Subtilase-mediated biogenesis of the expanded family of SERINE RICH ENDOGENOUS PEPTIDES

Yang, Huanjie, Kim, Xeniya, Skłenar, Jan, Aubourg, Sébastien, Sancho-Andrés, Gloria, Stahl, Elia, Guillou, Marie Charlotte, Gigli-Bisceglia, Nora, Tran Van Canh, Loup, Bender, Kyle W., Stintzi, Annick, Reymond, Philippe, Sánchez-Rodríguez, Clara, Testerink, Christa, Renou, Jean Pierre, Menke, Frank L. H. ORCID: https://orcid.org/0000-0003-2490-4824, Schaller, Andreas, Rhodes, Jack and Zipfel, Cyril (2023) Subtilase-mediated biogenesis of the expanded family of SERINE RICH ENDOGENOUS PEPTIDES. Nature Plants, 9 (12). pp. 2085-2094. ISSN 2055-026X

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Abstract

Plant signalling peptides are typically released from larger precursors by proteolytic cleavage to regulate plant growth, development and stress responses. Recent studies reported the characterization of a divergent family of Brassicaceae-specific peptides, SERINE RICH ENDOGENOUS PEPTIDES (SCOOPs), and their perception by the leucine-rich repeat receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2 (MIK2). Here, we reveal that the SCOOP family is highly expanded, containing at least 50 members in the Columbia-0 reference Arabidopsis thaliana genome. Notably, perception of these peptides is strictly MIK2-dependent. How bioactive SCOOP peptides are produced, and to what extent their perception is responsible for the multiple physiological roles associated with MIK2 are currently unclear. Using N-terminomics, we validate the N-terminal cleavage site of representative PROSCOOPs. The cleavage sites are determined by conserved motifs upstream of the minimal SCOOP bioactive epitope. We identified subtilases necessary and sufficient to process PROSCOOP peptides at conserved cleavage motifs. Mutation of these subtilases, or their recognition motifs, suppressed PROSCOOP cleavage and associated overexpression phenotypes. Furthermore, we show that higher-order mutants of these subtilases show phenotypes reminiscent of mik2 null mutant plants, consistent with impaired PROSCOOP biogenesis, and demonstrating biological relevance of SCOOP perception by MIK2. Together, this work provides insights into the molecular mechanisms underlying the functions of the recently identified SCOOP peptides and their receptor MIK2.

Item Type: Article
Additional Information: Data availability statement: The authors declare that the data supporting the findings of this study are available within the manuscript and its supplementary files. Source data are provided with this paper. Funding Information: Gatsby Charitable Foundation (C.Z.), the Biotechnology and Biological Research Council (BB/P012574/1) (C.Z.), the European Research Council under the European Union’s Horizon 2020 research and innovation programme no. 773153 (project ‘IMMUNO-PEPTALK’) (C.Z.) and programme no. 724321 (project ‘Sense2SurviveSalt’) (C.T.), the University of Zurich (C.Z.) and the Swiss National Science Foundation grants no. 31003A_182625 (C.Z.) and 310030_184769 (C.S.R.).
Uncontrolled Keywords: plant science ,/dk/atira/pure/subjectarea/asjc/1100/1110
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
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Depositing User: LivePure Connector
Date Deposited: 03 Dec 2024 01:35
Last Modified: 03 Dec 2024 01:35
URI: https://ueaeprints.uea.ac.uk/id/eprint/97865
DOI: 10.1038/s41477-023-01583-x

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