Activation loop phosphorylaton of a non-RD receptor kinase initiates plant innate immune signaling

Bender, Kyle W., Couto, Daniel, Kadota, Yasuhiro, Macho, Alberto P., Sklenar, Jan, Derbyshire, Paul, Bjornson, Marta, Defalco, Thomas A., Petriello, Annalise, Font Farre, Maria, Schwessinger, Benjamin, Ntoukakis, Vardis, Stransfeld, Lena, Jones, Alexandra M. E., Menke, Frank L. H. and Zipfel, Cyril (2021) Activation loop phosphorylaton of a non-RD receptor kinase initiates plant innate immune signaling. Proceedings of the National Academy of Sciences of the United States of America (PNAS), 118 (38). ISSN 0027-8424

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Abstract

Receptor kinases (RKs) are fundamental for extracellular sensing and regulate development and stress responses across kingdoms. In plants, leucine-rich repeat receptor kinases (LRR-RKs) are primarily peptide receptors that regulate responses to myriad internal and external stimuli. Phosphorylation of LRR-RK cytoplasmic domains is among the earliest responses following ligand perception, and reciprocal transphosphorylation between a receptor and its coreceptor is thought to activate the receptor complex. Originally proposed based on characterization of the brassinosteroid receptor, the prevalence of complex activation via reciprocal transphosphorylation across the plant RK family has not been tested. Using the LRR-RK ELONGATION FACTOR TU RECEPTOR (EFR) as a model, we set out to understand the steps critical for activating RK complexes. While the EFR cytoplasmic domain is an active protein kinase in vitro and is phosphorylated in a ligand-dependent manner in vivo, catalytically deficient EFR variants are functional in antibacterial immunity. These results reveal a noncatalytic role for EFR in triggering immune signaling and indicate that reciprocal transphoshorylation is not a ubiquitous requirement for LRR-RK complex activation. Rather, our analysis of EFR along with a detailed survey of the literature suggests a distinction between LRR-RKs with RD- versus non-RD protein kinase domains. Based on newly identified phosphorylation sites that regulate the activation state of the EFR complex in vivo, we propose that LRR-RK complexes containing a non-RD protein kinase may be regulated by phosphorylation-dependent conformational changes of the ligand-binding receptor, which could initiate signaling either allosterically or through driving the dissociation of negative regulators of the complex.

Item Type: Article
Additional Information: Funding Information: Gatsby Charitable Foundation, Biotechnology and Biological Research Council (BB/P012574/1), the European Research Council under the European Union’s Horizon 2020 research and innovation program (Grants 309858, project PHOSPHinnATE, and 773153, Project IMMUNO-PEPTALK), the University of Zürich, and the Swiss National Science Foundation Grant 31003A_182625, and a joint European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) grant (‘SICOPID’) from UK Research and Innovation (BB/S004734/1). Y.K. was supported by fellowships from RIKEN Special Postdoctoral Research Fellowship, Japanese Society for the Promotion of Science Excellent Young Researcher Overseas Visit Program, and the Uehara Memorial Foundation. M.B. was supported by the European Union’s Horizon 2020 Research and Innovation Program under Marie Skłodowska-Curie Actions (Grant 703954). B.S. was part of the John Innes Centre/The Sainsbury Laboratory PhD Rotation Program. T.A.D. was supported by postdoctoral fellowships from the European Molecular Biology Organization (EMBO LTF 100-2017) and the Natural Sciences and Engineering Research Council of Canada (NSERC PDF-532561-2019). Acknowledgements: We thank The Sainsbury Laboratory Plant Transformation support group for plant transformation; the John Innes Centre Horticultural Services and Tamaryn Ellick for plant care; and all past and current members of the C.Z. group for fruitful discussions.
Uncontrolled Keywords: phosphorylation,receptor kinase,signaling,general ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School:
Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 22 Sep 2021 02:06
Last Modified: 06 Oct 2021 01:58
URI: https://ueaeprints.uea.ac.uk/id/eprint/81482
DOI: 10.1073/pnas.2108242118

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