Tomato Spotted Wilt Virus Benefits Its Thrips Vector by Modulating Metabolic and Plant Defense Pathways in Tomato

Abstract

Several plant viruses modulate vector fitness and behavior in ways that may enhance virus transmission. Previous studies have documented indirect, plant-mediated effects of tomato spotted wilt virus (TSWV) infection on the fecundity, growth and survival of its principal thrips vector, Frankliniella occidentalis, the western flower thrips. We conducted thrips performance and preference experiments combined with plant gene expression, phytohormone and total free amino acid analyses to determine if systemically-infected tomato plants modulate primary metabolic and defense-related pathways to culminate into a more favorable environment for the vector. In a greenhouse setting, we documented a significant increase in the number of offspring produced by F. occidentalis on TSWV-infected tomato plants compared to mock-inoculated plants, and in choice test assays, females exhibited enhanced settling on TSWV-infected leaves. Microarray analysis combined with phytohormone signaling pathway analysis revealed reciprocal modulation of key phytohormone pathways under dual attack, possibly indicating a coordinated and dampening defense against the vector on infected plants. TSWV infection, alone or in combination with thrips, suppressed genes associated with photosynthesis and chloroplast function thereby significantly impacting primary metabolism of the host plant, and hierarchical cluster and network analyses revealed that many of these genes were co-regulated with phytohormone defense signaling genes. TSWV infection increased expression of genes related to protein synthesis and degradation which was reflected in the increased total free amino acid content in virus-infected plants that harbored higher thrips populations. These results suggest coordinated gene networks that regulate plant primary metabolism and defense responses rendering virus-infected plants more conducive for vector colonization, an outcome that is potentially beneficial to the vector and the virus when considered within the context of the complex transmission biology of TSWV. To our knowledge this is the first study to identify global transcriptional networks that underlie the TSWV-thrips interaction as compared to a single mechanistic approach. Findings of this study increase our fundamental knowledge of host plant-virus-vector interactions and identifies underlying mechanisms of induced host susceptibility to the insect vector.