Anion channel SLAH3 is a regulatory target of chitin receptor-associated kinase PBL27 in microbial stomatal closure

  1. Yi Liu
  2. Tobias Maierhofer
  3. Katarzyna Rybak
  4. Jan Sklenar
  5. Andy Breakspear
  6. Matthew G Johnston
  7. Judith Fliegmann
  8. Shouguang Huang
  9. M Rob G Roelfsema
  10. Georg Felix
  11. Christine Faulkner
  12. Frank LH Menke
  13. Dietmar Geiger
  14. Rainer Hedrich  Is a corresponding author
  15. Silke Robatzek  Is a corresponding author
  1. The Sainsbury Laboratory, United Kingdom
  2. University of Würzburg, Germany
  3. Ludwig-Maximilian-University of Munich, Germany
  4. John Innes Centre, United Kingdom
  5. University of Tübingen, Germany

Abstract

In plants, antimicrobial immune responses involve the cellular release of anions and are responsible for the closure of stomatal pores. Detection of microbe-associated molecular patterns (MAMPs) by pattern recognition receptors (PRRs) induces currents mediated via slow-type (S-type) anion channels by a yet not understood mechanism. Here, we show that stomatal closure to fungal chitin is conferred by the major PRRs for chitin recognition, LYK5 and CERK1, the receptor-like cytoplasmic kinase PBL27, and the SLAH3 anion channel. PBL27 has the capacity to phosphorylate SLAH3, of which S127 and S189 are required to activate SLAH3. Full activation of the channel entails CERK1, depending on PBL27. Importantly, both S127 and S189 residues of SLAH3 are required for chitin-induced stomatal closure and anti-fungal immunity at the whole leaf level. Our results demonstrate a short signal transduction module from MAMP recognition to anion channel activation, and independent of ABA-induced SLAH3 activation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for main and supplemental figures.

Article and author information

Author details

  1. Yi Liu

    The Sainsbury Laboratory, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Tobias Maierhofer

    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Katarzyna Rybak

    LMU Biocenter, Ludwig-Maximilian-University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Jan Sklenar

    The Sainsbury Laboratory, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Andy Breakspear

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew G Johnston

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1141-6135
  7. Judith Fliegmann

    Department of Plant Biochemistry, Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Shouguang Huang

    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. M Rob G Roelfsema

    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Georg Felix

    Department of Plant Biochemistry, Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Christine Faulkner

    John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3905-8077
  12. Frank LH Menke

    The Sainsbury Laboratory, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2490-4824
  13. Dietmar Geiger

    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0715-5710
  14. Rainer Hedrich

    Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany
    For correspondence
    hedrich@botanik.uni-wuerzburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3224-1362
  15. Silke Robatzek

    LMU Biocenter, Ludwig-Maximilian-University of Munich, Martinsried, Germany
    For correspondence
    robatzek@bio.lmu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9788-322X

Funding

Gatsby Charitable Foundation (Group Leader Fellowship)

  • Silke Robatzek

H2020 European Research Council (Project Award)

  • Silke Robatzek

Biotechnology and Biological Sciences Research Council (Project Award)

  • Christine Faulkner

Deutsche Forschungsgemeinschaft (Project Award)

  • Dietmar Geiger
  • Rainer Hedrich

Deutsche Forschungsgemeinschaft (Project Award)

  • Rainer Hedrich

Deutsche Forschungsgemeinschaft (Heisenberg Fellowship)

  • Silke Robatzek

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

Reviewing Editor

  1. Jian-Min Zhou, Chinese Academy of Sciences, China

Publication history

  1. Received: December 17, 2018
  2. Accepted: September 13, 2019
  3. Accepted Manuscript published: September 16, 2019 (version 1)
  4. Version of Record published: October 3, 2019 (version 2)

Copyright

© 2019, Liu 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. Yi Liu
  2. Tobias Maierhofer
  3. Katarzyna Rybak
  4. Jan Sklenar
  5. Andy Breakspear
  6. Matthew G Johnston
  7. Judith Fliegmann
  8. Shouguang Huang
  9. M Rob G Roelfsema
  10. Georg Felix
  11. Christine Faulkner
  12. Frank LH Menke
  13. Dietmar Geiger
  14. Rainer Hedrich
  15. Silke Robatzek
(2019)
Anion channel SLAH3 is a regulatory target of chitin receptor-associated kinase PBL27 in microbial stomatal closure
eLife 8:e44474.
https://doi.org/10.7554/eLife.44474

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