Integrated transcriptome and metabolome analysis of resistant and susceptible tomato cultivars in response to tomato mottle mosaic virus and functional characterization of snakin-2 in viral defense.

Abstract

Tomato mottle mosaic virus (ToMMV) is an emerging tobamovirus causing severe losses in tomato production. To elucidate host resistance mechanisms, we compared two tomato cultivars with contrasting responses to ToMMV using integrated transcriptomic, metabolomic, and functional analyses. The resistant line (R) carried resistance gene Tm‑2² at extremely low levels, while the susceptible line (S) did not; both lines highly expressed susceptibility gene tm-2. R plants exhibited minimal viral accumulation and maintained chlorophyll levels, whereas S plants showed high viral load and chlorophyll degradation. Multi-omics revealed that in S, ToMMV primarily disrupted chlorophyll biosynthesis and photosynthesis, while activating multiple defense pathways, including plant-pathogen interaction, phenylpropanoid/flavonoid biosynthesis, and MAPK signaling. In R, a broader activation of plant-pathogen interaction and phosphatidylinositol signaling pathways was observed, alongside early upregulation of SlSN2. The abundance of phenolic acids, notably caffeic acid, ferulic acid, and sinapic acid, was significantly higher in R than in S. Integrated transcriptomic and metabolomic analyses showed that both differential genes and metabolites were co-enriched in the phenylpropanoid biosynthesis pathway. Functional assays demonstrated that SlSN2 overexpression suppressed ToMMV accumulation and infection, likely via enhanced lignin biosynthesis. These findings suggest a potential role for SlSN2 in contributing to ToMMV resistance, independent of the known Tm‑2² pathway. This work identifies SlSN2 as a candidate factor for further evaluation in the prevention of ToMMV.