High-resolution kinetics of herbivore-induced plant volatile transfer reveal clocked response patterns in neighboring plants

Abstract

Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), with important consequences for community dynamics. However, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-Tof-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in distinct temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a clocked stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern, with potentially important consequences for plant-herbivore dynamics and tritrophic interactions. This work also contributes to answering the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants.