Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors

  1. Julien Gronnier  Is a corresponding author
  2. Christina M Franck
  3. Martin Stegmann
  4. Thomas A DeFalco
  5. Alicia Abarca
  6. Michelle Von Arx
  7. Kai Dünser
  8. Wenwei Lin
  9. Zhenbiao Yang
  10. Jürgen Kleine-Vehn
  11. Christoph Ringli
  12. Cyril Zipfel  Is a corresponding author
  1. University of Zurich, Switzerland
  2. Technical University of Munich, Germany
  3. University of Natural Resources and Life Sciences, Austria
  4. Fujian Agriculture and Forestry University, China
  5. University of Freiburg, Germany

Abstract

Spatial partitioning is a propensity of biological systems orchestrating cell activities in space and time. The dynamic regulation of plasma membrane nano-environments has recently emerged as a key fundamental aspect of plant signaling, but the molecular components governing it are still mostly unclear. The receptor kinase FERONIA (FER) controls ligand-induced complex formation of the immune receptor kinase FLAGELLIN SENSING 2 (FLS2) with its co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1), and perception of the endogenous peptide hormone RAPID ALKALANIZATION FACTOR 23 (RALF23) by FER inhibits immunity. Here, we show that FER regulates the plasma membrane nanoscale organization of FLS2 and BAK1. Our study demonstrates that akin to FER, leucine-rich repeat (LRR) extensin proteins (LRXs) contribute to RALF23 responsiveness, regulate BAK1 nanoscale organization and immune signaling. Furthermore, RALF23 perception leads to rapid modulation of FLS2 and BAK1 nanoscale organization, and its inhibitory activity on immune signaling relies on FER kinase activity. Our results suggest that perception of RALF peptides by FER and LRXs actively modulates plasma membrane nanoscale organization to regulate cell surface signaling by other ligand-binding receptor kinases.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Julien Gronnier

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    For correspondence
    julien.gronnier@zmbp.uni-tuebingen.de
    Competing interests
    No competing interests declared.
  2. Christina M Franck

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
  3. Martin Stegmann

    Phytopathology, School of Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
  4. Thomas A DeFalco

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
  5. Alicia Abarca

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3569-851X
  6. Michelle Von Arx

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
  7. Kai Dünser

    Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  8. Wenwei Lin

    FAFU-UCR Joint Center for Horticultural Biology and Metabolomics Center, Fujian Agriculture and Forestry University, Fuzhou, China
    Competing interests
    No competing interests declared.
  9. Zhenbiao Yang

    FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Fujian Agriculture and Forestry University, Fuzhou, China
    Competing interests
    No competing interests declared.
  10. Jürgen Kleine-Vehn

    Department of Molecular Plant Physiology, University of Freiburg, Freiburg, Germany
    Competing interests
    Jürgen Kleine-Vehn, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4354-3756
  11. Christoph Ringli

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
  12. Cyril Zipfel

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    For correspondence
    cyril.zipfel@botinst.uzh.ch
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4935-8583

Funding

H2020 European Research Council (309858)

  • Cyril Zipfel

Deutsche Forschungsgemeinschaft (STE 2448/1)

  • Martin Stegmann

H2020 European Research Council (773153)

  • Cyril Zipfel

LTF-EMBO (438-2018)

  • Julien Gronnier

LTF-EMBO (512-2019)

  • Christina M Franck

LTF-EMBO (100-2017)

  • Thomas A DeFalco

H2020 European Research Council (639678)

  • Jürgen Kleine-Vehn

Swiss National Science Foundation (31003A_182625)

  • Cyril Zipfel

Swiss National Science Foundation (31003A_166577/1)

  • Christoph Ringli

Austrian Science Fund (P 33044)

  • Jürgen Kleine-Vehn

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, United States

Publication history

  1. Preprint posted: July 21, 2020 (view preprint)
  2. Received: September 23, 2021
  3. Accepted: January 5, 2022
  4. Accepted Manuscript published: January 6, 2022 (version 1)
  5. Version of Record published: January 25, 2022 (version 2)

Copyright

© 2022, Gronnier 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. Julien Gronnier
  2. Christina M Franck
  3. Martin Stegmann
  4. Thomas A DeFalco
  5. Alicia Abarca
  6. Michelle Von Arx
  7. Kai Dünser
  8. Wenwei Lin
  9. Zhenbiao Yang
  10. Jürgen Kleine-Vehn
  11. Christoph Ringli
  12. Cyril Zipfel
(2022)
Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors
eLife 11:e74162.
https://doi.org/10.7554/eLife.74162

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