Herbivore-induced volatiles reduce the susceptibility of neighboring tomato plants to transmission of a whitefly-borne begomovirus

Plant viruses exist in a broader ecological community, with key components include non-vector herbivores that can impact vector abundance, behavior, and virus transmission within shared host plants. However, little is known about the effects of non-vector herbivores infestation on the virus transmission by vector insects on the neighboring plants through inter-plant airborne chemicals. In this study, we investigated how volatiles emitted from tomato plants infested with the two-spotted spider mite (Tetranychus urticae) affect the infection of Tomato yellow leaf curl virus (TYLCV) transmitted by the whitefly (Bemisia tabaci) in the neighboring plants. Exposure of neighboring tomato plants to volatiles released from T. urticae-infested tomato plants reduced subsequent herbivory as well as TYLCV transmission and infection, and JA signaling pathway was essential for generation of the inter-plant defense signals. We also demonstrated that (E)-β-Ocimene and MeSA were two volatiles induced by T. urticae that synergistically attenuated TYLCV transmission and infection in tomato. Thus, our findings suggest that plant-plant communication via volatiles likely represents a widespread defensive mechanism that substantially contributes to plant fitness. Understanding such phenomena may help us to predict the occurrence and epidemic of multiple herbivores and viruses in the agroecosystem, ultimately to manage pest and virus outbreaks.