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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 triggers the degradation of AtJAZ1 during bacterial infection.(A) HopZ1a, but not AvrRpt2, promotes the degradation of AtJAZ1 in the Arabidopsis ecotype Col-0 (wild-type) during bacterial infection. Six-week 35S-HA-AtJAZ1Arabidopsis transgenic plants were infiltrated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a, HopZ1a(C216A) or AvrRpt2. (B) HopZ1a promotes the degradation of AtJAZ1 in zar1-1 Arabidopsis plants. Six week-old 35S-HA-AtJAZ1 zar1-1 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). (C) HopZ1a-mediated degradation of AtJAZ1 is dependent on COI1. 35S-HA-AtJAZ1, coi1-30 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). Bacterial infection assays were conducted using inoculums at OD600 = 0.2 (approximately 2×108 cfu/mL). The abundance of AtJAZ1 was determined by western blots using anti-HA antibody at 6 hpi. The protein gels were stained with Coomassie blue as loading controls. These experiments were repeated three times with similar results.
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ppat-1003715-g005: HopZ1a triggers the degradation of AtJAZ1 during bacterial infection.(A) HopZ1a, but not AvrRpt2, promotes the degradation of AtJAZ1 in the Arabidopsis ecotype Col-0 (wild-type) during bacterial infection. Six-week 35S-HA-AtJAZ1Arabidopsis transgenic plants were infiltrated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a, HopZ1a(C216A) or AvrRpt2. (B) HopZ1a promotes the degradation of AtJAZ1 in zar1-1 Arabidopsis plants. Six week-old 35S-HA-AtJAZ1 zar1-1 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). (C) HopZ1a-mediated degradation of AtJAZ1 is dependent on COI1. 35S-HA-AtJAZ1, coi1-30 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). Bacterial infection assays were conducted using inoculums at OD600 = 0.2 (approximately 2×108 cfu/mL). The abundance of AtJAZ1 was determined by western blots using anti-HA antibody at 6 hpi. The protein gels were stained with Coomassie blue as loading controls. These experiments were repeated three times with similar results.

Mentions: Although we observed the degradation of GmJAZ1 and AtJAZ6 when they were co-expressed with HopZ1a in N. benthamiana, it is important to examine whether HopZ1a can promote JAZ degradation during bacterial infection. For this purpose, we inoculated transgenic Arabidopsis plants expressing 35S-HA-AtJAZ1 with P. syringae producing HopZ1a or HopZ1a(C216A). The Arabidopsis pathogen Pseudomonas syringae pv. tomato strain DC3000 (PtoDC3000) is well-known to induce AtJAZ degradation through the production of coronatine, which acts as a JA mimic [22]. The mutant PtoDC3118 is deficient in coronatine production and therefore no longer degrades JAZs [29]. Importantly, PtoDC3118 expressing HopZ1a from its native promoter also significantly reduced the abundance of AtJAZ1 at 6 hpi (Fig. 5A). The level of AtJAZ1 remained unchanged in tissues infiltrated with PtoDC3118 carrying the empty vector or expressing the catalytic mutant HopZ1a(C216A). These data strongly suggest that HopZ1a can induce AtJAZ1 degradation during bacterial infection.


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 triggers the degradation of AtJAZ1 during bacterial infection.(A) HopZ1a, but not AvrRpt2, promotes the degradation of AtJAZ1 in the Arabidopsis ecotype Col-0 (wild-type) during bacterial infection. Six-week 35S-HA-AtJAZ1Arabidopsis transgenic plants were infiltrated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a, HopZ1a(C216A) or AvrRpt2. (B) HopZ1a promotes the degradation of AtJAZ1 in zar1-1 Arabidopsis plants. Six week-old 35S-HA-AtJAZ1 zar1-1 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). (C) HopZ1a-mediated degradation of AtJAZ1 is dependent on COI1. 35S-HA-AtJAZ1, coi1-30 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). Bacterial infection assays were conducted using inoculums at OD600 = 0.2 (approximately 2×108 cfu/mL). The abundance of AtJAZ1 was determined by western blots using anti-HA antibody at 6 hpi. The protein gels were stained with Coomassie blue as loading controls. These experiments were repeated three times with similar results.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3814404&req=5

ppat-1003715-g005: HopZ1a triggers the degradation of AtJAZ1 during bacterial infection.(A) HopZ1a, but not AvrRpt2, promotes the degradation of AtJAZ1 in the Arabidopsis ecotype Col-0 (wild-type) during bacterial infection. Six-week 35S-HA-AtJAZ1Arabidopsis transgenic plants were infiltrated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a, HopZ1a(C216A) or AvrRpt2. (B) HopZ1a promotes the degradation of AtJAZ1 in zar1-1 Arabidopsis plants. Six week-old 35S-HA-AtJAZ1 zar1-1 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). (C) HopZ1a-mediated degradation of AtJAZ1 is dependent on COI1. 35S-HA-AtJAZ1, coi1-30 Arabidopsis plants were inoculated with PtoDC3000, PtoDC3118 carrying the empty pUCP18 vector (EV), or PtoDC3118 expressing HopZ1a or HopZ1a(C216A). Bacterial infection assays were conducted using inoculums at OD600 = 0.2 (approximately 2×108 cfu/mL). The abundance of AtJAZ1 was determined by western blots using anti-HA antibody at 6 hpi. The protein gels were stained with Coomassie blue as loading controls. These experiments were repeated three times with similar results.
Mentions: Although we observed the degradation of GmJAZ1 and AtJAZ6 when they were co-expressed with HopZ1a in N. benthamiana, it is important to examine whether HopZ1a can promote JAZ degradation during bacterial infection. For this purpose, we inoculated transgenic Arabidopsis plants expressing 35S-HA-AtJAZ1 with P. syringae producing HopZ1a or HopZ1a(C216A). The Arabidopsis pathogen Pseudomonas syringae pv. tomato strain DC3000 (PtoDC3000) is well-known to induce AtJAZ degradation through the production of coronatine, which acts as a JA mimic [22]. The mutant PtoDC3118 is deficient in coronatine production and therefore no longer degrades JAZs [29]. Importantly, PtoDC3118 expressing HopZ1a from its native promoter also significantly reduced the abundance of AtJAZ1 at 6 hpi (Fig. 5A). The level of AtJAZ1 remained unchanged in tissues infiltrated with PtoDC3118 carrying the empty vector or expressing the catalytic mutant HopZ1a(C216A). These data strongly suggest that HopZ1a can induce AtJAZ1 degradation during bacterial infection.

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