A MPK3/6-WRKY33-ALD1-Pipecolic Acid Regulatory Loop Contributes to Systemic Acquired Resistance

Wang, Yiming; Schuck, Stefan; Wu, Jingni; Yang, Ping; Döring, Anne-Christin; Zeier, Jürgen; Tsuda, Kazuhiko

doi:10.1105/tpc.18.00547

Cited by 129 publications

(100 citation statements)

References 74 publications

(135 reference statements)

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“…We propose two main hypotheses to explain this phenomenon: (a) fungal signals influence plant responses to SA or (b) SA accumulation in ECM occurs in fungal hyphae and SA is not perceived by poplar cells. SA treatment of colonized LRs triggers the regulation of genes putatively involved in systemic defense (Data S9; Zhang et al, ; Wang et al, ; Guerra, Schilling, Sylvester, Conrads, & Romeis, ), suggesting that L. bicolor cannot suppress poplar responses to exogenous SA. However, we cannot exclude the possibility that fungal MiSSPs target endogenous SA signalling in poplar, similar to JA signalling (Plett et al, ).…”

Section: Discussionmentioning

confidence: 99%

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

Basso

Kohler

Miyauchi

et al. 2020

Plant Cell & Environment

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The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. Here, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography–tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone‐treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid‐stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.

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Section: Discussionmentioning

confidence: 99%

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

Basso

Kohler

Miyauchi

et al. 2020

Plant Cell & Environment

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“…a), they have previously shown to be targeted by SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN‐BINDING PROTEIN 60g (CBP60g) (Sun et al , ). A recent study just revealed that WRKY33 binds to the ALD1 promoter and positively regulates Pip accumulation (Y. Wang et al , ). Together, these findings imply that a regulatory connection between several known transcription factors, H3K4me3 histone marks and levels for defence gene expression.…”

Section: Discussionmentioning

confidence: 99%

JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels

Liu

Singh

et al. 2019

New Phytologist

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Summary Epigenetic modifications have emerged as an important mechanism underlying plant defence against pathogens. We examined the role of JMJ14, a Jumonji (JMJ) domain‐containing H3K4 demethylase, in local and systemic plant immune responses in Arabidopsis. The function of JMJ14 in local or systemic defence response was investigated by pathogen growth assays and by analysing expression and H3K4me3 enrichments of key defence genes using qPCR and ChIP‐qPCR. Salicylic acid (SA) and pipecolic acid (Pip) levels were quantified and function of JMJ14 in SA‐ and Pip‐mediated defences was analysed in Col‐0 and jmj14 plants. jmj14 mutants were compromised in both local and systemic defences. JMJ14 positively regulates pathogen‐induced H3K4me3 enrichment and expression of defence genes involved in SA‐ and Pip‐mediated defence pathways. Consequently, loss of JMJ14 results in attenuated defence gene expression and reduced Pip accumulation during establishment of systemic acquired resistance (SAR). Exogenous Pip partially restored SAR in jmj14 plants, suggesting that JMJ14 regulated Pip biosynthesis and other downstream factors regulate SAR in jmj14 plants. JMJ14 positively modulates defence gene expressions and Pip levels in Arabidopsis.

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“…Consistently, priming responses were compromised or lost in mutant lines of mpk3 and mpk6 (Beckers et al, 2009). MPK3 and MPK6 were shown to contribute to SAR via an ALD1-Pip regulatory loop (Wang et al, 2018b). Furthermore, an interplay between MPK and CPK signaling has been demonstrated for innate immune signaling in PTI (Boudsocq et al, 2010), where exemplary defense gene activation was shown to be either MPK-specific or CPK-specific, or to be controlled through joint MPK and CPK signaling.…”

Section: Cpk5 Protein Amount and Catalytic Activity Contribute To Thementioning

confidence: 98%

Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐l‐pipecolic acid‐ and SARD1‐dependent immune memory in systemic acquired resistance

et al. 2019

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Summary Systemic acquired resistance (SAR) prepares infected plants for faster and stronger defense activation upon subsequent attacks. SAR requires an information relay from primary infection to distal tissue and the initiation and maintenance of a self‐maintaining phytohormone salicylic acid (SA)‐defense loop. In spatial and temporal resolution, we show that calcium‐dependent protein kinase CPK5 contributes to immunity and SAR. In local basal resistance, CPK5 functions upstream of SA synthesis, perception, and signaling. In systemic tissue, CPK5 signaling leads to accumulation of SAR‐inducing metabolite N‐hydroxy‐L‐pipecolic acid (NHP) and SAR marker genes, including Systemic Acquired Resistance Deficient 1 (SARD1) Plants of increased CPK5, but not CPK6, signaling display an ‘enhanced SAR’ phenotype towards a secondary bacterial infection. In the sard1‐1 background, CPK5‐mediated basal resistance is still mounted, but NHP concentration is reduced and enhanced SAR is lost. The biochemical analysis estimated CPK5 half maximal kinase activity for calcium, K50 [Ca2+], to be c. 100 nM, close to the cytoplasmic resting level. This low threshold uniquely qualifies CPK5 to decode subtle changes in calcium, a prerequisite to signal relay and onset and maintenance of priming at later time points in distal tissue. Our data explain why CPK5 functions as a hub in basal and systemic plant immunity.

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A MPK3/6-WRKY33-ALD1-Pipecolic Acid Regulatory Loop Contributes to Systemic Acquired Resistance

Cited by 129 publications

References 74 publications

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels

Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐l‐pipecolic acid‐ and SARD1‐dependent immune memory in systemic acquired resistance

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