Ethylene response factors 15 and 16 trigger jasmonate biosynthesis in tomato during herbivore resistance

Abstract Jasmonates (JAs) are phytohormones with crucial roles in plant defense. Plants accumulate JAs in response to wounding or herbivore attack, but how JA biosynthesis is triggered remains poorly understood. Here we show that herbivory by cotton bollworm (Helicoverpa armigera) induced both ethylene (ET) and JA production in tomato (Solanum lycopersicum) leaves. Using RNA-seq, ET mutants, and inhibitors of ET signaling, we identified ET-induced ETHYLENE RESPONSE FACTOR 15 (ERF15) and ERF16 as critical regulators of JA biosynthesis in tomato plants. Transcripts of ERF15 and ERF16 were markedly upregulated and peaked at 60 and 15 min, respectively, after simulated herbivore attack. While mutation in ERF16 resulted in the attenuated expression of JA biosynthetic genes and decreased JA accumulation 15 min after the simulated herbivory treatment, these changes were not observed in erf15 mutants until 60 min after treatment. Electrophoretic mobility shift assays and dual-luciferase assays demonstrated that both ERFs15 and 16 are transcriptional activators of LIPOXYGENASE D, ALLENE OXIDE CYCLASE, and 12-OXO-PHYTODIENOIC ACID REDUCTASE 3, key genes in JA biosynthesis. Furthermore, JA-activated MYC2 and ERF16 also function as the transcriptional activators of ERF16, contributing to dramatic increases in ERF16 expression. Taken together, our results demonstrated that ET signaling is involved in the rapid induction of the JA burst. ET-induced ERF15 and ERF16 function as powerful transcriptional activators that trigger the JA burst in response to herbivore attack.