Letter | Published:

Tissue-specific clocks in Arabidopsis show asymmetric coupling

Nature volume 515, pages 419422 (20 November 2014) | Download Citation

Abstract

Many organisms rely on a circadian clock system to adapt to daily and seasonal environmental changes. The mammalian circadian clock consists of a central clock in the suprachiasmatic nucleus that has tightly coupled neurons and synchronizes other clocks in peripheral tissues1,2. Plants also have a circadian clock, but plant circadian clock function has long been assumed to be uncoupled3. Only a few studies have been able to show weak, local coupling among cells4,5,6,7. Here, by implementing two novel techniques, we have performed a comprehensive tissue-specific analysis of leaf tissues, and show that the vasculature and mesophyll clocks asymmetrically regulate each other in Arabidopsis. The circadian clock in the vasculature has characteristics distinct from other tissues, cycles robustly without environmental cues, and affects circadian clock regulation in other tissues. Furthermore, we found that vasculature-enriched genes that are rhythmically expressed are preferentially expressed in the evening, whereas rhythmic mesophyll-enriched genes tend to be expressed in the morning. Our results set the stage for a deeper understanding of how the vasculature circadian clock in plants regulates key physiological responses such as flowering time.

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Accessions

Primary accessions

Gene Expression Omnibus

Data deposits

All microarray data are available from the Gene Expression Omnibus database under accession code GSE50438.

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Acknowledgements

We thank H. Fukuda and Y. Sugisawa for processing raw microarray data; S. Yonehara for providing c-Jun and A-Fos plasmids; G. Breton, K. Hitomi, T. Oyama, T. Muranaka and Y. Kondo for advice; T. Koto, K. Katayama and B. Y. Chow for technical assistance; J. A. Hejna and T. R. Endo for English proofreading. This work was supported by an HFSP long-term Fellowship LT00017/2008-L (to M.E.), a JST PRESTO 11103346 (to M.E.), JSPS KAKENHI grants 22770036 and 25650097 (to M.E.), a Sumitomo Foundation and Nakatani Foundation (to M.E.), Grants-in-Aid for Scientific Research on Priority Areas 19060012 and 19060016 (to T.A.), and National Institutes of Health (NIH) Grants R01 GM056006 and GM067837 (to S.A.K.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Affiliations

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

    • Motomu Endo
    • , Hanako Shimizu
    •  & Takashi Araki
  2. Japan Science and Technology Agency, PRESTO, 4-1-8 Honcho Kawaguchi, Saitama 332-0012, Japan

    • Motomu Endo
  3. University of Southern California Molecular and Computational Biology, Department of Biology, Dana and David Dornsife College of Letters, Arts and Sciences, Los Angeles, California 90089, USA

    • Maria A. Nohales
    •  & Steve A. Kay

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Contributions

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

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Motomu Endo.

Extended data

Supplementary information

Excel files

  1. 1.

    Supplementary Table 1

    This file contains predefined models for the HAYSTACK.

  2. 2.

    Supplementary Table 2

    This file contains a list of genes that are candidates of internal control.

  3. 3.

    Supplementary Table 3

    This file contains a list of genes that are expressed dominantly in mesophyll.

  4. 4.

    Supplementary Table 4

    This file contains a list of genes that are expressed dominantly in vasculature.

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DOI

https://doi.org/10.1038/nature13919

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