Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3

  1. Jack Rhodes
  2. Andra-Octavia Roman
  3. Marta Bjornson
  4. Benjamin Brandt
  5. Paul Derbyshire
  6. Michele Wyler
  7. Marc W Schmid
  8. Frank LH Menke
  9. Julia Santiago
  10. Cyril Zipfel  Is a corresponding author
  1. The Sainsbury Laboratory, United Kingdom
  2. University of Lausanne, Switzerland
  3. University of Zurich, Switzerland
  4. The Sainsbury Laboratory,, United Kingdom
  5. MWSchmid GmbH, Switzerland

Abstract

Plant genomes encode hundreds of secreted peptides; however, relatively few have been characterised. We report here an uncharacterised, stress-induced family of plant signalling peptides, which we call CTNIPs. Based on the role of the common co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) in CTNIP-induced responses, we identified in Arabidopsis thaliana the orphan receptor kinase HAESA-LIKE 3 (HSL3) as the CTNIP receptor via a proteomics approach. CTNIP binding, ligand-triggered complex formation with BAK1, and induced downstream responses all involve HSL3. Notably, the HSL3-CTNIP signalling module is evolutionarily conserved amongst most extant angiosperms. The identification of this novel signalling module will further shed light on the diverse functions played by plant signalling peptides and will provide insights into receptor-ligand co-evolution.

Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE (Perez-Riverol et al., 2016) partner repository with the dataset identifier PXD029264 and 10.6019/PXD029264The RNA-seq datasets generated and analysed in the current study have been deposited in the ArrayExpress database at EMBL-EBI (www.ebi.ac.uk/arrayexpress) under accession number E-MTAB-11093.

Article and author information

Author details

  1. Jack Rhodes

    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:" 0000-0002-3953-1648
  2. Andra-Octavia Roman

    Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3037-3321
  3. Marta Bjornson

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8275-4521
  4. Benjamin Brandt

    Institute of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5867-8760
  5. Paul Derbyshire

    The Sainsbury Laboratory,, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Michele Wyler

    MWSchmid GmbH, Glarus, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1097-5322
  7. Marc W Schmid

    MWSchmid GmbH, Glarus, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. 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
  9. Julia Santiago

    Department of Plant Molecular Biology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  10. Cyril Zipfel

    Department of Plant Molecular Biology, University of Zurich, Zurich, Switzerland
    For correspondence
    cyril.zipfel@botinst.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4935-8583

Funding

H2020 European Research Council (773153)

  • Cyril Zipfel

H2020 European Research Council (716358)

  • Julia Santiago

The Gatsby Charitable Foundation

  • Cyril Zipfel

Universität Zürich

  • Cyril Zipfel

Swiss National Science Foundation (31003A_182625)

  • Cyril Zipfel

Swiss National Science Foundation (31003A_173101)

  • Julia Santiago

Fondation philanthropique Famille Sandoz

  • Julia Santiago

H2020 Marie Skłodowska-Curie Actions (703954)

  • Marta Bjornson

Biotechnology and Biological Sciences Research Council (BB/P012574/1)

  • Cyril Zipfel

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

Copyright

© 2022, Rhodes 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

  • 4,332
    views
  • 1,370
    downloads
  • 25
    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. Jack Rhodes
  2. Andra-Octavia Roman
  3. Marta Bjornson
  4. Benjamin Brandt
  5. Paul Derbyshire
  6. Michele Wyler
  7. Marc W Schmid
  8. Frank LH Menke
  9. Julia Santiago
  10. Cyril Zipfel
(2022)
Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3
eLife 11:e74687.
https://doi.org/10.7554/eLife.74687

Share this article

https://doi.org/10.7554/eLife.74687

Further reading

    1. Cell Biology
    2. Plant Biology
    Masanori Izumi, Sakuya Nakamura ... Shinya Hagihara
    Research Article

    Plants distribute many nutrients to chloroplasts during leaf development and maturation. When leaves senesce or experience sugar starvation, the autophagy machinery degrades chloroplast proteins to facilitate efficient nutrient reuse. Here, we report on the intracellular dynamics of an autophagy pathway responsible for piecemeal degradation of chloroplast components. Through live-cell monitoring of chloroplast morphology, we observed the formation of chloroplast budding structures in sugar-starved leaves. These buds were then released and incorporated into the vacuolar lumen as an autophagic cargo termed a Rubisco-containing body. The budding structures did not accumulate in mutants of core autophagy machinery, suggesting that autophagosome creation is required for forming chloroplast buds. Simultaneous tracking of chloroplast morphology and autophagosome development revealed that the isolation membranes of autophagosomes interact closely with part of the chloroplast surface before forming chloroplast buds. Chloroplasts then protrude at the site associated with the isolation membranes, which divide synchronously with autophagosome maturation. This autophagy-related division does not require DYNAMIN-RELATED PROTEIN 5B, which constitutes the division ring for chloroplast proliferation in growing leaves. An unidentified division machinery may thus fragment chloroplasts for degradation in coordination with the development of the chloroplast-associated isolation membrane.

    1. Plant Biology
    Koji Kato, Yoshiki Nakajima ... Ryo Nagao
    Research Article

    Photosynthetic organisms exhibit remarkable diversity in their light-harvesting complexes (LHCs). LHCs are associated with photosystem I (PSI), forming a PSI-LHCI supercomplex. The number of LHCI subunits, along with their protein sequences and pigment compositions, has been found to differ greatly among the PSI-LHCI structures. However, the mechanisms by which LHCIs recognize their specific binding sites within the PSI core remain unclear. In this study, we determined the cryo-electron microscopy structure of a PSI supercomplex incorporating fucoxanthin chlorophyll a/c-binding proteins (FCPs), designated as PSI-FCPI, isolated from the diatom Thalassiosira pseudonana CCMP1335. Structural analysis of PSI-FCPI revealed five FCPI subunits associated with a PSI monomer; these subunits were identified as RedCAP, Lhcr3, Lhcq10, Lhcf10, and Lhcq8. Through structural and sequence analyses, we identified specific protein–protein interactions at the interfaces between FCPI and PSI subunits, as well as among FCPI subunits themselves. Comparative structural analyses of PSI-FCPI supercomplexes, combined with phylogenetic analysis of FCPs from T. pseudonana and the diatom Chaetoceros gracilis, underscore the evolutionary conservation of protein motifs crucial for the selective binding of individual FCPI subunits. These findings provide significant insights into the molecular mechanisms underlying the assembly and selective binding of FCPIs in diatoms.