Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity

Liu, Lijing; Sonbol, F.M.; Huot, Bethany; Gu, Yangnan; Withers, John; Mwimba, Musoki; Yao, Jian; He, Sheng Yang; Dong, Xinnian

doi:10.1038/ncomms13099

Cited by 293 publications

(251 citation statements)

References 58 publications

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“…Our experiments do not rule out the possibility that ETI also affects COR production in the bacterial cell and/or COR delivery into the plant cell. Recently, Liu et al reported that expression of some JA-responsive genes is activated during ETI (42). The discrepancy between our and their studies could be explained by selective activation or repression of JA-responsive genes during ETI.…”

Section: Discussioncontrasting

confidence: 55%

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.

114

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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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Section: Discussioncontrasting

confidence: 55%

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.

114

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“…There are, however, many complexities with regard to the antagonism of JA and SA in A. thaliana [145]. Liu et al [145] showed that SA promotes the synthesis of JA and the activation of its signaling during ETI.…”

Section: Evolution Of Phytohormone Defense Networkmentioning

confidence: 99%

“…Liu et al [145] showed that SA promotes the synthesis of JA and the activation of its signaling during ETI. However, a recent study by Betsuyaku et al [146] showed that SA and JA act antagonistically during ETI on a narrow spatial scale.…”

Section: Evolution Of Phytohormone Defense Networkmentioning

confidence: 99%

On plant defense signaling networks and early land plant evolution

Vries

Dahlen

Gould

et al. 2018

Communicative & Integrative Biology

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All land plants must cope with phytopathogens. Algae face pathogens, too, and it is reasonable to assume that some of the strategies for dealing with pathogens evolved prior to the origin of embryophytes – plant terrestrialization simply changed the nature of the plant-pathogen interactions. Here we highlight that many potential components of the angiosperm defense toolkit are i) found in streptophyte algae and non-flowering embryophytes and ii) might be used in non-flowering plant defense as inferred from published experimental data. Nonetheless, the common signaling networks governing these defense responses appear to have become more intricate during embryophyte evolution. This includes the evolution of the antagonistic signaling pathways of jasmonic and salicylic acid, multiple independent expansions of resistance genes, and the evolution of resistance gene-regulating microRNAs. Future comparative studies will illuminate which modules of the streptophyte defense signaling network constitute the core and which constitute lineage- and/or environment-specific (peripheral) signaling circuits.

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“…Whether extracellular ATP can stimulate the activity of AtJAT1/AtABCG16 remains to be determined. Liu et al (2016) demonstrated a noncanonical pathway at the early stage of ETI in which the activation of JA signaling is mediated through direct degradation of JAZs by SA receptors, NPR3 and NPR4, in a COI1-independent manner. As it was attenuated in a sid2 mutant, SA is a necessary signal for the activation of JA signaling in this noncanonical pathway.…”

Section: Discussionmentioning

confidence: 99%

Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

et al. 2017

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Damaged cells send various signals to stimulate defense responses. Recent identification and genetic studies of the plant purinoceptor, P2K1 (also known as DORN1), have demonstrated that extracellular ATP is a signal involved in plant stress responses, including wounding, perhaps to evoke plant defense. However, it remains largely unknown how extracellular ATP induces plant defense responses. Here, we demonstrate that extracellular ATP induces plant defense mediated through activation of the intracellular signaling of jasmonate (JA), a well-characterized defense hormone. In Arabidopsis (Arabidopsis thaliana) leaves, ATP pretreatment induced resistance against the necrotrophic fungus, Botrytis cinerea. The induced resistance was enhanced in the P2K1 receptor overexpression line, but reduced in the receptor mutant, dorn1-3. Mining the transcriptome data revealed that ATP induces a set of JA-induced genes. In addition, the P2K1-associated coexpression network contains defense-related genes, including those encoding jasmonate ZIM-domain (JAZ) proteins, which play key roles as repressors of JA signaling. We examined whether extracellular ATP impacts the stability of JAZ1 in Arabidopsis. The results showed that the JAZ1 stability decreased in response to ATP addition in a proteasome-dependent manner. This reduction required intracellular signaling via second messengers-cytosolic calcium, reactive oxygen species, and nitric oxide. Interestingly, the ATP-induced JAZ1 degradation was attenuated in the JA receptor mutant, coi1, but not in the JA biosynthesis mutant, aos, or upon addition of JA biosynthesis inhibitors. Immunoprecipitation analysis demonstrated that ATP increases the interaction between COI1 and JAZ1, suggesting direct cross talk between extracellular ATP and JA in intracellular signaling events. Taken together, these results suggest that extracellular ATP signaling directly impacts the JA signaling pathway to maximize plant defense responses.

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Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity

Cited by 293 publications

References 58 publications

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

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

On plant defense signaling networks and early land plant evolution

Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

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