Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2001 Nov 29;356(1415):1735–1743. doi: 10.1098/rstb.2001.0936

Picking out parallels: plant circadian clocks in context.

H G McWatters 1, L C Roden 1, D Staiger 1
PMCID: PMC1088549  PMID: 11710980

Abstract

Molecular models have been described for the circadian clocks of representatives of several different taxa. Much of the work on the plant circadian system has been carried out using the thale cress, Arabidopsis thaliana, as a model. We discuss the roles of genes implicated in the plant circadian system, with special emphasis on Arabidopsis. Plants have an endogenous clock that regulates many aspects of circadian and photoperiodic behaviour. Despite the discovery of components that resemble those involved in the clocks of animals or fungi, no coherent model of the plant clock has yet been proposed. In this review, we aim to provide an overview of studies of the Arabidopsis circadian system. We shall compare these with results from different taxa and discuss them in the context of what is known about clocks in other organisms.

Full Text

The Full Text of this article is available as a PDF (219.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balsalobre A., Damiola F., Schibler U. A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 1998 Jun 12;93(6):929–937. doi: 10.1016/s0092-8674(00)81199-x. [DOI] [PubMed] [Google Scholar]
  2. Blázquez M. A., Weigel D. Integration of floral inductive signals in Arabidopsis. Nature. 2000 Apr 20;404(6780):889–892. doi: 10.1038/35009125. [DOI] [PubMed] [Google Scholar]
  3. Carpenter C. D., Kreps J. A., Simon A. E. Genes encoding glycine-rich Arabidopsis thaliana proteins with RNA-binding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol. 1994 Mar;104(3):1015–1025. doi: 10.1104/pp.104.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cashmore A. R., Jarillo J. A., Wu Y. J., Liu D. Cryptochromes: blue light receptors for plants and animals. Science. 1999 Apr 30;284(5415):760–765. doi: 10.1126/science.284.5415.760. [DOI] [PubMed] [Google Scholar]
  5. Ceriani M. F., Darlington T. K., Staknis D., Más P., Petti A. A., Weitz C. J., Kay S. A. Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science. 1999 Jul 23;285(5427):553–556. doi: 10.1126/science.285.5427.553. [DOI] [PubMed] [Google Scholar]
  6. Crosthwaite S. K., Dunlap J. C., Loros J. J. Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science. 1997 May 2;276(5313):763–769. doi: 10.1126/science.276.5313.763. [DOI] [PubMed] [Google Scholar]
  7. Deng X. W., Quail P. H. Signalling in light-controlled development. Semin Cell Dev Biol. 1999 Apr;10(2):121–129. doi: 10.1006/scdb.1999.0287. [DOI] [PubMed] [Google Scholar]
  8. Dunlap J. C. Molecular bases for circadian clocks. Cell. 1999 Jan 22;96(2):271–290. doi: 10.1016/s0092-8674(00)80566-8. [DOI] [PubMed] [Google Scholar]
  9. Edery I., Zwiebel L. J., Dembinska M. E., Rosbash M. Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2260–2264. doi: 10.1073/pnas.91.6.2260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fowler S., Lee K., Onouchi H., Samach A., Richardson K., Morris B., Coupland G., Putterill J. 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):4679–4688. doi: 10.1093/emboj/18.17.4679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Giebultowicz J. M., Stanewsky R., Hall J. C., Hege D. M. Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol. 2000 Jan 27;10(2):107–110. doi: 10.1016/s0960-9822(00)00299-2. [DOI] [PubMed] [Google Scholar]
  12. Green R. M., Tobin E. M. Loss of the circadian clock-associated protein 1 in Arabidopsis results in altered clock-regulated gene expression. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4176–4179. doi: 10.1073/pnas.96.7.4176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harmer S. L., Hogenesch J. B., Straume M., Chang H. S., Han B., Zhu T., Wang X., Kreps J. A., Kay S. A. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000 Dec 15;290(5499):2110–2113. doi: 10.1126/science.290.5499.2110. [DOI] [PubMed] [Google Scholar]
  14. Heintzen C., Melzer S., Fischer R., Kappeler S., Apel K., Staiger D. A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J. 1994 Jun;5(6):799–813. doi: 10.1046/j.1365-313x.1994.5060799.x. [DOI] [PubMed] [Google Scholar]
  15. Heintzen C., Nater M., Apel K., Staiger D. AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8515–8520. doi: 10.1073/pnas.94.16.8515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Helfrich-Förster C. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: a brain-behavioral study of disconnected mutants. J Comp Physiol A. 1998 Apr;182(4):435–453. doi: 10.1007/s003590050192. [DOI] [PubMed] [Google Scholar]
  17. Helfrich-Förster C., Stengl M., Homberg U. Organization of the circadian system in insects. Chronobiol Int. 1998 Nov;15(6):567–594. doi: 10.3109/07420529808993195. [DOI] [PubMed] [Google Scholar]
  18. Hicks K. A., Millar A. J., Carré I. A., Somers D. E., Straume M., Meeks-Wagner D. R., Kay S. A. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science. 1996 Nov 1;274(5288):790–792. doi: 10.1126/science.274.5288.790. [DOI] [PubMed] [Google Scholar]
  19. Huala E., Oeller P. W., Liscum E., Han I. S., Larsen E., Briggs W. R. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science. 1997 Dec 19;278(5346):2120–2123. doi: 10.1126/science.278.5346.2120. [DOI] [PubMed] [Google Scholar]
  20. Kloss B., Price J. L., Saez L., Blau J., Rothenfluh A., Wesley C. S., Young M. W. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell. 1998 Jul 10;94(1):97–107. doi: 10.1016/s0092-8674(00)81225-8. [DOI] [PubMed] [Google Scholar]
  21. Koornneef Maarten, Alonso-Blanco Carlos, Peeters Anton J. M., Soppe Wim. GENETIC CONTROL OF FLOWERING TIME IN ARABIDOPSIS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):345–370. doi: 10.1146/annurev.arplant.49.1.345. [DOI] [PubMed] [Google Scholar]
  22. Liu C., Weaver D. R., Strogatz S. H., Reppert S. M. Cellular construction of a circadian clock: period determination in the suprachiasmatic nuclei. Cell. 1997 Dec 12;91(6):855–860. doi: 10.1016/s0092-8674(00)80473-0. [DOI] [PubMed] [Google Scholar]
  23. Liu Y., Loros J., Dunlap J. C. Phosphorylation of the Neurospora clock protein FREQUENCY determines its degradation rate and strongly influences the period length of the circadian clock. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):234–239. doi: 10.1073/pnas.97.1.234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lowrey P. L., Shimomura K., Antoch M. P., Yamazaki S., Zemenides P. D., Ralph M. R., Menaker M., Takahashi J. S. Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science. 2000 Apr 21;288(5465):483–492. doi: 10.1126/science.288.5465.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Martínez-García J. F., Huq E., Quail P. H. Direct targeting of light signals to a promoter element-bound transcription factor. Science. 2000 May 5;288(5467):859–863. doi: 10.1126/science.288.5467.859. [DOI] [PubMed] [Google Scholar]
  26. McWatters H. G., Bastow R. M., Hall A., Millar A. J. The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature. 2000 Dec 7;408(6813):716–720. doi: 10.1038/35047079. [DOI] [PubMed] [Google Scholar]
  27. McWatters H., Dunlap J. C., Millar A. J. Circadian biology: clocks for the real world. Curr Biol. 1999 Sep 9;9(17):R633–R635. doi: 10.1016/s0960-9822(99)80410-2. [DOI] [PubMed] [Google Scholar]
  28. Merrow M., Brunner M., Roenneberg T. Assignment of circadian function for the Neurospora clock gene frequency. Nature. 1999 Jun 10;399(6736):584–586. doi: 10.1038/21190. [DOI] [PubMed] [Google Scholar]
  29. Millar A. J., Short S. R., Chua N. H., Kay S. A. A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell. 1992 Sep;4(9):1075–1087. doi: 10.1105/tpc.4.9.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Millar A. J., Straume M., Chory J., Chua N. H., Kay S. A. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science. 1995 Feb 24;267(5201):1163–1166. doi: 10.1126/science.7855596. [DOI] [PubMed] [Google Scholar]
  31. Nagy F., Schäfer E. Nuclear and cytosolic events of light-induced, phytochrome-regulated signaling in higher plants. EMBO J. 2000 Jan 17;19(2):157–163. doi: 10.1093/emboj/19.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Naidoo N., Song W., Hunter-Ensor M., Sehgal A. A role for the proteasome in the light response of the timeless clock protein. Science. 1999 Sep 10;285(5434):1737–1741. doi: 10.1126/science.285.5434.1737. [DOI] [PubMed] [Google Scholar]
  33. Nelson D. C., Lasswell J., Rogg L. E., Cohen M. A., Bartel B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell. 2000 Apr 28;101(3):331–340. doi: 10.1016/s0092-8674(00)80842-9. [DOI] [PubMed] [Google Scholar]
  34. Nishiwaki T., Iwasaki H., Ishiura M., Kondo T. Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):495–499. doi: 10.1073/pnas.97.1.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Park D. H., Somers D. E., Kim Y. S., Choy Y. H., Lim H. K., Soh M. S., Kim H. J., Kay S. A., Nam H. G. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science. 1999 Sep 3;285(5433):1579–1582. doi: 10.1126/science.285.5433.1579. [DOI] [PubMed] [Google Scholar]
  36. Putterill J. Flowering in time: genes controlling photoperiodic flowering in Arabidopsis. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1761–1767. doi: 10.1098/rstb.2001.0963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ralph M. R., Foster R. G., Davis F. C., Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990 Feb 23;247(4945):975–978. doi: 10.1126/science.2305266. [DOI] [PubMed] [Google Scholar]
  38. Ralph M. R., Menaker M. A mutation of the circadian system in golden hamsters. Science. 1988 Sep 2;241(4870):1225–1227. doi: 10.1126/science.3413487. [DOI] [PubMed] [Google Scholar]
  39. Roenneberg T., Merrow M. Circadian systems and metabolism. J Biol Rhythms. 1999 Dec;14(6):449–459. doi: 10.1177/074873099129001019. [DOI] [PubMed] [Google Scholar]
  40. Roenneberg T., Merrow M. Circadian systems: different levels of complexity. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1687–1696. doi: 10.1098/rstb.2001.0969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Roenneberg T., Merrow M. Molecular circadian oscillators: an alternative hypothesis. J Biol Rhythms. 1998 Apr;13(2):167–179. doi: 10.1177/074873098129000011. [DOI] [PubMed] [Google Scholar]
  42. Sakamoto K., Nagatani A. Nuclear localization activity of phytochrome B. Plant J. 1996 Nov;10(5):859–868. doi: 10.1046/j.1365-313x.1996.10050859.x. [DOI] [PubMed] [Google Scholar]
  43. Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carré I. A., Coupland G. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998 Jun 26;93(7):1219–1229. doi: 10.1016/s0092-8674(00)81465-8. [DOI] [PubMed] [Google Scholar]
  44. Somers D. E. Clock-associated genes in Arabidopsis: a family affair. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1745–1753. doi: 10.1098/rstb.2001.0965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Somers D. E., Devlin P. F., Kay S. A. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 1998 Nov 20;282(5393):1488–1490. doi: 10.1126/science.282.5393.1488. [DOI] [PubMed] [Google Scholar]
  46. Somers D. E., Schultz T. F., Milnamow M., Kay S. A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell. 2000 Apr 28;101(3):319–329. doi: 10.1016/s0092-8674(00)80841-7. [DOI] [PubMed] [Google Scholar]
  47. Somers D. E., Webb A. A., Pearson M., Kay S. A. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development. 1998 Feb;125(3):485–494. doi: 10.1242/dev.125.3.485. [DOI] [PubMed] [Google Scholar]
  48. Staiger D., Apel K. Circadian clock-regulated expression of an RNA-binding protein in Arabidopsis: characterisation of a minimal promoter element. Mol Gen Genet. 1999 Jun;261(4-5):811–819. doi: 10.1007/s004380050025. [DOI] [PubMed] [Google Scholar]
  49. Staiger D., Heintzen C. The circadian system of Arabidopsis thaliana: forward and reverse genetic approaches. Chronobiol Int. 1999 Jan;16(1):1–16. doi: 10.3109/07420529908998708. [DOI] [PubMed] [Google Scholar]
  50. Staiger D. RNA-binding proteins and circadian rhythms in Arabidopsis thaliana. Philos Trans R Soc Lond B Biol Sci. 2001 Nov 29;356(1415):1755–1759. doi: 10.1098/rstb.2001.0964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Strayer C., Oyama T., Schultz T. F., Raman R., Somers D. E., Más P., Panda S., Kreps J. A., Kay S. A. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science. 2000 Aug 4;289(5480):768–771. doi: 10.1126/science.289.5480.768. [DOI] [PubMed] [Google Scholar]
  52. Sugano S., Andronis C., Green R. M., Wang Z. Y., Tobin E. M. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):11020–11025. doi: 10.1073/pnas.95.18.11020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sugano S., Andronis C., Ong M. S., Green R. M., Tobin E. M. 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):12362–12366. doi: 10.1073/pnas.96.22.12362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Taylor B. L., Zhulin I. B. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev. 1999 Jun;63(2):479–506. doi: 10.1128/mmbr.63.2.479-506.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Thain S. C., Hall A., Millar A. J. Functional independence of circadian clocks that regulate plant gene expression. Curr Biol. 2000 Aug 24;10(16):951–956. doi: 10.1016/s0960-9822(00)00630-8. [DOI] [PubMed] [Google Scholar]
  56. Wang Z. Y., Tobin E. M. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998 Jun 26;93(7):1207–1217. doi: 10.1016/s0092-8674(00)81464-6. [DOI] [PubMed] [Google Scholar]
  57. Whitmarsh A. J., Davis R. J. Regulation of transcription factor function by phosphorylation. Cell Mol Life Sci. 2000 Aug;57(8-9):1172–1183. doi: 10.1007/PL00000757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Whitmore D., Foulkes N. S., Sassone-Corsi P. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature. 2000 Mar 2;404(6773):87–91. doi: 10.1038/35003589. [DOI] [PubMed] [Google Scholar]
  59. Yanovsky M. J., Mazzella M. A., Casal J. J. A quadruple photoreceptor mutant still keeps track of time. Curr Biol. 2000 Aug 24;10(16):1013–1015. doi: 10.1016/s0960-9822(00)00651-5. [DOI] [PubMed] [Google Scholar]
  60. Zagotta M. T., Hicks K. A., Jacobs C. I., Young J. C., Hangarter R. P., Meeks-Wagner D. R. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 1996 Oct;10(4):691–702. doi: 10.1046/j.1365-313x.1996.10040691.x. [DOI] [PubMed] [Google Scholar]
  61. van Nocker S., Vierstra R. D. Two cDNAs from Arabidopsis thaliana encode putative RNA binding proteins containing glycine-rich domains. Plant Mol Biol. 1993 Feb;21(4):695–699. doi: 10.1007/BF00014552. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society of London. Series B are provided here courtesy of The Royal Society

RESOURCES