1. Plant Biology
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A tension-adhesion feedback loop in plant epidermis

  1. Stéphane Verger  Is a corresponding author
  2. Yuchen Long
  3. Arezki Boudaoud
  4. Olivier Hamant  Is a corresponding author
  1. Université de Lyon, ENS de Lyon, France
Research Article
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Cite this article as: eLife 2018;7:e34460 doi: 10.7554/eLife.34460

Abstract

Mechanical forces have emerged as coordinating signals for most cell functions. Yet, because forces are invisible, mapping tensile stress patterns in tissues remains a major challenge in all kingdoms. Here we take advantage of the adhesion defects in the Arabidopsis mutant quasimodo1 (qua1) to deduce stress patterns in tissues. By reducing the water potential and epidermal tension in planta, we rescued the adhesion defects in qua1, formally associating gaping and tensile stress patterns in the mutant. Using suboptimal water potential conditions, we revealed the relative contributions of shape- and growth-derived stress in prescribing maximal tension directions in aerial tissues. Consistently, the tension patterns deduced from the gaping patterns in qua1 matched the pattern of cortical microtubules, which are thought to align with maximal tension, in wild-type organs. Conversely, loss of epidermis continuity in the qua1 mutant hampered supracellular microtubule alignments, revealing that coordination through tensile stress requires cell-cell adhesion.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data file for cell_separation_analysis pipeline has been provided and a reference to Github (where the code is now stored) has been added in the main text and Material and methods.

Article and author information

Author details

  1. Stéphane Verger

    Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, Lyon, France
    For correspondence
    stephane.verger@ens-lyon.fr
    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
  2. Yuchen Long

    Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Arezki Boudaoud

    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, ENS de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  4. 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, ENS de Lyon, Lyon, France
    For correspondence
    Olivier.Hamant@ens-lyon.fr
    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

Funding

H2020 European Research Council (ERC-2013-CoG-615739)

  • Olivier Hamant

European Molecular Biology Organization (EMBO ALTF 168-2015)

  • Yuchen Long

H2020 European Research Council (ERC-2012-StG-307387)

  • Arezki Boudaoud

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: December 18, 2017
  2. Accepted: April 20, 2018
  3. Accepted Manuscript published: April 23, 2018 (version 1)
  4. Version of Record published: May 22, 2018 (version 2)
  5. Version of Record updated: October 16, 2018 (version 3)
  6. Version of Record updated: March 23, 2020 (version 4)

Copyright

© 2018, Verger 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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Further reading

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    Chloroplast biogenesis describes the transition of non-photosynthetic proplastids to photosynthetically active chloroplasts in the cells of germinating seeds. Chloroplast biogenesis requires the import of thousands of nuclear-encoded preproteins by essential import receptor TOC159. We demonstrate that the small ubiquitin-related modifier (SUMO) pathway crosstalks with the ubiquitin–proteasome pathway to affect TOC159 stability during early plant development. We identified a SUMO3-interacting motif (SIM) in the TOC159 GTPase domain and a SUMO3 covalent SUMOylation site in the membrane domain. A single K to R substitution (K1370R) in the M-domain disables SUMOylation. Compared to wild-type TOC159, TOC159K1370R was destabilized under UPS-inducing stress conditions. However, TOC159K1370R recovered to same protein level as wild-type TOC159 in the presence of a proteasome inhibitor. Thus, SUMOylation partially stabilizes TOC159 against UPS-dependent degradation under stress conditions. Our data contribute to the evolving model of tightly controlled proteostasis of the TOC159 import receptor during proplastid to chloroplast transition.