Salicylic Acid Suppresses Jasmonic Acid Signaling Downstream of SCFCOI1-JAZ by Targeting GCC Promoter Motifs via Transcription Factor ORA59

• Published in: The Plant cell 2013-02, Vol.25 (2), p.744-761
• Main Authors: Van der Does, Dieuwertje, Leon-Reyes, Antonio, Koornneef, Annemart, Van Verk, Marcel C., Rodenburg, Nicole, Pauwels, Laurens, Goossens, Alain, Körbes, Ana P., Memelink, Johan, Ritsema, Tita, Van Wees, Saskia C.M., Pieterse, Corné M.J.
• Format: Article
• Language: English
• Subjects: Acetates - pharmacology; Arabidopsis - drug effects; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Binding Sites; Crosstalk; Cyclopentanes - metabolism; Cyclopentanes - pharmacology; Gene expression regulation; Gene Expression Regulation, Plant - drug effects; Genes; Homeodomain Proteins - genetics; Homeodomain Proteins - metabolism; Nuclear Proteins - genetics; Nuclear Proteins - metabolism; Nucleotide Motifs; Oxylipins - metabolism; Oxylipins - pharmacology; Pathogens; Peptide Termination Factors - genetics; Peptide Termination Factors - metabolism; Plant cells; Plants; Plants, Genetically Modified; Promoter Regions, Genetic; RNA; Salicylic Acid - metabolism; Salicylic Acid - pharmacology; Seedlings; Signal Transduction - drug effects; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Transcriptional regulatory elements
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.112.108548

Antagonism between the defense hormones salicylic acid (SA) and jasmonic acid (JA) plays a central role in the modulation of the plant immune signaling network, but the molecular mechanisms underlying this phenomenon are largely unknown. Here, we demonstrate that suppression of the JA pathway by SA functions downstream of the E3 ubiquitin-ligase Skip-Cullin-F-box complex SCF COI1 , which targets JASMONATE ZIM-domain transcriptional repressor proteins (JAZs) for proteasome-mediated degradation. In addition, neither the stability nor the JA-induced degradation of JAZs was affected by SA. In silico promoter analysis of the SA/JA crosstalk transcriptome revealed that the 1-kb promoter regions of JA-responsive genes that are suppressed by SA are significantly enriched in the JA-responsive GCC-box motifs. Using GCC:GUS lines carrying four copies of the GCC-box fused to the β-glucuronidase reporter gene, we showed that the GCC-box motif is sufficient for SA-mediated suppression of JA-responsive gene expression. Using plants overexpressing the GCC-box binding APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factors ERF1 or ORA59, we found that SA strongly reduces the accumulation of ORA59 but not that of ERF1. Collectively, these data indicate that the SA pathway inhibits JA signaling downstream of the SCF COI1 -JAZ complex by targeting GCC-box motifs in JA-responsive promoters via a negative effect on the transcriptional activator ORA59.