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.

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.

Metrics

  • 3,170
    views
  • 606
    downloads
  • 52
    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. 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

Share this article

https://doi.org/10.7554/eLife.44474

Further reading

    1. Plant Biology
    2. Structural Biology and Molecular Biophysics
    Théo Le Moigne, Martina Santoni ... Julien Henri
    Research Article

    The Calvin-Benson-Bassham cycle (CBBC) performs carbon fixation in photosynthetic organisms. Among the eleven enzymes that participate in the pathway, sedoheptulose-1,7-bisphosphatase (SBPase) is expressed in photo-autotrophs and catalyzes the hydrolysis of sedoheptulose-1,7-bisphosphate (SBP) to sedoheptulose-7-phosphate (S7P). SBPase, along with nine other enzymes in the CBBC, contributes to the regeneration of ribulose-1,5-bisphosphate, the carbon-fixing co-substrate used by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). The metabolic role of SBPase is restricted to the CBBC, and a recent study revealed that the three-dimensional structure of SBPase from the moss Physcomitrium patens was found to be similar to that of fructose-1,6-bisphosphatase (FBPase), an enzyme involved in both CBBC and neoglucogenesis. In this study we report the first structure of an SBPase from a chlorophyte, the model unicellular green microalga Chlamydomonas reinhardtii. By combining experimental and computational structural analyses, we describe the topology, conformations, and quaternary structure of Chlamydomonas reinhardtii SBPase (CrSBPase). We identify active site residues and locate sites of redox- and phospho-post-translational modifications that contribute to enzymatic functions. Finally, we observe that CrSBPase adopts distinct oligomeric states that may dynamically contribute to the control of its activity.

    1. Plant Biology
    Maryam Rahmati Ishka, Hayley Sussman ... Magdalena M Julkowska
    Research Article

    Soil salinity is one of the major threats to agricultural productivity worldwide. Salt stress exposure alters root and shoots growth rates, thereby affecting overall plant performance. While past studies have extensively documented the effect of salt stress on root elongation and shoot development separately, here we take an innovative approach by examining the coordination of root and shoot growth under salt stress conditions. Utilizing a newly developed tool for quantifying the root:shoot ratio in agar-grown Arabidopsis seedlings, we found that salt stress results in a loss of coordination between root and shoot growth rates. We identify a specific gene cluster encoding domain-of-unknown-function 247 (DUF247), and characterize one of these genes as Salt Root:shoot Ratio Regulator Gene (SR3G). Further analysis elucidates the role of SR3G as a negative regulator of salt stress tolerance, revealing its function in regulating shoot growth, root suberization, and sodium accumulation. We further characterize that SR3G expression is modulated by WRKY75 transcription factor, known as a positive regulator of salt stress tolerance. Finally, we show that the salt stress sensitivity of wrky75 mutant is completely diminished when it is combined with sr3g mutation. Together, our results demonstrate that utilizing root:shoot ratio as an architectural feature leads to the discovery of a new stress resilience gene. The study’s innovative approach and findings not only contribute to our understanding of plant stress tolerance mechanisms but also open new avenues for genetic and agronomic strategies to enhance crop environmental resilience.