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Decentralized circadian clocks process thermal and photoperiodic cues in specific tissues

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 demonstrated35. 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.

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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.

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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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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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The authors declare no competing financial interests.

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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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