bHLH003, bHLH013 and bHLH017 Are New Targets of JAZ Repressors Negatively Regulating JA Responses

Fonseca, Sandra; Fernández-Calvo, Patricia; Fernández, G.; Díez-Díaz, Mónica; Giménez-Ibáñez, Selena; López‐Vidriero, Irene; Godoy, Marta; Fernández-Barbero, Gemma; Leene, Jelle Van; Jaeger, Geert De; Franco-Zorrilla, José Manuel; Solano, Roberto

doi:10.1371/journal.pone.0086182

Cited by 113 publications

(93 citation statements)

References 62 publications

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“…Notably, we detected the interaction of JAZ12 only with MYC2, MYC3, and MYC4, both in cell cultures and in seedlings, although many other transcription factors have been reported to interact with the JAZ proteins, including JAZ12 (Pauwels and Goossens, 2011;Hu et al, 2013;Nakata et al, 2013;SasakiSekimoto et al, 2013;Song et al, 2013;Fonseca et al, 2014). Similarly, JAZ12 is the only JAZ for which we observed interaction using COI1 as bait.…”

Section: Use Of Tap-mass Spectrometry To Study Ubiquitin E3 Ligasessupporting

confidence: 48%

“…JAZ proteins function as repressors of specific transcription factors in the absence of JA-Ile (Niu et al, 2011;Pauwels and Goossens, 2011;Zhu et al, 2011;Hu et al, 2013;Nakata et al, 2013; Sasaki-Sekimoto et al, 2013; Song et al, 2013;Fonseca et al, 2014). The perception of jasmonates (JAs) thus leads to the derepression of these transcription factors, followed by a rapid reprogramming of gene expression (Pauwels et al, 2008;Attaran et al, 2014).…”

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confidence: 99%

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The RING E3 Ligase KEEP ON GOING Modulates JASMONATE ZIM-DOMAIN12 Stability

et al. 2015

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Jasmonate (JA) signaling in plants is mediated by the JASMONATE ZIM-DOMAIN (JAZ) proteins that repress the activity of several transcription factors regulating JA-inducible gene expression. The hormone JA-isoleucine triggers the interaction of JAZ repressor proteins with the F-box protein CORONATINE INSENSITIVE1 (COI1), part of an S-phase kinase-associated protein1/Cullin1/F-box protein COI1 (SCF COI1 ) E3 ubiquitin ligase complex, and their degradation by the 26S proteasome. In Arabidopsis (Arabidopsis thaliana), the JAZ family consists of 13 members. The level of redundancy or specificity among these members is currently not well understood. Here, we characterized JAZ12, encoded by a highly expressed JAZ gene. JAZ12 interacted with the transcription factors MYC2, MYC3, and MYC4 in vivo and repressed MYC2 activity. Using tandem affinity purification, we found JAZ12 to interact with SCF COI1 components, matching with observed in vivo ubiquitination and with rapid degradation after treatment with JA. In contrast to the other JAZ proteins, JAZ12 also interacted directly with the E3 RING ligase KEEP ON GOING (KEG), a known repressor of the ABSCISIC ACID INSENSITIVE5 transcription factor in abscisic acid signaling. To study the functional role of this interaction, we circumvented the lethality of keg loss-of-function mutants by silencing KEG using an artificial microRNA approach. Abscisic acid treatment promoted JAZ12 degradation, and KEG knockdown led to a decrease in JAZ12 protein levels. Correspondingly, KEG overexpression was capable of partially inhibiting COI1-mediated JAZ12 degradation. Our results provide additional evidence for KEG as an important factor in plant hormone signaling and a positive regulator of JAZ12 stability.

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Section: Use Of Tap-mass Spectrometry To Study Ubiquitin E3 Ligasessupporting

confidence: 48%

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confidence: 99%

The RING E3 Ligase KEEP ON GOING Modulates JASMONATE ZIM-DOMAIN12 Stability

et al. 2015

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“…bHLH3, bHLH13, bLHL14, and bHLH17 are repressors that bind to cis-regulatory elements of MYC target genes and inhibit transcription (Fonseca et al, 2014;Song et al, 2013;Sasaki-Sekimoto et al, 2013). We tested whether these factors could participate in the suppression of JA responses mediated by egginduced SA.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

et al. 2016

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Arabidopsis (Arabidopsis thaliana) plants recognize insect eggs and activate the salicylic acid (SA) pathway. As a consequence, expression of defense genes regulated by the jasmonic acid (JA) pathway is suppressed and larval performance is enhanced. Cross talk between defense signaling pathways is common in plant-pathogen interactions, but the molecular mechanism mediating this phenomenon is poorly understood. Here, we demonstrate that egg-induced SA/JA antagonism works independently of the APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factor ORA59, which controls the ERF branch of the JA pathway. In addition, treatment with egg extract did not enhance expression or stability of JASMONATE ZIM-domain transcriptional repressors, and SA/JA cross talk did not involve JASMONATE ASSOCIATED MYC2-LIKEs, which are negative regulators of the JA pathway. Investigating the stability of MYC2, MYC3, and MYC4, three basic helix-loop-helix transcription factors that additively control jasmonate-related defense responses, we found that egg extract treatment strongly diminished MYC protein levels in an SA-dependent manner. Furthermore, we identified WRKY75 as a novel and essential factor controlling SA/JA cross talk. These data indicate that insect eggs target the MYC branch of the JA pathway and uncover an unexpected modulation of SA/JA antagonism depending on the biological context in which the SA pathway is activated.

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“…Thus, the bHLH-mediated release of MYBs from inhibition will be followed by the MYB-mediated activation of GSL biosynthesis genes. Interestingly, several independent research groups have recently demonstrated that the bHLH subgroup IIId TFs (bHLH03, bHLH13, bHLH14, and bHLH17) are targets of JAZ proteins and therefore inhibitors of JA signaling, which can indeed serve as antagonists of the bHLH subgroup IIIe (bHLH04, bHLH05, and bHLH06) analyzed in this study (Nakata et al, 2013;Sasaki-Sekimoto et al, 2013;Song et al, 2013;Fonseca et al, 2014). Furthermore, these bHLH subgroup IIId TFs function redundantly to negatively regulate JA-mediated plant defense; therefore, it is highly probable that bHLH03, bHLH13, bHLH14, and bHLH17 factors are transcriptional repressors of GSL biosynthesis and antagonize bHLH04, bHLH05, and bHLH06.…”

Section: Combinatorial Gene Regulation By Myb-bhlh Complexesmentioning

confidence: 79%

bHLH05 Is an Interaction Partner of MYB51 and a Novel Regulator of Glucosinolate Biosynthesis in Arabidopsis

2014

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By means of yeast (Saccharomyces cerevisiae) two-hybrid screening, we identified basic helix-loop-helix transcription factor05 (bHLH05) as an interacting partner of MYB51, the key regulator of indolic glucosinolates (GSLs) in Arabidopsis (Arabidopsis thaliana). Furthermore, we show that bHLH04, bHLH05, and bHLH06/MYC2 also interact with other R2R3-MYBs regulating GSL biosynthesis. Analysis of bhlh loss-of-function mutants revealed that the single bhlh mutants retained GSL levels that were similar to those in wild-type plants, whereas the triple bhlh04/05/06 mutant was depleted in the production of GSL. Unlike bhlh04/06 and bhlh05/06 mutants, the double bhlh04/05 mutant was strongly affected in the production of GSL, pointing to a special role of bHLH04 and bHLH05 in the control of GSL levels in the absence of jasmonic acid. The combination of two specific gain-of-function alleles of MYB and bHLH proteins had an additive effect on GSL levels, as demonstrated by the analysis of the double MYB34-1D bHLH05D94N mutant, which produces 20-fold more indolic GSLs than bHLH05D94N and ecotype Columbia-0 of Arabidopsis. The amino acid substitution D94N in bHLH05D94N negatively affects the interaction with JASMONATE-ZIM DOMAIN protein, thereby resulting in constitutive activation of bHLH05 and mimicking jasmonic acid treatment. Our study revealed the bHLH04, bHLH05, and bHLH06/MYC2 factors as novel regulators of GSL biosynthesis in Arabidopsis.

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bHLH003, bHLH013 and bHLH017 Are New Targets of JAZ Repressors Negatively Regulating JA Responses

Cited by 113 publications

References 62 publications

The RING E3 Ligase KEEP ON GOING Modulates JASMONATE ZIM-DOMAIN12 Stability

The RING E3 Ligase KEEP ON GOING Modulates JASMONATE ZIM-DOMAIN12 Stability

Arabidopsis MYC Transcription Factors Are the Target of Hormonal Salicylic Acid/Jasmonic Acid Cross Talk in Response to Pieris brassicae Egg Extract

bHLH05 Is an Interaction Partner of MYB51 and a Novel Regulator of Glucosinolate Biosynthesis in Arabidopsis

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