Volatile organic compounds emitted from the damaged hot peppers are oppositely interpreted by thrips and its predator

A plant emits diverse volatile compounds and communicates with other organisms in different trophic levels. Deciphering these compounds would be useful to understand their biorational interactions. Hot pepper, Capsicum annuum, produced different compositions of volatile organic compounds (VOCs) upon an infestation by the western flower thrips, Frankliniella occidentalis. These VOCs induced a non-preference behavior to the thrips while they attracted a natural enemy, Orius laevigatus. Among the differentially emitted VOCs, green leaf volatiles (GLVs) and terpenes were included and played crucial roles in their interactions. Z-3-methyl hexenoate, one of GLVs, induced the non-preference behavior but attracted the predator. Similarly, a terpenoid linalool attracted the predator but gave the non-preference to the thrips. Suppression of GLV or linalool biosynthesis was performed by virus-induced gene silencing of hydroperoxide lyase (HPL) or linalool synthase (LS) expression in the hot pepper and led to significant malfunction in the tri-trophic communication. The tri-trophic interactions were mediated by jasmonic acid (JA), but not salicylic acid, signal in the hot pepper. Insect resistance of the hot peppers against the thrips were positively correlated with HPL or LS expression levels, which would be useful for breeding programs for insect-resistant hot peppers.