Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3
- The Sainsbury Laboratory, United Kingdom
- University of Lausanne, Switzerland
- University of Zurich, Switzerland
- The Sainsbury Laboratory,, United Kingdom
- 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
Andra-Octavia Roman
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.
Reviewing Editor
- Caroline Gutjahr, Technical University of Munich, Germany
Version history
- Received: October 13, 2021
- Preprint posted: October 26, 2021 (view preprint)
- Accepted: May 26, 2022
- Accepted Manuscript published: May 26, 2022 (version 1)
- Version of Record published: June 13, 2022 (version 2)
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.
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Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3
eLife 11:e74687.
https://doi.org/10.7554/eLife.74687
Further reading
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Transmembrane signaling by plant receptor kinases (RKs) has long been thought to involve reciprocal trans-phosphorylation of their intracellular kinase domains. The fact that many of these are pseudokinase domains, however, suggests that additional mechanisms must govern RK signaling activation. Non-catalytic signaling mechanisms of protein kinase domains have been described in metazoans, but information is scarce for plants. Recently, a non-catalytic function was reported for the leucine-rich repeat (LRR)-RK subfamily XIIa member EFR (elongation factor Tu receptor) and phosphorylation-dependent conformational changes were proposed to regulate signaling of RKs with non-RD kinase domains. Here, using EFR as a model, we describe a non-catalytic activation mechanism for LRR-RKs with non-RD kinase domains. EFR is an active kinase, but a kinase-dead variant retains the ability to enhance catalytic activity of its co-receptor kinase BAK1/SERK3 (brassinosteroid insensitive 1-associated kinase 1/somatic embryogenesis receptor kinase 3). Applying hydrogen-deuterium exchange mass spectrometry (HDX-MS) analysis and designing homology-based intragenic suppressor mutations, we provide evidence that the EFR kinase domain must adopt its active conformation in order to activate BAK1 allosterically, likely by supporting αC-helix positioning in BAK1. Our results suggest a conformational toggle model for signaling, in which BAK1 first phosphorylates EFR in the activation loop to stabilize its active conformation, allowing EFR in turn to allosterically activate BAK1.
