CsNAC2 and CsMYB306 orchestrate a jasmonate signaling cascade contributing to tea plant resistance to Ectropis obliqua

(Z)-3-Hexenyl acetate (3-HAC) is an herbivore-induced plant volatile (HIPV) that plays a crucial role in plant herbivore resistance. In this study, we report the mechanisms underlying the anti-herbivore activity of 3-HAC. Stable-isotope-labeled [2H2]-3-HAC was applied to tea plants and was effectively absorbed by the leaves, subsequently inducing resistance against the destructive herbivore Ectropis obliqua. An integrated omics approach revealed that 3-HAC accelerates jasmonic acid (JA) biosynthesis. A lipoxygenase gene (CsLOX2), an early committed gene in JA biosynthesis, was significantly induced by exogenous 3-HAC exposure, and its suppression attenuated 3-HAC-induced JA biosynthesis and impaired the acquired resistance of tea plants to E. obliqua. Furthermore, two transcription factors, CsNAC2 and CsMYB306, which were co-expressed with CsLOX2 under 3-HAC induction, positively regulated CsLOX2 transcription. Suppression of either one attenuated 3-HAC-induced JA biosynthesis and tea plant resistance to E. obliqua. Simultaneous suppression of both genes showed stronger effects than the suppression of either gene alone. These findings provide insights into the mechanisms of HIPV-induced herbivore resistance in plants and emphasize the agricultural significance of 3-HAC as an environmentally friendly anti-herbivore agent.