Skip to main content
PMC home page
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):1761–1767. doi: 10.1098/rstb.2001.0963

Flowering in time: genes controlling photoperiodic flowering in Arabidopsis.

J Putterill 1
PMCID: PMC1088552  PMID: 11710983

Abstract

Successful sexual reproduction in plants relies upon the strict coordination of flowering time with favourable seasons of the year. One of the most important seasonal cues for the model plant Arabidopsis thaliana (Arabidopsis) is day length. Genes influencing flowering time in Arabidopsis have been isolated, some of which are involved in the perception and signalling of day length. This review discusses recent progress that has been made in understanding how Arabidopsis integrates environmental and internal signals to ensure a sharp transition to flowering and new insights on the role of the circadian clock in controlling the expression of genes that promote flowering in response to day length.

Full Text

The Full Text of this article is available as a PDF (141.0 KB).

Selected References

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

  1. Alabadí D., Oyama T., Yanovsky M. J., Harmon F. G., Más P., Kay S. A. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science. 2001 Aug 3;293(5531):880–883. doi: 10.1126/science.1061320. [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. Chou M. L., Yang C. H. Late-flowering genes interact with early-flowering genes to regulate flowering time in Arabidopsis thaliana. Plant Cell Physiol. 1999 Jul;40(7):702–708. doi: 10.1093/oxfordjournals.pcp.a029596. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Dowson-Day M. J., Millar A. J. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 1999 Jan;17(1):63–71. doi: 10.1046/j.1365-313x.1999.00353.x. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. Hisada A., Hanzawa H., Weller J. L., Nagatani A., Reid J. B., Furuya M. Light-induced nuclear translocation of endogenous pea phytochrome A visualized by immunocytochemical procedures. Plant Cell. 2000 Jul;12(7):1063–1078. doi: 10.1105/tpc.12.7.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Huq E., Tepperman J. M., Quail P. H. GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9789–9794. doi: 10.1073/pnas.170283997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Johnson E., Bradley M., Harberd N. P., Whitelam G. C. Photoresponses of Light-Grown phyA Mutants of Arabidopsis (Phytochrome A Is Required for the Perception of Daylength Extensions). Plant Physiol. 1994 May;105(1):141–149. doi: 10.1104/pp.105.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kardailsky I., Shukla V. K., Ahn J. H., Dagenais N., Christensen S. K., Nguyen J. T., Chory J., Harrison M. J., Weigel D. Activation tagging of the floral inducer FT. Science. 1999 Dec 3;286(5446):1962–1965. doi: 10.1126/science.286.5446.1962. [DOI] [PubMed] [Google Scholar]
  15. Kim L., Kircher S., Toth R., Adam E., Schäfer E., Nagy F. Light-induced nuclear import of phytochrome-A:GFP fusion proteins is differentially regulated in transgenic tobacco and Arabidopsis. Plant J. 2000 Apr;22(2):125–133. doi: 10.1046/j.1365-313x.2000.00729.x. [DOI] [PubMed] [Google Scholar]
  16. Kobayashi Y., Kaya H., Goto K., Iwabuchi M., Araki T. A pair of related genes with antagonistic roles in mediating flowering signals. Science. 1999 Dec 3;286(5446):1960–1962. doi: 10.1126/science.286.5446.1960. [DOI] [PubMed] [Google Scholar]
  17. Koornneef M., Hanhart C. J., van der Veen J. H. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet. 1991 Sep;229(1):57–66. doi: 10.1007/BF00264213. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lee H., Suh S. S., Park E., Cho E., Ahn J. H., Kim S. G., Lee J. S., Kwon Y. M., Lee I. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 2000 Sep 15;14(18):2366–2376. doi: 10.1101/gad.813600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lin C. Photoreceptors and regulation of flowering time. Plant Physiol. 2000 May;123(1):39–50. doi: 10.1104/pp.123.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Menzel G., Apel K., Melzer S. Identification of two MADS box genes that are expressed in the apical meristem of the long-day plant Sinapis alba in transition to flowering. Plant J. 1996 Mar;9(3):399–408. doi: 10.1046/j.1365-313x.1996.09030399.x. [DOI] [PubMed] [Google Scholar]
  24. Millar A. J., Carré I. A., Strayer C. A., Chua N. H., Kay S. A. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science. 1995 Feb 24;267(5201):1161–1163. doi: 10.1126/science.7855595. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Neff M. M., Fankhauser C., Chory J. Light: an indicator of time and place. Genes Dev. 2000 Feb 1;14(3):257–271. [PubMed] [Google Scholar]
  27. 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]
  28. Ni M., Tepperman J. M., Quail P. H. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature. 1999 Aug 19;400(6746):781–784. doi: 10.1038/23500. [DOI] [PubMed] [Google Scholar]
  29. Nilsson O., Lee I., Blázquez M. A., Weigel D. Flowering-time genes modulate the response to LEAFY activity. Genetics. 1998 Sep;150(1):403–410. doi: 10.1093/genetics/150.1.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Onouchi H., Igeño M. I., Périlleux C., Graves K., Coupland G. Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell. 2000 Jun;12(6):885–900. doi: 10.1105/tpc.12.6.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Osterlund M. T., Hardtke C. S., Wei N., Deng X. W. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature. 2000 May 25;405(6785):462–466. doi: 10.1038/35013076. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Putterill J., Robson F., Lee K., Simon R., Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 1995 Mar 24;80(6):847–857. doi: 10.1016/0092-8674(95)90288-0. [DOI] [PubMed] [Google Scholar]
  34. Reed J. W., Nagatani A., Elich T. D., Fagan M., Chory J. Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994 Apr;104(4):1139–1149. doi: 10.1104/pp.104.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ruiz-García L., Madueño F., Wilkinson M., Haughn G., Salinas J., Martínez-Zapater J. M. Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell. 1997 Nov;9(11):1921–1934. doi: 10.1105/tpc.9.11.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Samach A., Coupland G. Time measurement and the control of flowering in plants. Bioessays. 2000 Jan;22(1):38–47. doi: 10.1002/(SICI)1521-1878(200001)22:1<38::AID-BIES8>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  37. Samach A., Onouchi H., Gold S. E., Ditta G. S., Schwarz-Sommer Z., Yanofsky M. F., Coupland G. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science. 2000 Jun 2;288(5471):1613–1616. doi: 10.1126/science.288.5471.1613. [DOI] [PubMed] [Google Scholar]
  38. Schaffer R., Landgraf J., Accerbi M., Simon V., Larson M., Wisman E. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell. 2001 Jan;13(1):113–123. doi: 10.1105/tpc.13.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Sheldon C. C., Finnegan E. J., Rouse D. T., Tadege M., Bagnall D. J., Helliwell C. A., Peacock W. J., Dennis E. S. The control of flowering by vernalization. Curr Opin Plant Biol. 2000 Oct;3(5):418–422. doi: 10.1016/s1369-5266(00)00106-0. [DOI] [PubMed] [Google Scholar]
  41. Simon R., Igeño M. I., Coupland G. Activation of floral meristem identity genes in Arabidopsis. Nature. 1996 Nov 7;384(6604):59–62. doi: 10.1038/384059a0. [DOI] [PubMed] [Google Scholar]
  42. Simpson G. G., Gendall A. R., Dean C. When to switch to flowering. Annu Rev Cell Dev Biol. 1999;15:519–550. doi: 10.1146/annurev.cellbio.15.1.519. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. 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]
  45. 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]
  46. Somers D. E. The physiology and molecular bases of the plant circadian clock. Plant Physiol. 1999 Sep;121(1):9–20. doi: 10.1104/pp.121.1.9. [DOI] [PMC free article] [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. 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]
  49. Suárez-López P., Wheatley K., Robson F., Onouchi H., Valverde F., Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature. 2001 Apr 26;410(6832):1116–1120. doi: 10.1038/35074138. [DOI] [PubMed] [Google Scholar]
  50. Swarup K., Alonso-Blanco C., Lynn J. R., Michaels S. D., Amasino R. M., Koornneef M., Millar A. J. Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant J. 1999 Oct;20(1):67–77. doi: 10.1046/j.1365-313x.1999.00577.x. [DOI] [PubMed] [Google Scholar]
  51. Wang Z. Y., Kenigsbuch D., Sun L., Harel E., Ong M. S., Tobin E. M. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell. 1997 Apr;9(4):491–507. doi: 10.1105/tpc.9.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. 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]
  53. Weigel D., Alvarez J., Smyth D. R., Yanofsky M. F., Meyerowitz E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell. 1992 May 29;69(5):843–859. doi: 10.1016/0092-8674(92)90295-n. [DOI] [PubMed] [Google Scholar]
  54. Yano M., Katayose Y., Ashikari M., Yamanouchi U., Monna L., Fuse T., Baba T., Yamamoto K., Umehara Y., Nagamura Y. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell. 2000 Dec;12(12):2473–2484. doi: 10.1105/tpc.12.12.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yanovsky M. J., Izaguirre M., Wagmaister J. A., Gatz C., Jackson S. D., Thomas B., Casal J. J. Phytochrome A resets the circadian clock and delays tuber formation under long days in potato. Plant J. 2000 Jul;23(2):223–232. doi: 10.1046/j.1365-313x.2000.00775.x. [DOI] [PubMed] [Google Scholar]
  56. 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]

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

RESOURCES