Cleavage of a pathogen apoplastic protein by plant subtilases activates host immunity

Abstract

Summary The plant apoplast is a harsh environment in which hydrolytic enzymes, especially proteases, accumulate during pathogen infection. However, the defense functions of most apoplastic proteases remain largely elusive. We show here that a newly identified small cysteine‐rich secreted protein PC2 from the potato late blight pathogen Phytophthora infestans induces immunity in Solanum plants only after cleavage by plant apoplastic subtilisin‐like proteases, such as tomato P69B. A minimal 61 amino acid core peptide carrying two key cysteines, conserved widely in most oomycete species, is sufficient for PC2‐induced cell death. Furthermore, we showed that Kazal‐like protease inhibitors, such as EPI1, produced by P. infestans prevent PC2 cleavage and dampen PC2 elicited host immunity. This study reveals that cleavage of pathogen proteins to release immunogenic peptides is an important function of plant apoplastic proteases.

Botrytis cinerea BcSSP2 protein is a late infection phase, cytotoxic effector

“…The other two residues might be part of epitopes that contribute to the phytotoxic activity and the mutations might lead to exposure of the immunogenic epitopes, resulting in enhanced activity. A similar study recently revealed that the secreted apoplastic protein PC2 from the potato late blight pathogen Phytophthora infestans was cleavage by plant apoplastic proteases, which is the essential process for PC2 to release the immunogenic peptides, thus to activate plant defence responses (Wang et al ., 2021a). Indeed, several studies demonstrated that heat denaturation or structural mutation of some secreted proteins did not abolish the necrosis‐inducing activity (Zhang et al ., 2014a; Zhang et al ., 2014b), indicating that the potential epitopes are sufficient for the plant cell death‐inducing activity.…”

Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses

“…On the one hand, several secreted fungalysins have been reported to enhance the pathogen invasion by cleaving plant secreted chitinases (Naumann et al, 2011;Jashni et al, 2015a;Sanz-Martín et al, 2016;Ökmen et al, 2018). On the other hand, the host plant can also release proteases to inhibit the growth and invasion of pathogens through direct cleavage of their cell wall protein components or triggering plant defense via cleavage of their secreted effector proteins (Jashni et al, 2015b;Wang et al, 2020Wang et al, , 2021. During the middle and late stages of L. deliciosus-P. taeda EcM development, 81 transcripts coding for secreted proteases accumulated at a much higher level in colonizing L. deliciosus hyphae.…”

Microbe‐derived non‐necrotic glycoside hydrolase family 12 proteins act as immunogenic signatures triggering plant defenses

“…In similar cases, cell death triggered by fungal endopolygalacturonases, the glycoside hydrolase 12 proteins, or elicitins is dependent on the Arabidopsis RLP AtRLP42, N. benthamiana RLP RXEG1, and Solanum microdontum RLP ELR (Zhang et al, 2013; Du et al, 2015; Wang et al, 2018). For many other elicitors, such as P. infestans apoplastic effector PC2, P. sojae effector AEP1, Zymoseptoria tritici effectors Zt9, Zt11, and Zt12 and Ustilaginoidea virens effector SGP1, although the corresponding immune receptors have not yet been identified, cell death activation has been shown to be reliant on membrane‐localized RLK BAK1 and/or SOBIR1 (Kettles et al, 2017; Song et al, 2021; Wang et al, 2021; Xu et al, 2021). One exception is Nep1‐like proteins (NLPs), for which cell death is activated by cytotoxic activity.…”