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CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis

Abstract

Flowering is often triggered by exposing plants to appropriate day lengths. This response requires an endogenous timer called the circadian clock to measure the duration of the day or night1. This timer also controls daily rhythms in gene expression and behavioural patterns such as leaf movements. Several Arabidopsis mutations affect both circadian processes and flowering time2,3,4,5,6,7,8,9,10; but how the effect of these mutations on the circadian clock is related to their influence on flowering remains unknown. Here we show that expression of CONSTANS (CO), a gene that accelerates flowering in response to long days11, is modulated by the circadian clock and day length. Expression of a CO target gene, called FLOWERING LOCUS T (FT), is restricted to a similar time of day as expression of CO. Three mutations that affect circadian rhythms and flowering time alter CO and FT expression in ways that are consistent with their effects on flowering. In addition, the late flowering phenotype of such mutants is corrected by overexpressing CO. Thus, CO acts between the circadian clock and the control of flowering, suggesting mechanisms by which day length regulates flowering time.

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Figure 1: CO expression in wild type-plants.
Figure 2: CO expression in flowering-time mutants.
Figure 3: Analysis of FT mRNA levels.
Figure 4: Model of the long-day flowering time pathway.

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References

  1. Thomas, B. & Vince-Prue, D. Photoperiodism in Plants (Academic, London, 1997).

    Google Scholar 

  2. Fowler, S. et al. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679–4688 (1999).

    Article  CAS  Google Scholar 

  3. 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. USA 96, 4176–4179 (1999).

    Article  ADS  CAS  Google Scholar 

  4. Hicks, K. A. et al. Conditional circadian dysfunction of the Arabidopsis early-flowering-3 mutant. Science 274, 790–792 (1996).

    Article  ADS  CAS  Google Scholar 

  5. Park, D. H. et al. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579–1582 (1999).

    Article  CAS  Google Scholar 

  6. Schaffer, R. et al. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219–1229 (1998).

    Article  CAS  Google Scholar 

  7. 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 93, 1207–1217 (1998).

    Article  CAS  Google Scholar 

  8. 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 101, 331–340 (2000).

    Article  CAS  Google Scholar 

  9. Somers, D. E., Schultz, T. F., Milnamow, M. & Kay, S. A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319–329 (2000).

    Article  CAS  Google Scholar 

  10. Strayer, C. et al. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771 (2000).

    Article  ADS  CAS  Google Scholar 

  11. 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 80, 847–857 (1995).

    Article  CAS  Google Scholar 

  12. Simpson, G. G., Gendall, A. R. & Dean, C. When to switch to flowering. Annu. Rev. Cell Dev. Biol. 15, 519–550 (1999).

    Article  CAS  Google Scholar 

  13. 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. 229, 57–66 (1991).

    Article  CAS  Google Scholar 

  14. Guo, H., Yang, H., Mockler, T. C. & Lin, C. Regulation of flowering time by Arabidopsis photoreceptors. Science 279, 1360–1363 (1998).

    Article  ADS  CAS  Google Scholar 

  15. Zagotta, M. T. et al. The Arabidopsis ELF3 gene regulates vegetative photomorphogenesis and the photoperiodic induction of flowering. Plant J. 10, 691–702 (1996).

    Article  CAS  Google Scholar 

  16. 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. 104, 1015–1025 (1994).

    Article  CAS  Google Scholar 

  17. 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. USA 94, 8515–8520 (1997).

    Article  ADS  CAS  Google Scholar 

  18. 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 12, 885–900 (2000).

    Article  CAS  Google Scholar 

  19. Chou, M. -L. & Yang, C. -H. Late-flowering genes interact with early-flowering genes to regulate flowering time in Arabidopsis thaliana. Plant Cell Physiol. 40, 702–708 (1999).

    Article  CAS  Google Scholar 

  20. Kardailsky, I. et al. Activation tagging of the floral inducer FT. Science 286, 1962–1965 (1999).

    Article  CAS  Google Scholar 

  21. Samach, A. et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613–1616 (2000).

    Article  ADS  CAS  Google Scholar 

  22. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. & Araki, T. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286, 1960–1962 (1999).

    Article  CAS  Google Scholar 

  23. Somers, D. E. & Kay, S. A. in Biological Rhythms and Photoperiodism in Plants (eds Lumsden, P. J. & Millar, A. J.) 81–98 (BIOS Scientific, Oxford, 1998).

    Google Scholar 

  24. Dunlap, J. C. Molecular bases for circadian clocks. Cell 96, 271–290 (1999).

    Article  CAS  Google Scholar 

  25. Wager-Smith, K. & Kay, S. A. Circadian rhythm genetics: from flies to mice to humans. Nature Genet. 26, 23–27 (2000).

    Article  CAS  Google Scholar 

  26. Sarov-Blat, L., So, W. V., Liu, L. & Rosbash, M. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 101, 647–656 (2000).

    Article  CAS  Google Scholar 

  27. Logemann, J., Schell, J. & Willmitzer, L. Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163, 16–20 (1987).

    Article  CAS  Google Scholar 

  28. Frohman, M. A., Dush, M. K. & Martin, G. R. Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc. Natl Acad. Sci. USA 85, 8998–9002 (1988).

    Article  ADS  CAS  Google Scholar 

  29. Blázquez, M. A. & Weigel, D. Independent regulation of flowering by phytochrome B and gibberellins in Arabidopsis. Plant Physiol. 120, 1025–1032 (1999).

    Article  Google Scholar 

  30. Wang, Z. -Y. et al. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9, 491–507 (1997).

    Article  CAS  Google Scholar 

  31. Martínez-García, J. F., Monte, E. & Quail, P. H. A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J. 20, 251–257 (1999).

    Article  Google Scholar 

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Acknowledgements

We thank L. Wright for RNA samples; M. I. Igeño for the cross gi-3 × 35S::CO; R. W. M. Sablowski for the 35S::GFP plants; M. M. R. Costa and M. Piñeiro for the 35S::GFP-CO plants; M. Koornneef, C. Lin and R. Meeks-Wagner for mutant seeds; C. Andronis for the UBQ10 cDNA probe; A. Samach for scientific discussions; and C. Dean, T. Mizoguchi, P. H. Reeves, A. Samach and G. G. Simpson for comments on the manuscript. We are grateful to the laboratories of J. Putterill and E. M. Tobin for sharing unpublished results, and to C. Andronis and M. A. Blázquez for advice with the UBQ10 controls. P.S.-L. was supported by a fellowship from the Human Frontier Science Program Organization and a Marie Curie fellowship, and F.V. by a FEBS long-term fellowship.

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Correspondence to George Coupland.

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Suárez-López, P., Wheatley, K., Robson, F. et al. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116–1120 (2001). https://doi.org/10.1038/35074138

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