The Coronatine Toxin of <i>Pseudomonas syringae</i> Is a Multifunctional Suppressor of <i>Arabidopsis</i> Defense

Geng, Xueqing; Cheng, Jiye; Gangadharan, Anju; Mackey, David

doi:10.1105/tpc.112.105312

Cited by 110 publications

(92 citation statements)

References 60 publications

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“…In addition to promoting stomatal opening and reducing salicylic acid levels (Zheng et al, 2012), coronatine also regulates glucosinolate accumulation and thereby inhibits callose induction by indole glucosinolate breakdown (Geng et al, 2012). Coronatinemediated suppression of innate immune defenses in Arabidopsis roots occurs in a COI1-dependent manner, but does not involve direct interference with salicylic acid signaling (Millet et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation

et al. 2016

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Biosynthesis of the polyamines putrescine, spermidine, and spermine is induced in response to pathogen infection of plants. Putrescine, which is produced from Arg, serves as a metabolic precursor for longer polyamines, including spermidine and spermine. Polyamine acetylation, which has important regulatory functions in mammalian cells, has been observed in several plant species. Here we show that Arabidopsis (Arabidopsis thaliana) N-ACETYLTRANSFERASE ACTIVITY1 (NATA1) catalyzes acetylation of putrescine to N-acetylputrescine and thereby competes with spermidine synthase for a common substrate. NATA1 expression is strongly induced by the plant defense signaling molecule jasmonic acid and coronatine, an effector molecule produced by DC3000, a Pseudomonas syringae strain that initiates a virulent infection in Arabidopsis ecotype Columbia-0. DC3000 growth is reduced in nata1 mutant Arabidopsis, suggesting a role for NATA1-mediated putrescine acetylation in suppressing antimicrobial defenses. During infection by P. syringae and other plant pathogens, polyamine oxidases use spermidine and spermine as substrates for the production of defense-related H 2 O 2 . Compared to wild-type Columbia-0 Arabidopsis, the response of nata1mutants to P. syringae infection includes reduced accumulation of acetylputrescine, greater abundance of nonacetylated polyamines, elevated H 2 O 2 production by polyamine oxidases, and higher expression of genes related to pathogen defense. Together, these results are consistent with a model whereby P. syringae growth is improved in a targeted manner through coronatine-induced putrescine acetylation by NATA1.

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Section: Discussionmentioning

confidence: 99%

Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation

et al. 2016

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“…HopM1 has also been shown to suppress callose deposition via both SA-dependent and -independent mechanisms (Geng et al, 2012). More recently, PR1 induction triggered by the nonhost microorganism P. syringae pv phaseolicola in Arabidopsis has been shown to be suppressed by P. syringae DC3000 HopM1 but independently of SA signaling (Gangadharan et al, 2013).…”

Section: Effectors Targeting Sa Signalingmentioning

confidence: 99%

“…Furthermore, COR could inhibit callose deposition and promote bacterial growth independently of COI1. COR-mediated inhibition of callose biosynthesis seems to occur through suppression of indole glucosinolate biosynthesis via a PENETRATION2-dependent pathway, but precise targets for COR other than COI1 are yet to be determined (Millet et al, 2010;Geng et al, 2012).…”

Section: Bacterial Effectorsmentioning

confidence: 99%

Intervention of Phytohormone Pathways by Pathogen Effectors

2014

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“…For example, various strains of the bacterial pathogen Pseudomonas syringae, including the model strain P. syringae pv. tomato (Pto) DC3000, produce the phytotoxin coronatine (COR) that activates jasmonate (JA) signaling and promotes virulence (7)(8)(9). COR is a structural mimic of the biologically active form of JA, (+)-7-iso-jasmonoyl-L-Ile (JA-Ile).…”

mentioning

confidence: 99%

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

Mine

Berens

Nobori

et al. 2017

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

109

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Phytopathogens promote virulence by, for example, exploiting signaling pathways mediated by phytohormones such as abscisic acid (ABA) and jasmonate (JA). Some plants can counteract pathogen virulence by invoking a potent form of immunity called effector-triggered immunity (ETI). Here, we report that ABA and JA mediate inactivation of the immune-associated MAP kinases (MAPKs), MPK3 and MPK6, in Arabidopsis thaliana. ABA induced expression of genes encoding the protein phosphatases 2C (PP2Cs), HAI1, HAI2, and HAI3 through ABF/AREB transcription factors. These three HAI PP2Cs interacted with MPK3 and MPK6 and were required for ABA-mediated MPK3/MPK6 inactivation and immune suppression. The bacterial pathogen Pseudomonas syringae pv. tomato (Pto) DC3000 activates ABA signaling and produces a JAmimicking phytotoxin, coronatine (COR), that promotes virulence. We found that Pto DC3000 induces HAI1 through COR-mediated activation of MYC2, a master transcription factor in JA signaling. HAI1 dephosphorylated MPK3 and MPK6 in vitro and was necessary for COR-mediated suppression of MPK3/MPK6 activation and immunity. Intriguingly, upon ETI activation, A. thaliana plants overcame the HAI1-dependent virulence of COR by blocking JA signaling. Finally, we showed conservation of induction of HAI PP2Cs by ABA and JA in other Brassicaceae species. Taken together, these results suggest that ABA and JA signaling pathways, which are hijacked by the bacterial pathogen, converge on the HAI PP2Cs that suppress activation of the immune-associated MAPKs. Also, our data unveil interception of JA-signaling activation as a host counterstrategy against the bacterial suppression of MAPKs during ETI.MAPK phosphatase | abscisic acid | jasmonate | coronatine | effector-triggered immunity

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The Coronatine Toxin of Pseudomonas syringae Is a Multifunctional Suppressor of Arabidopsis Defense

Cited by 110 publications

References 60 publications

Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation

Arabidopsis NATA1 acetylates putrescine and decreases defense-related hydrogen peroxide accumulation

Intervention of Phytohormone Pathways by Pathogen Effectors

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

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