Extracellular proteolytic cascade in tomato activates immune protease Rcr3

Autor: Laura Ossorio Carballo, Renier A. L. van der Hoorn, Shuaishuai Wang, Tram Ngoc Hong, Sophien Kamoun, Alice Godson, Matthew Smoker, Joe Win, Jiorgos Kourelis, Felix Homma, Daniel Krahn, Anja C. Hörger, Judith K Paulus, Selva Ramasubramanian, Suomeng Dong
Rok vydání: 2020
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Proceedings of the National Academy of Sciences
ISSN: 1091-6490
0027-8424
Popis: Significance The secretion of papain-like cysteine proteases (PLCPs) is an important component of the immune response across the plant kingdom. Here we show that immune protease Rcr3, a secreted PLCP of tomato, is activated by secreted subtilisins, which are common serine proteases in plants. Subtilase P69B activates proRcr3 by cleaving after aspartates in the junction between the autoinhibitory prodomain and the protease domain of the Rcr3 precursor, thereby activating Rcr3. Subtilases of a different subfamily facilitate proRcr3 processing in a tobacco relative, indicating that this proteolytic cascade might be common in plants. Thus, pathogens that secrete subtilisin inhibitors may indirectly prevent the activation of immune proteases.
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.
Databáze: OpenAIRE