Why plants make puzzle cells, and how their shape emerges

  1. Aleksandra Sapala
  2. Adam Runions
  3. Anne-Lise Routier-Kierzkowska
  4. Mainak Das Gupta
  5. Lilan Hong
  6. Hugo Hofhuis
  7. Stéphane Verger
  8. Gabriella Mosca
  9. Chun-Biu Li
  10. Angela Hay
  11. Olivier Hamant
  12. Adrienne HK Roeder
  13. Miltos Tsiantis
  14. Przemyslaw Prusinkiewicz
  15. Richard S Smith  Is a corresponding author
  1. Max Planck Institute for Plant Breeding Research, Germany
  2. Cornell University, United States
  3. Université de Lyon, France
  4. Stockholm University, Sweden
  5. University of Calgary, Canada

Abstract

The shape and function of plant cells are often highly interdependent. The puzzle-shaped cells that appear in the epidermis of many plants are a striking example of a complex cell shape, however their functional benefit has remained elusive. We propose that these intricate forms provide an effective strategy to reduce mechanical stress in the cell wall of the epidermis. When tissue-level growth is isotropic, we hypothesize that lobes emerge at the cellular level to prevent formation of large isodiametric cells that would bulge under the stress produced by turgor pressure. Data from various plant organs and species support the relationship between lobes and growth isotropy, which we test with mutants where growth direction is perturbed. Using simulation models we show that a mechanism actively regulating cellular stress plausibly reproduces the development of epidermal cell shape. Together, our results suggest that mechanical stress is a key driver of cell-shape morphogenesis.

Article and author information

Author details

  1. Aleksandra Sapala

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Adam Runions

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Anne-Lise Routier-Kierzkowska

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Mainak Das Gupta

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Lilan Hong

    Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Hugo Hofhuis

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Stéphane Verger

    Laboratoire Reproduction et Développement des Plantes, Université de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3643-3978
  8. Gabriella Mosca

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Chun-Biu Li

    Department of Mathematics, Stockholm University, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8009-6265
  10. Angela Hay

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Olivier Hamant

    Laboratoire de Reproduction de développement des plantes, Institut national de la recherche agronomique, Centre national de la recherche scientifique, ENS Lyon, Claude Bernard University Lyon, Université de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6906-6620
  12. Adrienne HK Roeder

    Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States
    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
  13. Miltos Tsiantis

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Przemyslaw Prusinkiewicz

    Department of Computer Science, University of Calgary, Calgary, Canada
    Competing interests
    The authors declare that no competing interests exist.
  15. Richard S Smith

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    For correspondence
    smith@mpipz.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9220-0787

Funding

Swiss National Science Foundation (SystemsX.ch iPhD grant 2010/073)

  • Richard S Smith

Bundesministerium für Bildung und Forschung (031A492)

  • Richard S Smith

Human Frontier Science Program (RGP0008/2013)

  • Chun-Biu Li
  • Olivier Hamant
  • Adrienne HK Roeder
  • Richard S Smith

European Commission (Marie Skłodowska-Curie individual fellowship (Horizon 2020 703886))

  • Adam Runions

Natural Science and Engineering Research Council of Canada (Discovery Grant RGPIN-2014-05325)

  • Przemyslaw Prusinkiewicz

European Research Council (ERC-2013-CoG-615739 'MechanoDevo')

  • Olivier Hamant

Max Planck Society (Core grant and open-access funding)

  • Miltos Tsiantis
  • Richard S Smith

Bundesministerium für Bildung und Forschung (031A494)

  • Richard S Smith

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

Reviewing Editor

  1. Sheila McCormick, University of California-Berkeley, United States

Publication history

  1. Received: October 13, 2017
  2. Accepted: January 31, 2018
  3. Accepted Manuscript published: February 27, 2018 (version 1)
  4. Version of Record published: March 7, 2018 (version 2)

Copyright

© 2018, Sapala 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. Aleksandra Sapala
  2. Adam Runions
  3. Anne-Lise Routier-Kierzkowska
  4. Mainak Das Gupta
  5. Lilan Hong
  6. Hugo Hofhuis
  7. Stéphane Verger
  8. Gabriella Mosca
  9. Chun-Biu Li
  10. Angela Hay
  11. Olivier Hamant
  12. Adrienne HK Roeder
  13. Miltos Tsiantis
  14. Przemyslaw Prusinkiewicz
  15. Richard S Smith
(2018)
Why plants make puzzle cells, and how their shape emerges
eLife 7:e32794.
https://doi.org/10.7554/eLife.32794

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