Wild-type and resistance-breaking strains of tomato spotted wilt virus differentially upregulate the immunosuppressive epoxyoctadecamonoenoic acid biosynthesis of its insect vector, Frankliniella occidentalis

TL;DR

Tomato spotted wilt virus uses different strains to manipulate thrips' immune system, increasing virus spread by altering fatty acid production.

Contribution

The study reveals how resistance-breaking virus strains suppress thrips immunity more effectively than wild-type strains through NSs protein variation.

Findings

Resistance-breaking TSWV strains increase viral titers in thrips by upregulating EpOME biosynthesis genes.

PGE2 reduces viral accumulation by promoting apoptosis in thrips gut cells.

NSs protein variation modulates differential immune suppression in thrips and non-target insects like Spodoptera exigua.

Abstract

Tomato spotted wilt virus (TSWV) is a highly destructive plant pathogen transmitted by thrips, including Frankliniella occidentalis, in a circulative and propagative manner. To counter viral infections, thrips activate antiviral defences through C20 oxygenated polyunsaturated fatty acids (PUFAs), known as eicosanoids. However, at later stages of infection, C18 PUFAs, including epoxyoctadecamonoenoic acids (EpOMEs), modulate immune responses by preventing excessive and unnecessary activation. Our previous study demonstrated that TSWV elevates EpOME levels in thrips to suppress antiviral responses and enhance viral replication, with its nonstructural protein S (NSs) playing a key role in this process. In this study, we investigated the impact of NSs protein variation on vector immunity and virus–vector interactions. We assessed relative TSWV titres in thrips larvae and examined the role of eicosanoids, specifically 12,13-EpOME and PGE2, in regulating viral load and apoptosis. Our results revealed that 12,13-EpOME significantly increased viral titres, whereas PGE2 reduced the viral accumulation by promoting apoptosis in the vector insect. Phylogenetic analysis identified distinct NSs variations among TSWV isolates, with resistance-breaking (RB) and WT strains, which modulated differential infection patterns in thrips gut tissues, as visualized through fluorescence in situ hybridization. RB strains exhibited significantly higher viral titres, along with increased expression of EpOME biosynthetic gene (Fo-CYP24) and decreasing expression of EpOME degradation gene (Fo-sEH2). Apoptosis assays using the terminal deoxynucleotidyl transferase dUTP nick-end labelling assay further indicated that RB strains suppressed the gut epithelial cell death in thrips by antagonizing a process regulated by PGE2. Additionally, in vivo transient expression of the NSs gene in a nontarget insect, Spodoptera exigua, demonstrated the immunosuppressive effects by inducing EpOME level through upregulation of Se-CYP expression and downregulation of Se-sEH expression. Indeed, RB strains suppressed cellular immune responses more effectively than WT strains in S. exigua. These findings provide novel insight into the role of NSs genetic variation in TSWV transmission in the insect vector as well as in the host plants.

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