Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal

  1. Heather M Meyer
  2. José Teles
  3. Pau Formosa-Jordan
  4. Yassin Refahi
  5. Rita San- Bento
  6. Gwyneth Ingram
  7. Henrik Jönsson  Is a corresponding author
  8. James CW Locke  Is a corresponding author
  9. Adrienne HK Roeder  Is a corresponding author
  1. Cornell University, United States
  2. University of Cambridge, United Kingdom
  3. Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, France

Abstract

Multicellular development produces patterns of specialized cell types. Yet, it is often unclear how individual cells within a field of identical cells initiate the patterning process. Using live imaging, quantitative image analyses and modeling, we show that during Arabidopsis thaliana sepal development, fluctuations in the concentration of the transcription factor ATML1 pattern a field of identical epidermal cells to differentiate into giant cells interspersed between smaller cells. We find that ATML1 is expressed in all epidermal cells. However, its level fluctuates in each of these cells. If ATML1 levels surpass a threshold during the G2 phase of the cell cycle, the cell will likely enter a state of endoreduplication and become giant. Otherwise the cell divides. Our results demonstrate a fluctuation-driven patterning mechanism for how cell fate decisions can be initiated through a random yet tightly regulated process.

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Article and author information

Author details

  1. Heather M Meyer

    Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. José Teles

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Pau Formosa-Jordan

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3005-597X
  4. Yassin Refahi

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6136-608X
  5. Rita San- Bento

    Laboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Gwyneth Ingram

    Laboratoire Reproduction et Développement des Plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Henrik Jönsson

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    Henrik.Jonsson@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:" 0000-0003-2340-588X
  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
  9. Adrienne HK Roeder

    Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
    For correspondence
    ahr75@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6685-2984

Funding

National Science Foundation (IOS-1553030)

  • Adrienne HK Roeder

Gatsby Charitable Foundation (GAT3272/GLC)

  • James CW Locke

Swedish Research Council (VR2013:4632)

  • Henrik Jönsson

Herchel Smith Foundation

  • José Teles

National Science Foundation (IOS-1256733)

  • Adrienne HK Roeder

Gatsby Charitable Foundation (GAT3395/PR4)

  • Henrik Jönsson

Herchel Smith Foundation

  • Pau Formosa-Jordan

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

Reviewing Editor

  1. Dominique C Bergmann, Stanford University/HHMI, United States

Publication history

  1. Received: June 26, 2016
  2. Accepted: January 31, 2017
  3. Accepted Manuscript published: February 1, 2017 (version 1)
  4. Version of Record published: March 2, 2017 (version 2)

Copyright

© 2017, Meyer 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. Heather M Meyer
  2. José Teles
  3. Pau Formosa-Jordan
  4. Yassin Refahi
  5. Rita San- Bento
  6. Gwyneth Ingram
  7. Henrik Jönsson
  8. James CW Locke
  9. Adrienne HK Roeder
(2017)
Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal
eLife 6:e19131.
https://doi.org/10.7554/eLife.19131
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