Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground

Plants transmit ecologically relevant messages to neighbouring plants through chemical cues. For instance, insect herbivory triggers the production of herbivore‐induced plant volatiles (HIPVs), which can enhance neighbouring plant defences. HIPVs are emitted from directly damaged plant tissues and from systemic, nondamaged tissues. Although volatile‐mediated interplant interactions have been observed both above‐ and belowground, it remains unknown whether belowground herbivory induces systemic HIPVs aboveground that influence neighbouring plants. To explore how belowground herbivory affects interplant interactions aboveground, we characterised systemic HIPVs from squash induced by belowground striped cucumber beetle (Acalymma vittatum) larval herbivory. We exposed squash ‘receiver plants’ to systemic HIPVs or volatiles from nondamaged plants. We then measured herbivore resistance by challenging ‘receiver plants’ with aboveground‐feeding herbivores: adult beetles (A. vittatum) or squash bugs (Anasa tristis). We discovered belowground‐damaged plants emitted more (E)‐β‐ocimene, a key volatile from the systemic HIPV blend, than nondamaged controls, and that exposure to systemic HIPVs enhanced neighbouring plant resistance to aboveground squash bugs, but not adult beetles. Further investigations into the mechanism of interplant interaction revealed β‐ocimene alone can elicit plant resistance against squash bugs. Overall, our findings reveal a novel form of volatile‐mediated interactions between plants spanning across aboveground–belowground plant systems. Summary Statement Belowground insect herbivory alters aboveground volatiles emitted by squash plants. Exposing neighbouring plants to these volatiles enhances plant resistance to an aboveground heterospecific insect herbivore, but not aboveground conspecifics.