Neophytadiene, a Plant Specialized Metabolite, Mediates the Virus-Vector-Plant Tripartite Interactions

While interactions between viruses and their vectors, as well as between viruses and host plants, have been extensively studied, the genetic mechanisms underlying tripartite interactions remain largely unknown. In this study, phenotypic assays are integrated with molecular biology and functional genomic approaches to elucidate the tripartite interactions involving tomato chlorosis virus (ToCV), a major threat to tomato production worldwide, the whitefly, Bemisia tabaci, an insect vector, and host plants. ToCV infection induces the production of a chlorophyll degradation product that acts as a volatile attractant for whiteflies. Furthermore, the suppression of Lhca4, a gene encoding subunit of light-harvesting complex I in host plants, by the P9 protein of ToCV leads to chlorophyll degradation and neophytadiene biosynthesis. Overexpression of Lhca4 reduced chlorophyll production and ToCV infection. Furthermore, OBP2, an odorant-binding protein from B. tabaci, capable of binding to neophytadiene is identified. Suppression of BtOBP2 impaired vector's subsequent preference for ToCV-infected plants. The results not only reveal the genetic underpinnings, including ToCV P9, host plant Lhca4, and whitefly BtOBP2, governing the virus-vector-plant interactions, but also highlight neophytadiene, a specialized metabolite in host plants, as a mediator of intricate multitrophic interactions, suggesting new avenues for managing plant virus vectored by insects.