Extracellular proteolytic cascade in tomato activates immune protease Rcr3

Paulus, Judith K, Kourelis, Jiorgos ORCID: https://orcid.org/0000-0002-9007-1333, Ramasubramanian, Selva, Homma, Felix, Godson, Alice, Hörger, Anja C, Hong, Tram Ngoc, Krahn, Daniel, Ossorio Carballo, Laura, Wang, Shuaishuai, Win, Joe, Smoker, Matthew, Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315, Dong, Suomeng and van der Hoorn, Renier A L (2020) Extracellular proteolytic cascade in tomato activates immune protease Rcr3. Proceedings of the National Academy of Sciences of the United States of America, 117 (29). pp. 17409-17417. ISSN 1091-6490

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Abstract

Proteolytic cascades regulate immunity and development in animals, but these cascades in plants have not yet been reported. Here we report that the extracellular immune protease Rcr3 of tomato is activated by P69B and other subtilases (SBTs), revealing a proteolytic cascade regulating extracellular immunity in solanaceous plants. Rcr3 is a secreted papain-like Cys protease (PLCP) of tomato that acts both in basal resistance against late blight disease (Phytophthora infestans) and in gene-for-gene resistance against the fungal pathogen Cladosporium fulvum (syn. Passalora fulva) Despite the prevalent model that Rcr3-like proteases can activate themselves at low pH, we found that catalytically inactive proRcr3 mutant precursors are still processed into mature mRcr3 isoforms. ProRcr3 is processed by secreted P69B and other Asp-selective SBTs in solanaceous plants, providing robust immunity through SBT redundancy. The apoplastic effector EPI1 of P. infestans can block Rcr3 activation by inhibiting SBTs, suggesting that this effector promotes virulence indirectly by preventing the activation of Rcr3(-like) immune proteases. Rcr3 activation in Nicotiana benthamiana requires a SBT from a different subfamily, indicating that extracellular proteolytic cascades have evolved convergently in solanaceous plants or are very ancient in the plant kingdom. The frequent incidence of Asp residues in the cleavage region of Rcr3-like proteases in solanaceous plants indicates that activation of immune proteases by SBTs is a general mechanism, illuminating a proteolytic cascade that provides robust apoplastic immunity.

Item Type:	Article
Additional Information:	Copyright © 2020 the Author(s). Published by PNAS.
Faculty \ School:	Faculty of Science > The Sainsbury Laboratory
UEA Research Groups:	Faculty of Science > Research Groups > Plant Sciences
Depositing User:	LivePure Connector
Date Deposited:	13 Aug 2020 23:59
Last Modified:	31 Jan 2024 02:42
URI:	https://ueaeprints.uea.ac.uk/id/eprint/76439
DOI:	10.1073/pnas.1921101117

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