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Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors.

Jiang S, Yao J, Ma KW, Zhou H, Song J, He SY, Ma W - PLoS Pathog. (2013)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, California, United States of America ; Center for Plant Cell Biology, University of California, Riverside, California, United States of America.

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.

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HopZ1a activates JA signaling during bacterial infection.Arabidopsis zar1-1 mutant plants were inoculated with PtoDC3000 or PtoDC3118 carrying the empty pUCP18 vector (EV), HopZ1a or HopZ1a(C216A). The transcript levels of the JA-responsive genes AtJAZ9 and AtJAZ10, as well as the SA biosynthetic gene AtICS1 were determined by quantitative RT-PCR. (A) HopZ1a induces the expression of JA-responsive genes in Arabidopsis. The abundances of AtJAZ9 and AtJAZ10 transcripts were examined at 6 hpi using AtActin as the internal standard. Relative expression levels were determined by comparing the normalized AtJAZ9 or AtJAZ10 transcripts between infected and mock-treated (leaves infiltrated with 10 mM MgSO4) samples. (B) HopZ1a reduces the expression of AtICS1 in Arabidopsis. AtICS1 transcript level was analyzed at 9 hpi using AtUBQ5 as the internal standard. Values are means ± standard deviations (as error bars) (n = 5). All experiments were repeated at least five times with similar results. The expression of HopZ1a in P. syringae was confirmed by western blots (Fig. S8).
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ppat-1003715-g006: HopZ1a activates JA signaling during bacterial infection.Arabidopsis zar1-1 mutant plants were inoculated with PtoDC3000 or PtoDC3118 carrying the empty pUCP18 vector (EV), HopZ1a or HopZ1a(C216A). The transcript levels of the JA-responsive genes AtJAZ9 and AtJAZ10, as well as the SA biosynthetic gene AtICS1 were determined by quantitative RT-PCR. (A) HopZ1a induces the expression of JA-responsive genes in Arabidopsis. The abundances of AtJAZ9 and AtJAZ10 transcripts were examined at 6 hpi using AtActin as the internal standard. Relative expression levels were determined by comparing the normalized AtJAZ9 or AtJAZ10 transcripts between infected and mock-treated (leaves infiltrated with 10 mM MgSO4) samples. (B) HopZ1a reduces the expression of AtICS1 in Arabidopsis. AtICS1 transcript level was analyzed at 9 hpi using AtUBQ5 as the internal standard. Values are means ± standard deviations (as error bars) (n = 5). All experiments were repeated at least five times with similar results. The expression of HopZ1a in P. syringae was confirmed by western blots (Fig. S8).

Mentions: In Arabidopsis, JAZ proteins are repressors of JA transcription factors (e.g. AtMYC2) that are involved in the expression of JA-responsive genes [32], [33], [34]. Since HopZ1a induces the degradation of AtJAZ1, we examined whether it could induce the expression of JA-responsive genes during bacterial infection. Real-time RT-PCR was carried out to determine the transcript levels of JA-responsive genes in Arabidopsis. Five-week old zar1-1 plants were inoculated with PtoDC3118 expressing HopZ1a or HopZ1a(C216A) at OD600 = 0.2 (approximately 2×108 cfu/mL). The transcript levels of two early JA-responsive genes, AtJAZ9 and AtJAZ10[34], were analyzed at 6 hpi. Both genes were induced approximately ten fold in plants infected by PtoDC3118(HopZ1a), whereas their expression was not changed in tissues infected by PtoDC3118 expressing HopZ1a(C216A) (Fig. 6A). The level of gene induction by HopZ1a was lower than that by coronatine, as shown by the approximately 40-fold induction of AtJAZ9 and AtJAZ10 in plants infected with PtoDC3000. This is consistent with the partial vs. complete degradation of AtJAZ1 by HopZ1a or coronatine during bacterial infection. Nonetheless, these experiments suggest that bacterium-delivered HopZ1a can activate JA signaling.


Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors.

Jiang S, Yao J, Ma KW, Zhou H, Song J, He SY, Ma W - PLoS Pathog. (2013)

HopZ1a activates JA signaling during bacterial infection.Arabidopsis zar1-1 mutant plants were inoculated with PtoDC3000 or PtoDC3118 carrying the empty pUCP18 vector (EV), HopZ1a or HopZ1a(C216A). The transcript levels of the JA-responsive genes AtJAZ9 and AtJAZ10, as well as the SA biosynthetic gene AtICS1 were determined by quantitative RT-PCR. (A) HopZ1a induces the expression of JA-responsive genes in Arabidopsis. The abundances of AtJAZ9 and AtJAZ10 transcripts were examined at 6 hpi using AtActin as the internal standard. Relative expression levels were determined by comparing the normalized AtJAZ9 or AtJAZ10 transcripts between infected and mock-treated (leaves infiltrated with 10 mM MgSO4) samples. (B) HopZ1a reduces the expression of AtICS1 in Arabidopsis. AtICS1 transcript level was analyzed at 9 hpi using AtUBQ5 as the internal standard. Values are means ± standard deviations (as error bars) (n = 5). All experiments were repeated at least five times with similar results. The expression of HopZ1a in P. syringae was confirmed by western blots (Fig. S8).
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ppat-1003715-g006: HopZ1a activates JA signaling during bacterial infection.Arabidopsis zar1-1 mutant plants were inoculated with PtoDC3000 or PtoDC3118 carrying the empty pUCP18 vector (EV), HopZ1a or HopZ1a(C216A). The transcript levels of the JA-responsive genes AtJAZ9 and AtJAZ10, as well as the SA biosynthetic gene AtICS1 were determined by quantitative RT-PCR. (A) HopZ1a induces the expression of JA-responsive genes in Arabidopsis. The abundances of AtJAZ9 and AtJAZ10 transcripts were examined at 6 hpi using AtActin as the internal standard. Relative expression levels were determined by comparing the normalized AtJAZ9 or AtJAZ10 transcripts between infected and mock-treated (leaves infiltrated with 10 mM MgSO4) samples. (B) HopZ1a reduces the expression of AtICS1 in Arabidopsis. AtICS1 transcript level was analyzed at 9 hpi using AtUBQ5 as the internal standard. Values are means ± standard deviations (as error bars) (n = 5). All experiments were repeated at least five times with similar results. The expression of HopZ1a in P. syringae was confirmed by western blots (Fig. S8).
Mentions: In Arabidopsis, JAZ proteins are repressors of JA transcription factors (e.g. AtMYC2) that are involved in the expression of JA-responsive genes [32], [33], [34]. Since HopZ1a induces the degradation of AtJAZ1, we examined whether it could induce the expression of JA-responsive genes during bacterial infection. Real-time RT-PCR was carried out to determine the transcript levels of JA-responsive genes in Arabidopsis. Five-week old zar1-1 plants were inoculated with PtoDC3118 expressing HopZ1a or HopZ1a(C216A) at OD600 = 0.2 (approximately 2×108 cfu/mL). The transcript levels of two early JA-responsive genes, AtJAZ9 and AtJAZ10[34], were analyzed at 6 hpi. Both genes were induced approximately ten fold in plants infected by PtoDC3118(HopZ1a), whereas their expression was not changed in tissues infected by PtoDC3118 expressing HopZ1a(C216A) (Fig. 6A). The level of gene induction by HopZ1a was lower than that by coronatine, as shown by the approximately 40-fold induction of AtJAZ9 and AtJAZ10 in plants infected with PtoDC3000. This is consistent with the partial vs. complete degradation of AtJAZ1 by HopZ1a or coronatine during bacterial infection. Nonetheless, these experiments suggest that bacterium-delivered HopZ1a can activate JA signaling.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, California, United States of America ; Center for Plant Cell Biology, University of California, Riverside, California, United States of America.

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.

Show MeSH
Related in: MedlinePlus