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Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues

Nature Plants volume 1, Article number: 15163 (2015) Cite this article

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Abstract

The circadian clock increases organisms' fitness by regulating physiological responses1. In mammals, the circadian clock in the suprachiasmatic nucleus (SCN) governs daily behavioural rhythms2. Similarly, in Arabidopsis, tissue-specific circadian clock functions have emerged, and the importance of the vasculature clock for photoperiodic flowering has been demonstrated3–5. However, it remains unclear if the vasculature clock regulates the majority of physiological responses, like the SCN in mammals, and if other environmental signals are also processed by the vasculature clock. Here, we studied the involvement of tissue-specific circadian clock regulation of flowering and cell elongation under different photoperiods and temperatures. We found that the circadian clock in vascular phloem companion cells is essential for photoperiodic flowering regulation; by contrast, the epidermis has a crucial impact on ambient temperature-dependent cell elongation. Thus, there are clear assignments of roles among circadian clocks in each tissue. Our results reveal that, unlike the more centralized circadian clock in mammals, the plant circadian clock is decentralized, where each tissue specifically processes individual environmental cues and regulates individual physiological responses. Our new conceptual framework will be a starting point for deciphering circadian clock functions in each tissue, which will lead to a better understanding of how circadian clock processing of environmental signals may be affected by ongoing climate change6.

In many organisms, the circadian clock plays essential roles that influence behaviour through transcriptional and hormonal regulation in response to environmental changes1,2. In mammals, for example, light and food availability signals entrain central and peripheral clocks7,8. Although food anticipatory behaviour is reported to be SCN independent7, the majority of peripheral clocks are regulated by the SCN, and those clocks form a more centralized network (Supplementary Fig. 1)9. In plants, by contrast, although the importance of thermal and photoperiodic signals for circadian clock entrainment is well understood1,10, it is largely unknown which tissue processes these environmental signals and what kind of a network structure the plant circadian clock has.

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Figure 1: Circadian clock functions in phloem companion cells are necessary for photoperiodic flowering.
Figure 2: Circadian clock functions in epidermal cells are necessary for cell elongation.
Figure 3: An epidermal clock regulates cell elongation in response to ambient temperature.
Figure 4: A schematic drawing of the decentralized circadian clock system in Arabidopsis.

References

  1. Doherty, C. J. & Kay, S. A. Circadian control of global gene expression patterns. Annu. Rev. Genet. 44, 419–444 (2010).

    Article  CAS  Google Scholar 

  2. Barclay, J. L., Tsang, A. H. & Oster, H. Interaction of central and peripheral clocks in physiological regulation. Prog. Brain Res. 199, 163–181 (2012).

    Article  CAS  Google Scholar 

  3. James, A. B. et al. The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322, 1832–1835 (2008).

    Article  CAS  Google Scholar 

  4. Yakir, E. et al. Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J. 68, 520–531 (2011).

    Article  CAS  Google Scholar 

  5. Endo, M. et al. Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 515, 419–422 (2014).

    Article  CAS  Google Scholar 

  6. Wolkovich, E. M. et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012).

    Article  CAS  Google Scholar 

  7. Tahara, Y. & Shibata, S. Chronobiology and nutrition. Neuroscience 253, 78–88 (2013).

    Article  CAS  Google Scholar 

  8. Eckel-Mahan, K. & Sassone-Corsi, P. Metabolism and the circadian clock converge. Physiol. Rev. 93, 107–135 (2013).

    Article  CAS  Google Scholar 

  9. Baran, P. On Distributed Communications: I. Introduction to Distributed Communications Networks, RM-3420-PR (1964); http://www.rand.org/content/dam/rand/pubs/research_memoranda/2006/RM3420.pdf

  10. Wigge, P. A. Ambient temperature signalling in plants. Curr. Opin. Plant Biol. 16, 661–666 (2013).

    Article  CAS  Google Scholar 

  11. 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 

  12. Makino, S., Matsushika, A., Kojima, M., Yamashino, T. & Mizuno, T. The APRR1/TOC1 quintet implicated in circadian rhythms of Arabidopsis thaliana: I. Characterization with APRR1-overexpressing plants. Plant Cell Physiol. 43, 58–69 (2002).

    Article  CAS  Google Scholar 

  13. Fukuda, H. Signals that control plant vascular cell differentiation. Nature Rev. Mol. Cell Biol. 5, 379–391 (2004).

    Article  CAS  Google Scholar 

  14. Endo, M., Mochizuki, N., Suzuki, T. & Nagatani, A. CRYPTOCHROME2 in vascular bundles regulates flowering in Arabidopsis. Plant Cell 19, 84–93 (2007).

    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. Abe, M. et al. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052–1056 (2005).

    Article  CAS  Google Scholar 

  17. Wigge, P. A. et al. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056–1059 (2005).

    Article  CAS  Google Scholar 

  18. Huang, W. et al. Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336, 75–79 (2012).

    Article  CAS  Google Scholar 

  19. Gendron, J. M. et al. Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc. Natl Acad. Sci. USA 109, 3167–3172 (2012).

    Article  CAS  Google Scholar 

  20. Imaizumi, T. Arabidopsis circadian clock and photoperiodism: time to think about location. Curr. Opin. Plant Biol. 13, 83–89 (2010).

    Article  CAS  Google Scholar 

  21. Kumar, S. V. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245 (2012).

    Article  CAS  Google Scholar 

  22. King, R. W., Hisamatsu, T., Goldschmidt, E. E. & Blundell, C. The nature of floral signals in Arabidopsis. I. Photosynthesis and a far-red photoresponse independently regulate flowering by increasing expression of FLOWERING LOCUS T (FT). J. Exp. Bot. 59, 3811–3820 (2008).

    Article  CAS  Google Scholar 

  23. Kutschera, U. & Niklas, K. J. The epidermal-growth-control theory of stem elongation: an old and a new perspective. J. Plant Physiol. 164, 1395–1409 (2007).

    Article  CAS  Google Scholar 

  24. Nusinow, D. A. et al. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475, 398–402 (2011).

    Article  CAS  Google Scholar 

  25. Hornitschek, P. et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699–711 (2012).

    Article  CAS  Google Scholar 

  26. Stokes, M. E., Chattopadhyay, A., Wilkins, O., Nambara, E. & Campbell, M. M. Interplay between sucrose and folate modulates auxin signaling in Arabidopsis. Plant Physiol. 162, 1552–1565 (2013).

    Article  CAS  Google Scholar 

  27. Turchi, L. et al. Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development 140, 2118–2129 (2013).

    Article  CAS  Google Scholar 

  28. Nomoto, Y., Kubozono, S., Yamashino, T., Nakamichi, N. & Mizuno, T. Circadian clock- and PIF4-controlled plant growth: a coincidence mechanism directly integrates a hormone signaling network into the photoperiodic control of plant architectures in Arabidopsis thaliana. Plant Cell Physiol. 53, 1950–1964 (2012).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  30. Michael, T. P., Salome, P. A. & McClung, C. R. Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc. Natl Acad. Sci. USA 100, 6878–6883 (2003).

    Article  CAS  Google Scholar 

  31. Shimada, T. L., Shimada, T. & Hara-Nishimura, I. A rapid and non-destructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J. 61, 519–528 (2010).

    Article  CAS  Google Scholar 

  32. Porra, R. J., Thompson, W. A. & Kriedeman, P. E. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394 (1989).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank M. Niwa, K. Ifuku, and Y.C. Brenda for technical assistance; Y. Kondo, S.L. Harmer and T. Imaizumi for helpful advice; J.A. Hejna for English proofreading. This work was supported by a JST PRESTO 14529738 (to M.E.), JSPS KAKENHI grants 25650097 (to M.E.), a Nakatani Foundation (to M.E.), a Mitsubishi Foundation (to M.E.), Grant-in-Aid for Scientific Research on Innovative Areas 87006029 (to M.E.), 26113510 (to M.E.) and 25113005 (to T.A.).

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Authors and Affiliations

  1. Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Sakyo, 606-8501, Kyoto, Japan

    Hanako Shimizu, Kana Katayama, Tomoko Koto, Kotaro Torii, Takashi Araki & Motomu Endo

  2. Japan Science and Technology Agency, PRESTO, 4-1-8 Honcho Kawaguchi, Saitama, 332-0012, Japan

    Motomu Endo

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  1. Hanako Shimizu
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Contributions

M.E. planned the experiments. H.S., T.K., K.T. and K.K. performed experiments. H.S. and M.E. wrote the manuscript. M.E. and T.A. supervised the project. All authors discussed the results and commented on the manuscript.

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Correspondence to Motomu Endo.

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Shimizu, H., Katayama, K., Koto, T. et al. Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues. Nature Plants 1, 15163 (2015). https://doi.org/10.1038/nplants.2015.163

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