Cutting the line: manipulation of plant immunity by bacterial type III effector proteases

Abstract

Pathogens and their hosts are engaged in an evolutionary arms race. Pathogen-derived effectors promote virulence by targeting components of a host’s innate immune system, while hosts have evolved proteins that sense effectors and trigger a pathogen-specific immune response. Many bacterial effectors are translocated into host cells using type III secretion systems. Type III effector proteases irreversibly modify host proteins by cleavage of peptide bonds and are prevalent among both plant and animal bacterial pathogens. In plants, the study of model effector proteases has yielded important insights into the virulence mechanisms employed by pathogens to overcome their host’s immune response, as well as into the mechanisms deployed by their hosts to detect these effector proteases and counteract their effects. In recent years, the study of a larger number of effector proteases, across a wider range of pathogens, has yielded novel insights into their functions and recognition. One key limitation has remained the lack of methods to detect protease cleavage at the proteome-wide level. We review known substrates and mechanisms of plant pathogen type III effector proteases, compare their functions to those of known type III effector proteases of mammalian pathogens. Finally, we discuss approaches to uncover their function on a system-wide level.

Host manipulation by bacterial type III and type IV secretion system effector proteases

“…Pathogens disable PTI using effectors, but resistance (R) proteins guard this and activate ETI (Yuan, Ngou, Ding, & Xin, 2021). T3SS effector proteases are a major component of the virulence factor arsenal of phytopathogens and were reviewed recently (Figaj, Ambroziak, Przepiora, & Skorko-Glonek, 2019;Mooney, Mantz, Graciet, & Huesgen, 2021).…”

“…Given the central role of RIN4, it is not surprising that several ETI mechanisms detect the action of AvrRpt2 (Mooney et al, 2021).…”

“…Plant hormones beyond auxins, for example, salicylic acid (SA) and jasmonate (JA), are important PTI signals, and their modulation is a widely employed strategy of phytopathogens. Peptidase C103 effectors HopX1 (AvrPphE) and RipE1 degrade JAZ proteins, repressors of the JA pathway, resulting in suppression of SA-induced defences, facilitating bacterial entry and replication; however, HopX1 is also counteracted by ETI in some plants (Gimenez-Ibanez et al, 2014;Mooney et al, 2021;Nakano & Mukaihara, 2019;Z. L. Nimchuk, Fisher, Desveaux, Chang, & Dangl, 2007).…”

“…Phytopathogens, like animal pathogens, also harbour a large arsenal of CE clan proteases effectors, which are often DUBs removing ubiquitin and/or ubiquitin-like modifiers, for example, XopD and AvrXv4. However, in particular, members of the peptidase C55 subfamily, for example, Pseudomonas HopZ1 and Yersinia effector YopJ, additionally or exclusively, can have acetyltransferase activity (Mooney et al, 2021;Pruneda et al, 2016). Notably, C55 peptidases Figaj, D., Ambroziak, P., Przepiora, T., & Skorko-Glonek, J.…”

Expression of putative effectors of different Xylella fastidiosa strains triggers cell death‐like responses in various Nicotiana model plants

“…In order to meet their nutritional needs and proliferate effectively inside the host, several pathogens have evolved to secrete virulence factors—known as effectors—directly into the host cell cytoplasm or into the extremely hostile apoplastic space (Mooney et al, 2021 ). Effector proteins are key aspects of plant–pathogen interactions, potentially controlling the host range through their recognition by the plant surveillance system (Büttner & Bonas, 2010 ; Reddy et al, 2019 ).…”