Multi-omics analysis reveals discordant proteome and transcriptome responses in larval guts of Frankliniella occidentalis infected with an orthotospovirus.

Abstract

The western flower thrips, Frankliniella occidentalis, is the principal thrips vector of Orthotospovirus tomatomaculae (order Bunyavirales, family Tospoviridae), a devastating plant-pathogenic virus commonly referred to as tomato spotted wilt virus (TSWV). The larval gut is the gateway for virus transmission by F. occidentalis adults to plants. In a previous report, gut expression at the transcriptome level was subtle but significant in response to TSWV in L1s. Since it has been well documented that the relationship between the expression of mRNA and associated protein products in eukaryotic cells is often discordant, we performed identical, replicated experiments to identify and quantify virus-responsive larval gut proteins to expand our understanding of insect host response to TSWV. While we documented statistically significant, positive correlations between the abundance of proteins (4189 identified) and their cognate mRNAs expressed in first and second instar guts, there was virtually no alignment of individual genes identified to be differentially modulated by virus infection at the transcriptome and proteome levels. Predicted protein-protein interaction networks associated with clusters of co-expressed proteins revealed wide variation in correlation strength between protein and cognate transcript abundance, which appeared to be associated with the type of cellular processes, cellular compartments and network connectivity represented by the proteins. In total, our findings indicate distinct and dynamic regulatory mechanisms of transcript and protein abundance (expression, modifications and/or turnover) in virus-infected gut tissues. This study provides molecular candidates for future functional analysis of thrips vector competence and underscores the necessity of examining complex virus-vector interactions at a systems level.