Multi-omics approach reveals the molecular basis of ToMMV-induced resistance and its effects on tomato fruit quality

Tomato mottle mosaic virus (ToMMV) is a major threat to cultivating tomatoes and other solanaceous plants. Here, an infectious clone of the ToMMV Huludao isolate was constructed, and ToMMV infection significantly reduces soluble sugar, soluble phenolic, and vitamin C contents, while increases titratable acid content in Micro-Tom fruits, thus altering their flavor profile and quality. Integrated transcriptomic and metabolomic analysis indicate that ToMMV infection induced 2090 differentially expressed genes and 709 differentially accumulated metabolites in Micro-Tom fruits. Then, functional analysis using gene silencing validated that bifunctional 3-dehydroquinate dehydratase/shikimate dehydrogenase and glyceraldehyde-3-phosphate dehydrogenase induced by ToMMV in the amino acid biosynthesis pathway play critical roles in tomato fruit quality, while 4-coumarate-CoA ligase, phenylalanine ammonia-lyase and scopoletin glucosyltransferase in the phenylpropanoid biosynthesis pathway were required for host resistance. Our findings elucidate molecular mechanisms of ToMMV-induced fruit quality alteration and highlight metabolic targets for enhanced viral resistance in tomatoes.