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Ethylene Signaling Renders the Jasmonate Response of Arabidopsis Insensitive to Future Suppression by Salicylic Acid

¹Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, P.O. Box 800.56, 3508 TB Utrecht, The Netherlands; ²Institute of Biology, Leiden University, P.O. Box 9505, 2300 RA Leiden, The Netherlands; ³Dipartimento di Agrobiologia e Agrochimica, Universita' della Tuscia, Viterbo, 01100, Italy; ⁴Centre for BioSystems Genomics, P.O. Box 98, 6700 AB Wageningen, The Netherlands

Cross-talk between jasmonate (JA), ethylene (ET), and Salicylic acid (SA) signaling is thought to operate as a mechanism to fine-tune induced defenses that are activated in response to multiple attackers. Here, 43 Arabidopsis genotypes impaired in hormone signaling or defense-related processes were screened for their ability to express SA-mediated suppression of JA-responsive gene expression. Mutant cev1, which displays constitutive expression of JA and ET responses, appeared to be insensitive to SA-mediated suppression of the JA-responsive marker genes PDF1.2 and VSP2. Accordingly, strong activation of JA and ET responses by the necrotrophic pathogens Botrytis cinerea and Alternaria brassicicola prior to SA treatment counteracted the ability of SA to suppress the JA response. Pharmacological assays, mutant analysis, and studies with the ET-signaling inhibitor 1-methylcyclopropene revealed that ET signaling renders the JA response insensitive to subsequent suppression by SA. The APETALA2/ETHYLENE RESPONSE FACTOR transcription factor ORA59, which regulates JA/ET-responsive genes such as PDF1.2, emerged as a potential mediator in this process. Collectively, our results point to a model in which simultaneous induction of the JA and ET pathway renders the plant insensitive to future SA-mediated suppression of JA-dependent defenses, which may prioritize the JA/ET pathway over the SA pathway during multi-attacker interactions.