Herbivory-Induced Stomatal Opening Triggers the Dispersal of an Invasive Insect Herbivore

Stomata play important roles in plant responses to phytopathogens, but less is known about their roles in plant-herbivore interactions. Herbivore damage commonly closes stomata but also elicits the release of herbivory-induced plant volatiles, important mediators of plant-herbivore interactions. Here, we examined the responses in tomato plants attacked by the invasive tomato leafminer (Phthorimaea absoluta), the larvae of which performed better on infested plants, while ovipositing adults were repelled by larvae-infested plants, which were distinct from those induced by two other tomato pests, Bemisia tabaci and Spodoptera exigua. Behavioral assays confirmed that increased releases of volatile benzaldehyde mediated P. absoluta's adult avoidance response, and large-scale glasshouse trials revealed that the induced release of benzaldehyde was sufficient to trigger long-distance dispersal of adults. The benzaldehyde release occurred through herbivory-induced stomatal openings, which were activated by the transcriptional regulation of IQ-Motif Containing Protein 1 (IQM1). P. absoluta population growth and outbreaks were amplified in glasshouse populations of wild-type plants compared to IQM1-mutated plants. P. absoluta's ability to elicit stomatal opening, as some pathogens do, may have facilitated its rapid range expansion as an invasive pest. Our study illustrates a new pattern in stomata-herbivore interactions, adding another layer of complexity to stomata-mediated plant-herbivore interactions.