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

Abstract

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.

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

“…Additional experiments demonstrated that ET can override NPR1 dependency of SA-JA antagonism, indicating that biotic induction of ET modulates the interaction between SA and JA pathways (Leon-Reyes et al, 2010b). Two recent studies discovered that SA treatment promotes ORA59 protein degradation (Van der Does et al, 2013) and inhibit ORA59 expression (Zander et al, 2014), providing the first clues on how gene expression from the ERF branch of the JA pathway is suppressed.…”

Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways

“…For example, synergism between JA and ethylene signaling ensures effective induction of plant defenses directed against necrotrophic pathogen attack (Memelink, 2009). Moreover, the JA/ethylene and SA signaling pathways negatively influence each other to prioritize specific defense outputs in plant-pathogen interactions (Koornneef and Pieterse, 2008;Zander et al, 2014). JA biosynthesis and signaling is strongly induced by P. syringae infection in inoculated leaves.…”

Ethylene: traffic controller on hormonal crossroads to defense

“…However, in the presence of SA, the same TGAs have a role in SA-mediated antagonism of ERF branch signaling. The TGAs can directly target the activation sequence-1 (as-1) promoter sequence in the ERF transcription factor gene ORA59, thereby regulating its expression (Zander et al, 2014). Possibly through SA-induced glutaredoxins such as GLUTAREDOXIN480 (GRX480) that interact with TGA transcription factors, expression of ORA59 is suppressed (Zander et al, 2012;Caarls et al, 2015).…”