Acad Sci U S A. 2011 Apr 26;108(17):7241-6 PMID: 21471455
  24. Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism.
    Front Plant Sci. 2015 Apr 09;6:245 PMID: 25914715
  25. Circadian rhythms and post-transcriptional regulation in higher plants.
    Front Plant Sci. 2015 Jun 12;6:437 PMID: 26124767
  26. Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles.
    Plant Physiol. 2010 May;153(1):170-84 PMID: 20335405
  27. The TIME FOR COFFEE gene maintains the amplitude and timing of Arabidopsis circadian clocks.
    Plant Cell. 2003 Nov;15(11):2719-29 PMID: 14555691
  28. Multiple layers of posttranslational regulation refine circadian clock activity in Arabidopsis.
    Plant Cell. 2014 Jan;26(1):79-87 PMID: 24481076
  29. Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock.
    Curr Biol. 2005 Jan 11;15(1):47-54 PMID: 15649364
  30. Rethinking transcriptional activation in the Arabidopsis circadian clock.
    PLoS Comput Biol. 2014 Jul 17;10(7):e1003705 PMID: 25033214
  31. Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea.
    Plant J. 2015 Dec;84(5):937-48 PMID: 26466558
  32. Enhanced fitness conferred by naturally occurring variation in the circadian clock.
    Science. 2003 Nov 7;302(5647):1049-53 PMID: 14605371
  33. Time-dependent sequestration of RVE8 by LNK proteins shapes the diurnal oscillation of anthocyanin biosynthesis.
    Proc Natl Acad Sci U S A. 2015 Apr 21;112(16):5249-53 PMID: 25848001
  34. TIME FOR COFFEE is an essential component in the maintenance of metabolic homeostasis in Arabidopsis thaliana.
    Plant J. 2013 Oct;76(2):188-200 PMID: 23869666
  35. Balanced nucleocytosolic partitioning defines a spatial network to coordinate circadian physiology in plants.
    Dev Cell. 2013 Jul 15;26(1):73-85 PMID: 23830866
  36. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought.
    EMBO J. 2009 Dec 2;28(23):3745-57 PMID: 19816401
  37. 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
  38. Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid.
    Proc Natl Acad Sci U S A. 2015 Jul 28;112(30):9166-73 PMID: 26139525
  39. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior.
    Proc Natl Acad Sci U S A. 2012 Mar 20;109(12):4674-7 PMID: 22331878
  40. Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis.
    Plant Cell. 2004 Apr;16(4):956-66 PMID: 15031410
  41. 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
  42. Modulation of copper deficiency responses by diurnal and circadian rhythms in Arabidopsis thaliana.
    J Exp Bot. 2016 Jan;67(1):391-403 PMID: 26516126
  43. The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks.
    Curr Opin Plant Biol. 2013 Oct;16(5):621-9 PMID: 23856081
  44. Circadian oscillations of cytosolic and chloroplastic free calcium in plants.
    Science. 1995 Sep 29;269(5232):1863-5 PMID: 7569925
  45. Sweet immunity in the plant circadian regulatory network.
    J Exp Bot. 2013 Apr;64(6):1439-49 PMID: 23564957
  46. 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
  47. Mutations in CHLOROPLAST RNA BINDING provide evidence for the involvement of the chloroplast in the regulation of the circadian clock in Arabidopsis.
    Plant J. 2007 Aug;51(4):551-62 PMID: 17617174
  48. LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator.
    Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):12120-5 PMID: 23818596
  49. PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals.
    New Phytol. 2014 Jun;202(4):1126-41 PMID: 24571056
  50. A methyl transferase links the circadian clock to the regulation of alternative splicing.
    Nature. 2010 Nov 4;468(7320):112-6 PMID: 20962777
  51. REVEILLE8 and PSEUDO-REPONSE REGULATOR5 form a negative feedback loop within the Arabidopsis circadian clock.
    PLoS Genet. 2011 Mar;7(3):e1001350 PMID: 21483796
  52. Sensitive to freezing6 integrates cellular and environmental inputs to the plant circadian clock.
    Plant Physiol. 2008 Sep;148(1):293-303 PMID: 18614706
  53. FBH1 affects warm temperature responses in the Arabidopsis circadian clock.
    Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14595-600 PMID: 25246594
  54. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.
    Plant Cell. 2005 Dec;17(12):3257-81 PMID: 16299223
  55. Copper homeostasis influences the circadian clock in Arabidopsis.
    Plant Signal Behav. 2010 Oct;5(10):1237-40 PMID: 20861682
  56. 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
  57. RNA around the clock - regulation at the RNA level in biological timing.
    Front Plant Sci. 2015 May 05;6:311 PMID: 25999975
  58. Timing of plant immune responses by a central circadian regulator.
    Nature. 2011 Feb 3;470(7332):110-4 PMID: 21293378
  59. Plants under continuous light.
    Trends Plant Sci. 2011 Jun;16(6):310-8 PMID: 21396878
  60. Complexity in the wiring and regulation of plant circadian networks.
    Curr Biol. 2012 Aug 21;22(16):R648-57 PMID: 22917516
  61. 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
  62. An expanding universe of circadian networks in higher plants.
    Trends Plant Sci. 2010 May;15(5):259-65 PMID: 20382065
  63. Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves.
    J Exp Bot. 2005 Nov;56(421):2877-83 PMID: 16157652
  64. Arabidopsis thaliana: a model plant for genome analysis.
    Science. 1998 Oct 23;282(5389):662, 679-82 PMID: 9784120
  65. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis.
    Nat Commun. 2013;4:1352 PMID: 23322040
  66. Regulation of iron homeostasis in Arabidopsis thaliana by the clock regulator time for coffee.
    J Biol Chem. 2009 Dec 25;284(52):36271-81 PMID: 19828447
  67. The circadian clock regulates auxin signaling and responses in Arabidopsis.
    PLoS Biol. 2007 Aug;5(8):e222 PMID: 17683202
  68. Temporal aspects of copper homeostasis and its crosstalk with hormones.
    Front Plant Sci. 2015 Apr 17;6:255 PMID: 25941529
  69. Diurnal regulation of the brassinosteroid-biosynthetic CPD gene in Arabidopsis.
    Plant Physiol. 2006 May;141(1):299-309 PMID: 16531479
  70. ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis.
    Plant J. 2004 May;38(3):381-95 PMID: 15086800
  71. Comparison of plant hormone signalling systems.
    Essays Biochem. 2015;58:165-81 PMID: 26374894
  72. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops.
    Mol Syst Biol. 2012 Mar 06;8:574 PMID: 22395476
  73. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.
    Genome Biol. 2008;9(8):R130 PMID: 18710561
  74. TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis.
    Plant Cell. 2012 Jun;24(6):2470-82 PMID: 22693280
  75. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9458-63 PMID: 20439704
  76. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock.
    Science. 2001 Aug 3;293(5531):880-3 PMID: 11486091
  77. 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
  78. Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function.
    EMBO J. 2013 Feb 20;32(4):511-23 PMID: 23241948
  79. Circadian organization of behavior and physiology in Drosophila.
    Annu Rev Physiol. 2010;72:605-24 PMID: 20148690
  80. Transcriptional regulation of LUX by CBF1 mediates cold input to the circadian clock in Arabidopsis.
    Curr Biol. 2014 Jul 7;24(13):1518-24 PMID: 24954045
  81. The circadian system in higher plants.
    Annu Rev Plant Biol. 2009;60:357-77 PMID: 19575587
  82. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene.
    Science. 1999 Sep 3;285(5433):1579-82 PMID: 10477524
  83. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7.
    Plant J. 2013 Oct;76(1):101-14 PMID: 23808423
  84. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator.
    Plant Cell. 2014 Jul;26(7):2843-57 PMID: 25012192
  85. A systems view of responses to nutritional cues in Arabidopsis: toward a paradigm shift for predictive network modeling.
    Plant Physiol. 2010 Feb;152(2):445-52 PMID: 19939945
  86. Circadian oscillation of gibberellin signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2011 May 31;108(22):9292-7 PMID: 21576475
  87. 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
  88. Central and peripheral circadian clocks in mammals.
    Annu Rev Neurosci. 2012;35:445-62 PMID: 22483041
  89. STRESSing the role of the plant circadian clock.
    Trends Plant Sci. 2015 Apr;20(4):230-7 PMID: 25631123
  90. Plant nitrogen assimilation and use efficiency.
    Annu Rev Plant Biol. 2012;63:153-82 PMID: 22224450
  91. A hierarchical multi-oscillator network orchestrates the Arabidopsis circadian system.
    Cell. 2015 Sep 24;163(1):148-59 PMID: 26406375
  92. Growth-defense tradeoffs in plants: a balancing act to optimize fitness.
    Mol Plant. 2014 Aug;7(8):1267-1287 PMID: 24777989
  93. Tissue-specific clocks in Arabidopsis show asymmetric coupling.
    Nature. 2014 Nov 20;515(7527):419-22 PMID: 25363766
  94. Revised Morning Loops of the Arabidopsis Circadian Clock Based on Analyses of Direct Regulatory Interactions.
    PLoS One. 2015 Dec 01;10(12):e0143943 PMID: 26625126
  95. Domestication selected for deceleration of the circadian clock in cultivated tomato.
    Nat Genet. 2016 Jan;48(1):89-93 PMID: 26569124
  96. Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response.
    Plant Cell Physiol. 2009 Mar;50(3):447-62 PMID: 19131357
  97. Circadian regulation of chloroplastic f and m thioredoxins through control of the CCA1 transcription factor.
    J Exp Bot. 2011 Mar;62(6):2039-51 PMID: 21196476
  98. Transcriptional repressor PRR5 directly regulates clock-output pathways.
    Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):17123-8 PMID: 23027938
  99. The language of calcium signaling.
    Annu Rev Plant Biol. 2010;61:593-620 PMID: 20192754
  100. Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis.
    Plant Physiol. 2013 Feb;161(2):893-903 PMID: 23250624
  101. The link between flowering time and stress tolerance.
    J Exp Bot. 2016 Jan;67(1):47-60 PMID: 26428061
  102. Rhythmic growth explained by coincidence between internal and external cues.
    Nature. 2007 Jul 19;448(7151):358-61 PMID: 17589502
  103. Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants.
    Pest Manag Sci. 2009 May;65(5):497-503 PMID: 19206090
  104. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid.
    Cell. 2006 Sep 22;126(6):1109-20 PMID: 16990135
  105. Circadian clock-dependent gating in ABA signalling networks.
    Protoplasma. 2012 Jul;249(3):445-57 PMID: 21773710
  106. The phosphate transporter PHT4;1 is a salicylic acid regulator likely controlled by the circadian clock protein CCA1.
    Front Plant Sci. 2014 Dec 16;5:701 PMID: 25566276
  107. Redox rhythm reinforces the circadian clock to gate immune response.
    Nature. 2015 Jul 23;523(7561):472-6 PMID: 26098366
  108. Circadian Clock Genes Universally Control Key Agricultural Traits.
    Mol Plant. 2015 Aug;8(8):1135-52 PMID: 25772379
  109. Interactions between plant circadian clocks and solute transport.
    J Exp Bot. 2011 Apr;62(7):2333-48 PMID: 21378117
  110. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.
    Science. 2005 Jul 22;309(5734):630-3 PMID: 16040710
  111. Beyond Arabidopsis: the circadian clock in non-model plant species.
    Semin Cell Dev Biol. 2013 May;24(5):430-6 PMID: 23466287
  112. Just in time: circadian defense patterns and the optimal defense hypothesis.
    Plant Signal Behav. 2013 Jun;8(6):e24410 PMID: 23603968
  113. CCA1 and ELF3 Interact in the control of hypocotyl length and flowering time in Arabidopsis.
    Plant Physiol. 2012 Feb;158(2):1079-88 PMID: 22190341
  114. Coordination of carbon supply and plant growth.
    Plant Cell Environ. 2007 Sep;30(9):1126-49 PMID: 17661751
  115. Posttranslational regulation of CIRCADIAN CLOCK ASSOCIATED1 in the circadian oscillator of Arabidopsis.
    Plant Physiol. 2009 Jun;150(2):844-57 PMID: 19339503
  116. Differential Involvement of the Circadian Clock in the Expression of Genes Required for Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Synthesis, Assembly, and Activation in Arabidopsis thaliana.
    Plant Physiol. 1993 Oct;103(2):553-564 PMID: 12231961
  117. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4939-44 PMID: 18344319
  118. Circadian regulation of abiotic stress tolerance in plants.
    Front Plant Sci. 2015 Aug 27;6:648 PMID: 26379680
  119. Integrating circadian dynamics with physiological processes in plants.
    Nat Rev Genet. 2015 Oct;16(10):598-610 PMID: 26370901
  120. 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
  121. Accurate timekeeping is controlled by a cycling activator in Arabidopsis.
    Elife. 2013 Apr 30;2:e00473 PMID: 23638299
  122. 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
  123. Local and systemic signaling of iron status and its interactions with homeostasis of other essential elements.
    Front Plant Sci. 2015 Sep 14;6:716 PMID: 26442030
  124. Circadian rhythms of ethylene emission in Arabidopsis.
    Plant Physiol. 2004 Nov;136(3):3751-61 PMID: 15516515
Article Info
Journal
Cold Spring Harbor perspectives in biology
Abbr.
Cold Spring Harb Perspect Biol
ISSN
1943-0264
Published
2016-12-01
Epub
2016-00-01
Language
English
Region
United States
NLM ID
101513680
PMCID
PMC5131769
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com