Cell type boundaries organize plant development

  1. Monica Pia Caggiano
  2. Xiulian Yu
  3. Neha Bhatia
  4. André Larsson
  5. Hasthi Ram
  6. Carolyn K Ohno
  7. Pia Sappl
  8. Elliot M Meyerowitz
  9. Henrik Jönsson
  10. Marcus G Heisler  Is a corresponding author
  1. European Molecular Biology Laboratory, Germany
  2. Lund University, Sweden
  3. California Institute of Technology, United States
  4. University of Sydney, Australia

Abstract

In plants the dorsoventral boundary of leaves defines an axis of symmetry through the centre of the organ separating the top (dorsal) and bottom (ventral) tissues. Although the positioning of this boundary is critical for leaf morphogenesis, how the boundary is established and how it influences development remains unclear. Using live-imaging and perturbation experiments we show that leaf orientation, morphology and position are pre-patterned by HD-ZIPIII and KAN gene expression in the shoot, leading to a model in which dorsoventral genes coordinate to regulate plant development by localizing auxin response between their expression domains. However we also find that auxin levels feedback on dorsoventral patterning by spatially organizing HD-ZIPIII and KAN expression in the shoot periphery. By demonstrating that the regulation of these genes by auxin also governs their response to wounds, our results also provide a parsimonious explanation for the influence of wounds on leaf dorsoventrality.

Article and author information

Author details

  1. Monica Pia Caggiano

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiulian Yu

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Neha Bhatia

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. André Larsson

    Computational Biology and Biological Physics, Department of Astronomy and Theoretical Physics, Lund University, Lund, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Hasthi Ram

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Carolyn K Ohno

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Pia Sappl

    European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Elliot M Meyerowitz

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4798-5153
  9. Henrik Jönsson

    Computational Biology and Biological Physics, Department of Astronomy and Theoretical Physics, Lund University, Lund, Sweden
    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
  10. Marcus G Heisler

    School of Life and Environmental Sciences, University of Sydney, Sydney, Australia
    For correspondence
    marcus.heisler@sydney.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5644-8398

Funding

H2020 European Research Council (261081)

  • Marcus G Heisler

Marie Curie Actions (255089)

  • Pia Sappl

Gordon and Betty Moore Foundation (GBMF3406)

  • Elliot M Meyerowitz

Gatsby Charitable Foundation (GAT3395/PR4)

  • Henrik Jönsson

Swedish Research Council (VR2013-4632)

  • Henrik Jönsson

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

Version history

  1. Received: April 3, 2017
  2. Accepted: September 11, 2017
  3. Accepted Manuscript published: September 12, 2017 (version 1)
  4. Accepted Manuscript updated: September 25, 2017 (version 2)
  5. Version of Record published: September 27, 2017 (version 3)

Copyright

© 2017, Caggiano 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. Monica Pia Caggiano
  2. Xiulian Yu
  3. Neha Bhatia
  4. André Larsson
  5. Hasthi Ram
  6. Carolyn K Ohno
  7. Pia Sappl
  8. Elliot M Meyerowitz
  9. Henrik Jönsson
  10. Marcus G Heisler
(2017)
Cell type boundaries organize plant development
eLife 6:e27421.
https://doi.org/10.7554/eLife.27421

Share this article

https://doi.org/10.7554/eLife.27421

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