Integrated Omics Analysis Reveals Flavonoid‐Mediated Resistance to Tomato Spotted Wilt Virus

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ABSTRACT Tomato spotted wilt virus (TSWV) poses a severe threat to global tomato production. Developing resistant cultivars requires a deeper understanding of the molecular mechanisms underlying plant‐virus interactions. In this study, we employed an intergrated transcriptomic and metabolomic analysis to investigate the defense responses of a moderately resistant tomato line (MR2T826) compared to two susceptible lines (SV2T482 and SV2T1130) at 3 days post‐inoculation under TSWV infection. Metabolomic profiling identified a total of 1970 metabolites, with flavonoids and alkaloids being the most abundant classes. KEGG based pathway analysis revealed that the top four pathways ranked by enrichment significance in both comparisons (MR2T826_vs_SV2T482 and MR2T826_vs_SV2T1130). The pathway names were Biosynthesis of solanidine and solasodine steroidal glycoalkaloids, Flavonoid biosynthesis, Flavone and flavonol biosynthesis, and Biosynthesis of quercetin aglycones I. Further analysis of Flavonoid biosynthesis pathway presented eighteen shared flavonoid differentially accumulated metabolites (DAMs). Notably, eleven out of eighteen shared flavonoid DAMs were consistently upregulated in MR2T826, including several quercetin derivatives. Alongside, transcriptomic analysis revealed 450 differentially expressed genes common in MR2T826_vs_ SV2T482 and MR2T826_vs_ SV2T1130, among which 180 were significantly upregulated in MR2T826, including key transcription factors (e.g., NAC22, NAC56, BH063) and pathogenesis‐related protein genes. Integrated KEGG analysis revealed coordinated upregulation of quercetin‐related metabolites and key flavonoid biosynthetic genes in the resistant line MR2T826 compared with susceptible lines, indicating enhanced activation of flavonoid‐related pathways. Taken together, our results suggest that activation of flavonoid biosynthesis, potentially coordinated by specific transcription factors and associated with enhanced antioxidant capacity, is associated with the resistance response of tomato to TSWV. These findings provide new insights into the metabolic features of a moderately resistant tomato line and offer potential targets for future functional studies and resistance breeding.

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