The Bacterial Effector HopX1 Targets JAZ Transcriptional Repressors to Activate Jasmonate Signaling and Promote Infection in Arabidopsis

Giménez-Ibáñez, Selena; Botër, Marta; Fernández-Barbero, Gemma; Chini, Andrea; Rathjen, John P.; Solano, Roberto

doi:10.1371/journal.pbio.1001792

Cited by 224 publications

(223 citation statements)

References 71 publications

Supporting

Mentioning

221

Contrasting

Order By: Relevance

“…Another bacterial effector, HopX1 from P. syringae pv tabaci, degrades JAZs and thus promotes virulence by inhibiting SA defenses through activation of the JA pathway (Gimenez-Ibanez et al, 2014). Relatively little information is available on the molecular mechanisms of JA/SA cross talk, but it was recently found that COR induces the expression of NAC transcriptions factors that inhibit SA biosynthesis .…”

mentioning

confidence: 99%

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

et al. 2016

View full text Add to dashboard Cite

Arabidopsis (Arabidopsis thaliana) plants recognize insect eggs and activate the salicylic acid (SA) pathway. As a consequence, expression of defense genes regulated by the jasmonic acid (JA) pathway is suppressed and larval performance is enhanced. Cross talk between defense signaling pathways is common in plant-pathogen interactions, but the molecular mechanism mediating this phenomenon is poorly understood. Here, we demonstrate that egg-induced SA/JA antagonism works independently of the APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factor ORA59, which controls the ERF branch of the JA pathway. In addition, treatment with egg extract did not enhance expression or stability of JASMONATE ZIM-domain transcriptional repressors, and SA/JA cross talk did not involve JASMONATE ASSOCIATED MYC2-LIKEs, which are negative regulators of the JA pathway. Investigating the stability of MYC2, MYC3, and MYC4, three basic helix-loop-helix transcription factors that additively control jasmonate-related defense responses, we found that egg extract treatment strongly diminished MYC protein levels in an SA-dependent manner. Furthermore, we identified WRKY75 as a novel and essential factor controlling SA/JA cross talk. These data indicate that insect eggs target the MYC branch of the JA pathway and uncover an unexpected modulation of SA/JA antagonism depending on the biological context in which the SA pathway is activated.

show abstract

mentioning

confidence: 99%

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Because pathogenic organisms favor the use of secreted "effector" proteins to subvert host immunity, a great deal of research has focused on the role of pathogenic effectors and how they are used to modify the signaling of defense pathways controlled by plant hormones (10)(11)(12)(20)(21)(22)(23)(24). For example, the pathogenic bacteria Pseudomonas syringae and the oomycete Hyaloperonospora arabidopsidis secrete a number of effectors that target either JAZ proteins (10,11,23) or ethylene signaling (24), whereas Phytophthora infestans produces different effectors that interfere with SA-related signaling (21,22).…”

Section: Significancementioning

confidence: 99%

“…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.…”

mentioning

confidence: 99%

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

Plett

Daguerre

Wittulsky

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

310

285

View full text Add to dashboard Cite

Ectomycorrhizal fungi, such as Laccaria bicolor, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secreted Protein 7) encoded by L. bicolor is necessary for the establishment of symbiosis with host trees, although the mechanistic reasoning behind this role was unknown. We demonstrate here that MiSSP7 interacts with the host protein PtJAZ6, a negative regulator of jasmonic acid (JA)-induced gene regulation in Populus. As with other characterized JASMONATE ZIM-DOMAIN (JAZ) proteins, PtJAZ6 interacts with PtCOI1 in the presence of the JA mimic coronatine, and PtJAZ6 is degraded in plant tissues after JA treatment. The association between MiSSP7 and PtJAZ6 is able to protect PtJAZ6 from this JA-induced degradation. Furthermore, MiSSP7 is able to block-or mitigate-the impact of JA on L. bicolor colonization of host roots. We show that the loss of MiSSP7 production by L. bicolor can be complemented by transgenically varying the transcription of PtJAZ6 or through inhibition of JA-induced gene regulation. We conclude that L. bicolor, in contrast to arbuscular mycorrhizal fungi and biotrophic pathogens, promotes mutualism by blocking JA action through the interaction of MiSSP7 with PtJAZ6.ectomycorrhizal fungus | defense | tree nutrition | host immunity | plant hormone

show abstract

“…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).…”

Section: Introductionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

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

Zhou

Yang

et al. 2015

Plant Cell

View full text Add to dashboard Cite

ORCID IDs: 0000-0003-0202-3890 (C.L.); 0000-0002-9943-2975 (J.-M.Z.) Stomata are natural openings through which many pathogenic bacteria enter plants. Successful bacterial pathogens have evolved various virulence factors to promote stomatal opening. Here, we show that the Pseudomonas syringae type III effector protein AvrB induces stomatal opening and enhances bacterial virulence in a manner dependent on RPM1-INTERACTING4 (RIN4), which promotes stomatal opening by positively regulating the Arabidopsis plasma membrane H + -ATPase (AHA1), which is presumed to directly regulate guard cell turgor pressure. In support of a role of AHA1 in AvrBinduced stomatal opening, AvrB enhances ATPase activity in plants. Unexpectedly, AHA1 promotes the interaction between the jasmonate (JA) receptor CORONATINE INSENSITIVE1 (COI1) and JASMONATE ZIM-DOMAIN (JAZ) proteins and enhances JA signaling. JA signaling is required for optimum stomatal infection in AHA1-active plants. Similarly, AvrB also induces the COI1-JAZ9 interaction and the degradation of multiple JAZ proteins. AvrB-induced stomatal opening and virulence require the canonical JA signaling pathway, which involves the COI1 and NAC transcription factors. The findings thus point to a previously unknown pathway exploited by P. syringae that acts upstream of COI1 to regulate JA signaling and stomatal opening.

show abstract

The Bacterial Effector HopX1 Targets JAZ Transcriptional Repressors to Activate Jasmonate Signaling and Promote Infection in Arabidopsis

Abstract: A bacterial effector protein, HopX1, targets host plant JAZ transcriptional repressors for degradation to activate the jasmonate pathway, thereby promoting bacterial pathogenesis by suppressing host defense responses.

Cited by 224 publications

References 71 publications

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

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

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

Contact Info

Product

Resources

About