Herbivore-Induced (Z)-3-Hexen-1-ol is an Airborne Signal That Promotes Direct and Indirect Defenses in Tea (Camellia sinensis) under Light

Tea (Camellia sinensis) is the most popular nonalcoholic beverage worldwide. During cultivation, tea plants are susceptible to herbivores and pathogens, which can seriously affect tea yield and quality. A previous report showed that (Z)-3-hexenol is a potentially efficient defensive substance. However, the molecular mechanism mediating (Z)-3-hexenol signaling in tea plants and the resulting effects on plant defenses remain uncharacterized. To clarify the signaling mechanisms in which (Z)-3-hexenol and light are involved, the gene transcription and metabolite levels were assessed, respectively. This study demonstrated that tea plants rapidly and continuously release (Z)-3-hexen-1-ol in response to an insect infestation. (Z)-3-Hexen-1-ol absorbed by adjacent healthy plants would be converted into three insect defensive compounds: (Z)-3-hexenyl-glucoside, (Z)-3-hexenyl-primeveroside, and (Z)-3-hexenyl-vicianoside identified with laboratory-synthesized standards. Moreover, (Z)-3-hexen-1-ol also activates the synthesis of jasmonic acid to enhance the insect resistance of tea plants. Additionally, a continuous light treatment induces the accumulation of (Z)-3-hexenyl-glycosides. Hence, (Z)-3-hexenol serves as a light-regulated signaling molecule that activates the systemic defenses of adjacent plants. Our study reveals the molecular mechanisms by which biotic and abiotic factors synergistically regulate the signaling functions of herbivore-induced plant volatiles in plants, providing valuable information for future comprehensive analyses of the systemic defense mechanisms in plants.