Computational modeling and quantitative physiology reveal central parameters for brassinosteroid-regulated early cell physiological processes linked to elongation growth of the Arabidopsis root

Abstract

Brassinosteroids (BR) are key hormonal regulators of plant development. However, whereas the individual components of BR perception and signaling are well characterized experimentally, the question of how they can act and whether they are sufficient to carry out the critical function of cellular elongation remains open. Here, we combined computational modeling with quantitative cell physiology to understand the dynamics of the plasma membrane (PM)-localized BR response pathway during the initiation of cellular responses in the epidermis of the Arabidopsis root tip that are be linked to cell elongation. The model, consisting of ordinary differential equations, comprises the BR induced hyperpolarization of the PM, the acidification of the apoplast and subsequent cell wall swelling. We demonstrate that the competence of the root epidermal cells for the BR response predominantly depends on the amount and activity of H+-ATPases in the PM. The model further predicts that an influx of cations is required to compensate for the shift of positive charges caused by the apoplastic acidification. A potassium channel was subsequently identified and experimentally characterized, fulfilling this function. Thus, we established the landscape of components and parameters for physiological processes potentially linked to cell elongation, a central process in plant development.

Data availability

All data generated and analysed during this study are included in the manuscript and the supporting file (Appendix 1). Raw and metadata are provided for Figures 4, 5, 6, 7 and 8 as well as for Appendix 1 Figures 2, 3, 4 and 6. Figure 1 represents scheme of early BRI1 signaling and Figure 2 the scheme of the used model structure. Predominantly published scRNA-Seq data were used for Figure 3. Modelling codes are available in supporting file (Appendix 1 - model information).

The following previously published data sets were used

Article and author information

Author details

  1. 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.
  2. Friederike Wanke

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Leander Rohr

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4592-4197
  4. Nina Glöckner

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Luiselotte Rausch

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Stefan Scholl

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Emanuele Scacchi

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Amelie-Jette Spazierer

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Lana Shabala

    Tasmanian Institute for Agriculture, University of Tasmania, Hobard, Australia
    Competing interests
    The authors declare that no competing interests exist.
  10. Sergey Shabala

    Tasmanian Institute for Agriculture, University of Tasmania, Hobart, Australia
    Competing interests
    The authors declare that no competing interests exist.
  11. Karin Schumacher

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6484-8105
  12. Ursula Kummer

    Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Klaus Harter

    Center for Molecular Biology of Plants, University of Tübingen, Tübingen, Germany
    For correspondence
    klaus.harter@zmbp.uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2150-6970

Funding

Deutsche Forschungsgemeinschaft (CRC 1101)

  • Karin Schumacher
  • Ursula Kummer
  • Klaus Harter

Deutsche Forschungsgemeinschaft ((INST 37/819- 594 1 FUGG,INST 37/965-1 FUGG,INST 37/991-1 FUGG,INST 37/992-1 FUGG)

  • Klaus Harter

Schmeil Stiftung (RG)

  • Ruth Großeholz

Joachim Herz Stiftung (RG)

  • 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, CBGP Centro de Biotecnologia y Genomica de Plantas UPM-INIA, Spain

Version history

  1. Preprint posted: April 14, 2021 (view preprint)
  2. Received: August 13, 2021
  3. Accepted: September 3, 2022
  4. Accepted Manuscript published: September 7, 2022 (version 1)
  5. Accepted Manuscript updated: September 13, 2022 (version 2)
  6. Version of Record published: September 30, 2022 (version 3)

Copyright

© 2022, Großeholz 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. Ruth Großeholz
  2. Friederike Wanke
  3. Leander Rohr
  4. Nina Glöckner
  5. Luiselotte Rausch
  6. Stefan Scholl
  7. Emanuele Scacchi
  8. Amelie-Jette Spazierer
  9. Lana Shabala
  10. Sergey Shabala
  11. Karin Schumacher
  12. Ursula Kummer
  13. Klaus Harter
(2022)
Computational modeling and quantitative physiology reveal central parameters for brassinosteroid-regulated early cell physiological processes linked to elongation growth of the Arabidopsis root
eLife 11:e73031.
https://doi.org/10.7554/eLife.73031

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https://doi.org/10.7554/eLife.73031

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