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Transcription factor PIF4 controls the thermosensory activation of flowering

Abstract

Plant growth and development are strongly affected by small differences in temperature1. Current climate change has already altered global plant phenology and distribution2,3, and projected increases in temperature pose a significant challenge to agriculture4. Despite the important role of temperature on plant development, the underlying pathways are unknown. It has previously been shown that thermal acceleration of flowering is dependent on the florigen, FLOWERING LOCUS T (FT)5,6. How this occurs is, however, not understood, because the major pathway known to upregulate FT, the photoperiod pathway, is not required for thermal acceleration of flowering6. Here we demonstrate a direct mechanism by which increasing temperature causes the bHLH transcription factor PHYTOCHROME INTERACTING FACTOR4 (PIF4) to activate FT. Our findings provide a new understanding of how plants control their timing of reproduction in response to temperature. Flowering time is an important trait in crops as well as affecting the life cycles of pollinator species. A molecular understanding of how temperature affects flowering will be important for mitigating the effects of climate change.

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Figure 1: PIF4 is necessary for the thermal induction of flowering in short photoperiods.
Figure 2: Regulation of PIF4 by temperature.
Figure 3: PIF4 directly binds the FT promoter in a temperature-dependent manner.
Figure 4: PIF4 integrates environmental signals.

References

  1. Samach, A. & Wigge, P. A. Ambient temperature perception in plants. Curr. Opin. Plant Biol. 8, 483–486 (2005)

    Article  Google Scholar 

  2. Fitter, A. H. & Fitter, R. S. Rapid changes in flowering time in British plants. Science 296, 1689–1691 (2002)

    Article  ADS  CAS  Google Scholar 

  3. Willis, C. G., Ruhfel, B., Primack, R. B., Miller-Rushing, A. J. & Davis, C. C. Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17029–17033 (2008)

    Article  ADS  CAS  Google Scholar 

  4. Battisti, D. S. & Naylor, R. L. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240–244 (2009)

    Article  CAS  Google Scholar 

  5. Halliday, K. J., Salter, M. G., Thingnaes, E. & Whitelam, G. C. Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J. 33, 875–885 (2003)

    Article  CAS  Google Scholar 

  6. Balasubramanian, S., Sureshkumar, S., Lempe, J. & Weigel, D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, e106 (2006)

    Article  Google Scholar 

  7. Blazquez, M. A., Ahn, J. H. & Weigel, D. A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nature Genet. 33, 168–171 (2003)

    Article  CAS  Google Scholar 

  8. Koini, M. A. et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413 (2009)

    Article  CAS  Google Scholar 

  9. Stavang, J. A. et al. Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60, 589–601 (2009)

    Article  CAS  Google Scholar 

  10. Nozue, K. et al. Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361 (2007)

    Article  ADS  CAS  Google Scholar 

  11. Valverde, F. et al. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003–1006 (2004)

    Article  ADS  CAS  Google Scholar 

  12. Lorrain, S., Allen, T., Duek, P. D., Whitelam, G. C. & Fankhauser, C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312–323 (2008)

    Article  CAS  Google Scholar 

  13. Wenkel, S. et al. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18, 2971–2984 (2006)

    Article  CAS  Google Scholar 

  14. Foreman, J. et al. Light receptor action is critical for maintaining plant biomass at warm ambient temperatures. Plant J. 65, 441–452 (2011)

    Article  CAS  Google Scholar 

  15. Takada, S. & Goto, K. Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell 15, 2856–2865 (2003)

    Article  CAS  Google Scholar 

  16. Adrian, J. et al. cis-regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Plant Cell 22, 1425–1440 (2010)

    Article  CAS  Google Scholar 

  17. Liu, H. et al. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535–1539 (2008)

    Article  ADS  CAS  Google Scholar 

  18. Franklin, K. A. et al. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. USA 108, 20231–20235 (2011)

    Article  ADS  CAS  Google Scholar 

  19. Angel, A., Song, J., Dean, C. & Howard, M. A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476, 105–108 (2011)

    Article  CAS  Google Scholar 

  20. Kumar, S. V. & Wigge, P. A. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–140 (2010)

    Article  CAS  Google Scholar 

  21. de Lucas, M. et al. A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–484 (2008)

    Article  ADS  CAS  Google Scholar 

  22. Feng, S. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479 (2008)

    Article  ADS  CAS  Google Scholar 

  23. Mutasa-Gottgens, E. & Hedden, P. Gibberellin as a factor in floral regulatory networks. J. Exp. Bot. 60, 1979–1989 (2009)

    Article  Google Scholar 

  24. Hisamatsu, T. & King, R. W. The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. J. Exp. Bot. 59, 3821–3829 (2008)

    Article  CAS  Google Scholar 

  25. Brian, P. W. Role of gibberellin-like hormones in regulation of plant growth & flowering. Nature 181, 1122–1123 (1958)

    Article  ADS  Google Scholar 

  26. Brock, M. T., Maloof, J. N. & Weinig, C. Genes underlying quantitative variation in ecologically important traits: PIF4 (phytochrome interacting factor 4) is associated with variation in internode length, flowering time, and fruit set in Arabidopsis thaliana. Mol. Ecol. 19, 1187–1199 (2010)

    Article  Google Scholar 

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Acknowledgements

We thank S. Prat, C. Fankhauser, K. Franklin, K. Goto, G. Coupland and D. Weigel for seeds. We are grateful to members of the Wigge laboratory for discussions. This work was supported in part by award No. KUK-I1-002-03 (to N.P.H.) made by King Abdullah University of Science and Technology and a Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/I019022/1 (to S.V.K.). D.L. was supported by an Erwin Schroedinger Fellowship from the Austrian Science Fund FWF. P.A.W. was supported by start-up funds from the John Innes Centre and BBSRC, a BBSRC grant (BB/D0100470/1) and a European Research Council Starting Grant (ERC 243140).

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S.V.K., D.L., K.E.J. and E.A. performed the experiments. N.P.H. and P.A.W. designed the study and supervised the work. All authors discussed the results and made substantial contributions to the manuscript.

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Correspondence to Philip A. Wigge.

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The authors declare no competing financial interests.

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Kumar, S., Lucyshyn, D., Jaeger, K. et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012). https://doi.org/10.1038/nature10928

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