Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors

Abstract

Gram-negative bacterial pathogens deliver a variety of virulence proteins through the type III secretion system (T3SS) directly into the host cytoplasm. These type III secreted effectors (T3SEs) play an essential role in bacterial infection, mainly by targeting host immunity. However, the molecular basis of their functionalities remains largely enigmatic. Here, we show that the Pseudomonas syringae T3SE HopZ1a, a member of the widely distributed YopJ effector family, directly interacts with jasmonate ZIM-domain (JAZ) proteins through the conserved Jas domain in plant hosts. JAZs are transcription repressors of jasmonate (JA)-responsive genes and major components of the jasmonate receptor complex. Upon interaction, JAZs can be acetylated by HopZ1a through a putative acetyltransferase activity. Importantly, P. syringae producing the wild-type, but not a catalytic mutant of HopZ1a, promotes the degradation of HopZ1-interacting JAZs and activates JA signaling during bacterial infection. Furthermore, HopZ1a could partially rescue the virulence defect of a P. syringae mutant that lacks the production of coronatine, a JA-mimicking phytotoxin produced by a few P. syringae strains. These results highlight a novel example by which a bacterial effector directly manipulates the core regulators of phytohormone signaling to facilitate infection. The targeting of JAZ repressors by both coronatine toxin and HopZ1 effector suggests that the JA receptor complex is potentially a major hub of host targets for bacterial pathogens.

An Arabidopsis Plasma Membrane Proton ATPase Modulates JA Signaling and Is Exploited by the Pseudomonas syringae Effector Protein AvrB for Stomatal Invasion

“…An alternative possibility is that the activation of PM H + -ATPase induces a posttranslational modification of JAZ proteins. For example, degradation of JAZ by the bacterial effector HopZ1a is mediated by acetylation of the JAZ proteins (Jiang et al, 2013). A third, more likely, possibility is that the activation of PM H + -ATPase induces the generation of an unknown signal, which potentiates the COI1-JAZ interaction.…”

“…For the JAZ protein degradation assay in Nicotiana benthamiana, AvrB-FLAG, RIN4, and AHA1-HA were coexpressed individually with JAZ-HA using Agrobacterium tumefaciens-mediated transient expression as previously described (Jiang et al, 2013). Proteins were extracted 24 h after infiltration of Agrobacterium, and the abundance of JAZ proteins was analyzed by immunoblot.…”

“…Syringolin A, which is produced by some P. syringae pv syringae strains, acts as a proteasome inhibitor to open stomata and counteract stomatal innate immunity in bean (Phaseolus vulgaris) and Arabidopsis thaliana plants (Schellenberg et al, 2010). Furthermore, some the P. syringae effector proteins HopZ1a and HopX1 have recently been shown to assist bacterial entry through stomata (Jiang et al, 2013;Gimenez-Ibanez et al, 2014).…”

“…Arabidopsis coi1 mutants do not respond to COR (Xie et al, 1998;Kloek et al, 2001) and do not support COR-induced stomatal opening and virulence (Mittal and Davis, 1995;Melotto et al, 2006). Similarly, HopZ1a acetylates and promotes the degradation of JAZ proteins, whereas HopX1 is a cysteine protease that directly degrades JAZ proteins, resulting in the activation of JA signaling and stomatal opening (Jiang et al, 2013;Gimenez-Ibanez et al, 2014). Recent findings indicate that JA signaling regulates stomatal opening through conserved NAM-ATAF-CUC2 (NAC) transcription factors, including ARABIDOPSIS NACs (ANAC019, ANAC055, and ANAC072) and tomato (Solanum lycopersicum) JA2-LIKE (JA2L) (Zheng et al, 2012;Du et al, 2014).…”

Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes

“…Because JAZ proteins are negative regulators of the JA signaling network, their degradation leads to transcriptional activation of plant defense networks within affected cells (6)(7)(8). Biotrophic pathogens have evolved methods of favoring JA signaling through the use of effector proteins because the outcomes of this hormonal pathway is considered less detrimental to their growth within plant tissues compared with defenses induced by other plant hormones [e.g., salicylic acid (SA)] (9)(10)(11)(12). Not all organisms attempting to colonize plant tissues, however, have adverse affects on plant health.…”