Integrative multi-omics analysis uncovers the critical role of plant-derived ferulic acid influencing the occurrence of tomato Fusarium foot rot disease.

Fusarium foot rot, caused by Fusarium solani (Mart.) Sacc., is a major threat to tomato production resulting in a tremendous loss of yield. The interaction between tomato and F. solani has not been well studied. Here we apply an integrative approach with physiological, transcriptomic, and metabolomic analysis to investigate the molecular basis of tomato defense responses to F. solani infection. Pathogen-infected plants have reduced leaf chlorophyll fluorescence, plant elongation, stem thickness and root growth compared to non-infected control. Transcriptome analysis reveals 5654 differentially expressed genes (DEGs) in tomato after the pathogen infection, in which genes associated with the phenylpropanoid biosynthesis such as SlPAL, SlC4H, Sl4CL, and SlCCoAOMT are significantly enriched in KEGG pathway enrichment analysis. Metabolome analysis identifies 1130 differentially accumulated metabolites (DAMs), in which the accumulation of two metabolites from the phenylpropanoid biosynthesis pathway, ferulic acid (FA) and p-coumaraldehyde have dramatic changes after the pathogen infection. Addition of FA in the medium inhibits the fungal growth of F. solani with a concentration-dependent manner. Exogenous application of FA on tomato plants significantly enhanced the resistance to F. solani infection, in which the disease symptoms and plant growth reduction are mitigated compared to the water control plants. Taken together, our study for the first time demonstrates the role of ferulic acid in tomato - F. solani interaction using an integrated multi-omics approach, which benefits the resistance breeding and disease control of Fusarium foot rot in tomato.