The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi

Maruyama, Yosuke; Yamoto, Natsuko; Suzuki, Yoshishige; Chiba, Yasuhiro; Yamazaki, Kaoru; Sato, Takeo; Yamaguchi, Junji

doi:10.1016/j.plantsci.2013.08.008

Cited by 109 publications

(87 citation statements)

References 35 publications

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“…As soon as ORA59 protein levels would drop beneath a certain threshold, EAR-ERFs, which are only slightly affected by SA, might compete efficiently with ORA59 at GCCGCC elements and would, thus, lower transcription of ACC-induced ORA59 target genes. This notion is consistent with a recent report that documents a repressive function of ERF9 at the GCCGCC element of the PDF1.2 promoter (Maruyama et al, 2013). Although such a contribution of repressive ERFs to the SA-ET antagonism is conceivable, it does not explain that the SA-ET antagonism is stronger at promoters downstream of ORA59 than on the ORA59 promoter itself.…”

Section: Ora59 But Not Erf1 Affects Expression Of Downstream Genes Susupporting

confidence: 89%

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression

2014

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Salicylic acid (SA), a hormone essential for defense against biotrophic pathogens, triggers increased susceptibility of plants against necrotrophic attackers by suppressing the jasmonic acid-ethylene (ET) defense response. Here, we show that this diseasepromoting SA effect is abolished in plants lacking the three related TGACG sequence-specific binding proteins TGA2, TGA5, and TGA6 (class II TGAs). After treatment of plants with the ET precursor 1-aminocyclopropane-1-carboxylic acid (ACC), activation of all those genes that are suppressed by SA depended on class II TGAs. Rather than TGA binding sites, GCC-box motifs were significantly enriched in the corresponding promoters. GCC-box motifs are recognized by members of the superfamily of APETALA2/ETHYLENE RESPONSE FACTORs (ERFs). Of 11 activating ACC-induced APETALA2/ERFs, only ORA59 (for OCTADECANOID-RESPONSIVE ARABIDOPSIS APETALA2/ETHYLENE RESPONSE FACTOR domain protein59) and ERF96 were strongly suppressed by SA. ORA59 is the master regulator of the jasmonic acid-ET-induced defense program. ORA59 transcript levels do not reach maximal levels in the tga2 tga5 tga6 triple mutant, and this residual activity cannot be suppressed by SA. The ORA59 promoter contains an essential TGA binding site and is a direct target of class II TGAs as revealed by chromatin immunoprecipitation experiments. We suggest that class II TGAs at the ORA59 promoter constitute an important regulatory hub for the activation and SA suppression of ACC-induced genes.

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Section: Ora59 But Not Erf1 Affects Expression Of Downstream Genes Susupporting

confidence: 89%

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression

2014

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“…AtERF4 expression is induced by ABA, JA, ET, and abiotic stress, and overexpression of AtERF4 represses ABA responses, whereas it may enhance JA responsiveness (Yang et al, 2005;Memelink, 2009). Other plant AP2-ERFs, including OsERF922 and wheat PATHOGEN-INDUCED ERF1, also appear to regulate abiotic stress tolerance or disease resistance against necrotrophic pathogens mediated by JA, ABA, or ET (Pré et al, 2008;Liu et al, 2012;Moffat et al, 2012;Maruyama et al, 2013;Zhu et al, 2014). Notably, HvERF-like and HvERF44411 were systemically induced by MeJA and/or ABA application (Fig.…”

Section: Discussionmentioning

confidence: 99%

Bacteria-Triggered Systemic Immunity in Barley Is Associated with WRKY and ETHYLENE RESPONSIVE FACTORs But Not with Salicylic Acid

et al. 2014

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Leaf-to-leaf systemic immune signaling known as systemic acquired resistance is poorly understood in monocotyledonous plants. Here, we characterize systemic immunity in barley (Hordeum vulgare) triggered after primary leaf infection with either Pseudomonas syringae pathovar japonica (Psj) or Xanthomonas translucens pathovar cerealis (Xtc). Both pathogens induced resistance in systemic, uninfected leaves against a subsequent challenge infection with Xtc. In contrast to systemic acquired resistance in Arabidopsis (Arabidopsis thaliana), systemic immunity in barley was not associated with NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 or the local or systemic accumulation of salicylic acid. Instead, we documented a moderate local but not systemic induction of abscisic acid after infection of leaves with Psj. In contrast to salicylic acid or its functional analog benzothiadiazole, local applications of the jasmonic acid methyl ester or abscisic acid triggered systemic immunity to Xtc. RNA sequencing analysis of local and systemic transcript accumulation revealed unique gene expression changes in response to both Psj and Xtc and a clear separation of local from systemic responses. The systemic response appeared relatively modest, and quantitative reverse transcriptionpolymerase chain reaction associated systemic immunity with the local and systemic induction of two WRKY and two ETHYLENE RESPONSIVE FACTOR (ERF)-like transcription factors. Systemic immunity against Xtc was further associated with transcriptional changes after a secondary/systemic Xtc challenge infection; these changes were dependent on the primary treatment. Taken together, bacteria-induced systemic immunity in barley may be mediated in part by WRKY and ERF-like transcription factors, possibly facilitating transcriptional reprogramming to potentiate immunity.

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“…Another set of TFs had previously been linked to growth and the cell cycle, including E2Fc (del Pozo et al, 2006;Berckmans et al, 2011), G-BOX BINDING FACTOR2 (GBF2; Schindler et al, 1992;Menkens and Cashmore, 1994;Terzaghi et al, 1997), GROWTH REGULATING FACTOR (GRF; (Hewezi et al, 2012;Casadevall et al, 2013), and AINTEGUMENTA (ANT; Elliott et al, 1996;Klucher et al, 1996;Krizek et al, 2000;Liu et al, 2000;Mizukami and Fischer, 2000;Horstman et al, 2014). Of these previously characterized TFs, only ERF9 had been previously associated with biotic stress and the resistance to necrotrophic fungi (Camehl and Oelmüller, 2010;Maruyama et al, 2013). This diversity of TF functions suggests that the aliphatic GLS biosynthetic gene promoters can function as a site of integration for a complex set of signals integrating across growth and defense to both abiotic and biotic stresses with respect to GLS levels.…”

Section: Phenotypic Validation Of Gls Regulatory Potentialmentioning

confidence: 99%

Promoter-Based Integration in Plant Defense Regulation

Li¹,

Gaudinier

Tang

et al. 2014

Plant Physiology

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A key unanswered question in plant biology is how a plant regulates metabolism to maximize performance across an array of biotic and abiotic environmental stresses. In this study, we addressed the potential breadth of transcriptional regulation that can alter accumulation of the defensive glucosinolate metabolites in Arabidopsis (Arabidopsis thaliana). A systematic yeast one-hybrid study was used to identify hundreds of unique potential regulatory interactions with a nearly complete complement of 21 promoters for the aliphatic glucosinolate pathway. Conducting high-throughput phenotypic validation, we showed that .75% of tested transcription factor (TF) mutants significantly altered the accumulation of the defensive glucosinolates. These glucosinolate phenotypes were conditional upon the environment and tissue type, suggesting that these TFs may allow the plant to tune its defenses to the local environment. Furthermore, the pattern of TF/promoter interactions could partially explain mutant phenotypes. This work shows that defense chemistry within Arabidopsis has a highly intricate transcriptional regulatory system that may allow for the optimization of defense metabolite accumulation across a broad array of environments.An organism's growth and fitness within its environment are largely determined by its ability to efficiently obtain and utilize energy and elements to create biomass to survive. Central to this process is primary metabolism, which determines the use of energy and chemicals from the environment to produce all of the necessary building blocks for cells and the resulting biomass. To optimize fitness, metabolism must be precisely tuned and coordinated to make the most efficient use of available resources. This basic supposition is central to a wide range of biological fields from the study of organismal growth to the study of interactions with the environment, and has led to strong interest in understanding how metabolism is regulated (Karban and Baldwin, 1997;Smith and Stitt, 2007).The last decade has seen an upsurge in studies investigating the transcriptional control over metabolism. This has largely been driven by three key areas of focus: regulation of sugar metabolism, amino acid metabolism, and secondary metabolism (Desvergne et al., 2006). In most organisms, Glc levels cause transcriptional reprograming of sugar metabolism and organismal development often by a mitogen-activated protein kinase cascade (Moore et al., 2003;Rolland et al., 2006). Transcriptional control over amino acid metabolism frequently involves General Control Nonderepressible4, whereas other transcriptional activators play a role in coordinating amino acid metabolism (Hope and Struhl, 1986;Neuwald and Landsman, 1997;Li et al., 2013). Within plants, there are also amino acid pathway-specific transcription factors (TFs) known for a couple of plant amino acid biosynthetic pathways (Celenza et al., 2005;Maruyama-Nakashita et al., 2006). In plants, the transcriptional regulation of secondary metabolites has also received signifi...

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The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi

Cited by 109 publications

References 35 publications

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression

TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression

Bacteria-Triggered Systemic Immunity in Barley Is Associated with WRKY and ETHYLENE RESPONSIVE FACTORs But Not with Salicylic Acid

Promoter-Based Integration in Plant Defense Regulation

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