Rapid green leaf volatile sensing allows intact plants to release induced volatiles earlier than wounded emitters

Abstract

Organisms in the vicinity of attacked neighbors can respond to danger cues by activating their own defenses. However, the temporal dynamics of these interactions remain poorly resolved, despite their importance for the ensuing effects. Here, we investigated defense responses of maize plants that are exposed to induced volatiles from herbivory-induced neighbors in real time. These experiments revealed a surprising temporal paradox: Intact neighbors start emitting most induced volatiles 15-80 min earlier than the attacked plants themselves. This earlier responsiveness was not associated with earlier induction of defense hormones, volatile biosynthesis genes or within-leaf volatile accumulation. Instead, receiver plants kept their stomata open, while attacked sender plants rapidly closed them to combat water loss. Using different volatile deficient mutants, we demonstrate that the rapid responses in receivers are triggered by green leaf volatiles, which are released from the wound sites of sender plants within minutes independently of stomatal aperture. Thus, non-attacked neighbors can act as "unhindered observers" that activate some defenses more quickly than attacked organisms themselves, as they do not have to deal with wound trauma. The resulting plant volatile concatenation patterns expand our understanding of volatile signaling and have the potential to shape population-level multitrophic interactions.