1. Plant Biology

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
https://doi.org/10.7554/eLife.34460
Share this article
Cite this article
  1. Stéphane Verger
  2. Yuchen Long
  3. Arezki Boudaoud
  4. Olivier Hamant
(2018)
A tension-adhesion feedback loop in plant epidermis
eLife 7:e34460.
https://doi.org/10.7554/eLife.34460
  2. Download BibTeX
  3. Download .RIS

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

Version 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.

Metrics

  • 6,029
    views
  • 890
    downloads
  • 110
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Stéphane Verger
  2. Yuchen Long
  3. Arezki Boudaoud
  4. Olivier Hamant
(2018)
A tension-adhesion feedback loop in plant epidermis
eLife 7:e34460.
https://doi.org/10.7554/eLife.34460

Share this article

https://doi.org/10.7554/eLife.34460

Categories and tags

Research organism

Further reading

    1. Plant Biology

    Single-molecule analysis reveals the phosphorylation of FLS2 governs its spatiotemporal dynamics and immunity

    Yaning Cui, Hongping Qian ... Jinxing Lin
    Short Report

    The Arabidopsis thaliana FLAGELLIN-SENSITIVE2 (FLS2), a typical receptor kinase, recognizes the conserved 22 amino acid sequence in the N-terminal region of flagellin (flg22) to initiate plant defense pathways, which was intensively studied in the past decades. However, the dynamic regulation of FLS2 phosphorylation at the plasma membrane after flg22 recognition needs further elucidation. Through single-particle tracking, we demonstrated that upon flg22 treatment the phosphorylation of Ser-938 in FLS2 impacts its spatiotemporal dynamics and lifetime. Following Förster resonance energy transfer-fluorescence lifetime imaging microscopy and protein proximity indexes assays revealed that flg22 treatment increased the co-localization of GFP-tagged FLS2/FLS2S938D but not FLS2S938A with AtRem1.3-mCherry, a sterol-rich lipid marker, indicating that the phosphorylation of FLS2S938 affects FLS2 sorting efficiency to AtRem1.3-associated nanodomains. Importantly, we found that the phosphorylation of Ser-938 enhanced flg22-induced FLS2 internalization and immune responses, demonstrating that the phosphorylation may activate flg22-triggered immunity through partitioning FLS2 into functional AtRem1.3-associated nanodomains, which fills the gap between the FLS2S938 phosphorylation and FLS2-mediated immunity.

    1. Plant Biology

    Unraveling the role of urea hydrolysis in salt stress response during seed germination and seedling growth in Arabidopsis thaliana

    Yuanyuan Bu, Xingye Dong ... Shenkui Liu
    Research Article

    Urea is intensively utilized as a nitrogen fertilizer in agriculture, originating either from root uptake or from catabolism of arginine by arginase. Despite its extensive use, the underlying physiological mechanisms of urea, particularly its adverse effects on seed germination and seedling growth under salt stress remains unclear. In this study, we demonstrate that salt stress induces excessive hydrolysis of arginine-derived urea, leading to an increase in cytoplasmic pH within seed radical cells, which, in turn, triggers salt-induced inhibition of seed germination (SISG) and hampers seedling growth. Our findings challenge the long-held belief that ammonium accumulation and toxicity are the primary causes of SISG, offering a novel perspective on the mechanism underlying these processes. This study provides significant insights into the physiological impact of urea hydrolysis under salt stress, contributing to a better understanding of SISG.