A calcium-decoding module translates volatile DMNT into jasmonic acid-mediated herbivore resistance in Camellia sinensis

Plants employ sophisticated volatile-mediated signaling mechanisms to defend against herbivore attacks; however, the molecular pathways underlying these processes remain poorly understood. Herein, we unveil the molecular mechanism by which the herbivore-induced volatile (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) activates jasmonic acid (JA) biosynthesis in tea plants (Camellia sinensis). We demonstrate that DMNT triggers early signaling events in tea plants, characterized by a rapid influx of Ca2+ in mesophyll cells, which subsequently initiates a signaling cascade involving the CsCAMTA3 (calmodulin-binding transcription activator, CAMTA). Using luciferase reporter assays, yeast 1-hybrid analysis, electrophoretic mobility shift assays, and antisense oligonucleotide silencing, we demonstrated that CsCAMTA3 directly binds to the CG-box element in the promoter region of the key transcription factor CsWRKY70 and activates its expression. Subsequently, CsWRKY70 binds to the W-box motif in the CsLOX3 (lipoxygenase, LOX) promoter, driving the expression of the JA biosynthetic gene and promoting the accumulation of JA and jasmonoyl-isoleucine (JA-Ile). Silencing CsCAMTA3 or CsWRKY70 significantly inhibits JA biosynthesis and reduces tea plant resistance to tea geometrid (Ectropis obliqua). Furthermore, the suppression of both CsCAMTA3 and CsWRKY70 significantly diminished the ability of tea plants to synthesize JA and JA-Ile in response to DMNT signal induction. Our findings reveal a Ca2+-CAMTA3-WRKY70-LOX3 signaling cascade induced by DMNT, broadening the theoretical framework of plant-plant communication.