Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression

  1. Peter D Gould
  2. Mirela Domijan
  3. Mark Greenwood
  4. Isao T Tokuda
  5. Hannah Rees
  6. Laszlo Kozma-Bognar
  7. Anthony JW Hall  Is a corresponding author
  8. James CW Locke  Is a corresponding author
  1. University of Liverpool, United Kingdom
  2. University of Cambridge, United Kingdom
  3. Ritsumeikan University, Japan
  4. Hungarian Academy of Sciences, Hungary

Abstract

The Arabidopsis circadian clock orchestrates gene regulation across the day/night cycle. Although a multiple feedback loop circuit has been shown to generate the 24h rhythm, it remains unclear how robust the clock is in individual cells, or how clock timing is coordinated across the plant. Here we examine clock activity at the single cell level across Arabidopsis seedlings over several days under constant environmental conditions. Our data reveal robust single cell oscillations, albeit desynchronised. In particular, we observe two waves of clock activity; one going down, and one up the root. We also find evidence of cell-to-cell coupling of the clock, especially in the root tip. A simple model shows that cell-to-cell coupling and our measured period differences between cells can generate the observed waves. Our results reveal the spatial structure of the plant clock and suggest that unlike the centralised mammalian clock, the Arabidopsis clock has multiple coordination points.

Data availability

Single cell data is available from https://gitlab.com/slcu/teamJL/Gould_etal_2018

The following data sets were generated
    1. Gould PD
    2. Domijan M
    3. Greenwood M
    4. Tokuda IT
    5. Rees H
    6. Kozma-Bognar L
    7. Hall AJW
    8. Locke JCW
    (2018) WT
    https://gitlab.com/slcu/teamJL/Gould_etal_2018/tree/master/SingleCellFiles/Data_singlecell/WT_final_coordinates.
    1. Gould PD
    2. Domijan M
    3. Greenwood M
    4. Tokuda IT
    5. Rees H
    6. Kozma-Bognar L
    7. Hall AJW
    8. Locke JCW
    (2018) WT repeat
    https://gitlab.com/slcu/teamJL/Gould_etal_2018/tree/master/SingleCellFiles/Data_singlecell/WTrepeat_final_coordinates.
    1. Gould PD
    2. Domijan M
    3. Greenwood M
    4. Tokuda IT
    5. Rees H
    6. Kozma-Bognar L
    7. Hall AJW
    8. Locke JCW
    (2018) CCA1-Long
    https://gitlab.com/slcu/teamJL/Gould_etal_2018/tree/master/SingleCellFiles/Data_singlecell/CCA1-long_final_coordinates.

Article and author information

Author details

  1. Peter D Gould

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Mirela Domijan

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark Greenwood

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Isao T Tokuda

    Department of Mechanical Engineering, Ritsumeikan University, Kusatsu, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6212-0022
  5. Hannah Rees

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Laszlo Kozma-Bognar

    Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8289-193X
  7. Anthony JW Hall

    Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
    For correspondence
    anthony.hall@earlham.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  8. James CW Locke

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    james.locke@slcu.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0670-1943

Funding

Gatsby Charitable Foundation

  • James CW Locke

H2020 European Research Council

  • James CW Locke

Biotechnology and Biological Sciences Research Council

  • Peter D Gould
  • Mirela Domijan
  • Anthony JW Hall
  • James CW Locke

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Richard Amasino, University of Wisconsin, United States

Publication history

  1. Received: September 6, 2017
  2. Accepted: April 25, 2018
  3. Accepted Manuscript published: April 26, 2018 (version 1)
  4. Version of Record published: June 5, 2018 (version 2)

Copyright

© 2018, Gould et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Peter D Gould
  2. Mirela Domijan
  3. Mark Greenwood
  4. Isao T Tokuda
  5. Hannah Rees
  6. Laszlo Kozma-Bognar
  7. Anthony JW Hall
  8. James CW Locke
(2018)
Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression
eLife 7:e31700.
https://doi.org/10.7554/eLife.31700

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