Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

  1. Ivan Lebovka
  2. Bruno Hay Mele
  3. Xiaomin Liu
  4. Alexandra Zakieva
  5. Theresa Schlamp
  6. Nial Rau Gursanscky
  7. Roeland MH Merks
  8. Ruth Großeholz  Is a corresponding author
  9. Thomas Greb  Is a corresponding author
  1. Heidelberg University, Germany
  2. Università degli Studi di Napoli Federico II, Italy
  3. Gregor Mendel Institute, Austria
  4. Leiden University, Netherlands

Abstract

Precise organization of growing structures is a fundamental process in developmental biology. In plants, radial growth is mediated by the cambium, a stem cell niche continuously producing wood (xylem) and bast (phloem) in a strictly bidirectional manner. While this process contributes large parts to terrestrial biomass, cambium dynamics eludes direct experimental access due to obstacles in live cell imaging. Here, we present a cell-based computational model visualizing cambium activity and integrating the function of central cambium regulators. Performing iterative comparisons of plant and model anatomies, we conclude that the receptor-like kinase PXY and its ligand CLE41 are part of a minimal framework sufficient for instructing tissue organization. By integrating tissue-specific cell wall stiffness values, we moreover probe the influence of physical constraints on tissue geometry. Our model highlights the role of intercellular communication within the cambium and shows that a limited number of factors is sufficient to create radial growth by bidirectional tissue production.

Data availability

Code files for presented models are deposited at https://github.com/thomasgreb/Lebovka-et-al_cambium-models.

Article and author information

Author details

  1. Ivan Lebovka

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Bruno Hay Mele

    Department of Agricultural Sciences, Università degli Studi di Napoli Federico II, Napoli, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5579-183X
  3. Xiaomin Liu

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandra Zakieva

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Theresa Schlamp

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Nial Rau Gursanscky

    Plant Science, Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  7. Roeland MH Merks

    Mathematical Institute and Institute of Biology, Leiden University, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6152-687X
  8. Ruth Großeholz

    BioQuant, Heidelberg University, Heidelberg, Germany
    For correspondence
    ruth.grosseholz@bioquant.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
  9. Thomas Greb

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    For correspondence
    thomas.greb@cos.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6176-646X

Funding

Deutsche Forschungsgemeinschaft (GR2104/4-1)

  • Thomas Greb

Deutsche Forschungsgemeinschaft (GR2104/5-2)

  • Thomas Greb

Deutsche Forschungsgemeinschaft (GR2104/6)

  • Thomas Greb

Joachim Herz Stiftung

  • Ruth Großeholz

Deutsche Forschungsgemeinschaft (CRC 1101)

  • Ruth Großeholz

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

Reviewing Editor

  1. Krzysztof Wabnik, Technical University of Madrid, Spain

Version history

  1. Preprint posted: January 17, 2020 (view preprint)
  2. Received: January 17, 2021
  3. Accepted: March 6, 2023
  4. Accepted Manuscript published: March 10, 2023 (version 1)
  5. Version of Record published: April 3, 2023 (version 2)

Copyright

© 2023, Lebovka 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. Ivan Lebovka
  2. Bruno Hay Mele
  3. Xiaomin Liu
  4. Alexandra Zakieva
  5. Theresa Schlamp
  6. Nial Rau Gursanscky
  7. Roeland MH Merks
  8. Ruth Großeholz
  9. Thomas Greb
(2023)
Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth
eLife 12:e66627.
https://doi.org/10.7554/eLife.66627

Share this article

https://doi.org/10.7554/eLife.66627

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