Soil-derived bacterial root commensals induce systemic alterations of defence-related secondary metabolism and response in tomato whole plants for favoring resistance against Fusarium wilt

Aims Root-associated beneficial microbes orchestrate systemic defense priming in plants, yet the underlying metabolism-mediated plant-microbe interplay remains poorly understood. Methods Here, it was demonstrated that synthetic bacterial consortia ( Bacillus velezensis YY13, B . subtilis JN1, and Pseudomonas chlororaphis JN72) colonizing tomato roots confer resistance against Fusarium wilt. Untargeted metabolomics and transcriptional reprogramming analysis were employed. The impact of root-exuded flavonoids on the rhizosphere soil microbiome was also investigated. Results Rhizosphere soil colonization by the Syncoms reduced disease severity by 33.49% and enhanced biomass accumulation. Untargeted metabolomics revealed systemic alterations in phenylpropanoid derivatives, with roots showing elevated feruloyltyramine glycosides (2.1-fold) and leaves accumulating quercetin-O-rutinoside (1.8-fold), while redirecting carbon flux from lignin precursors to antifungal metabolites. Transcriptional reprogramming exhibited spatiotemporal specificity, with the early upregulation of PAL/4CL/CHS in roots preceding F3H activation in leaves, thereby synchronizing JA/ET-mediated PR gene induction. Crucially, root-exuded flavonoids (naringenin, quercetin) reshaped rhizosphere soil microbiomes, enriching Actinobacteria (27%) and recruiting plant-protective genera ( Bacillus , Pseudomonas ). This restructured microbiota amplified defense priming through JA/ET-PR positive feedback loops. Conclusions Our findings unveil a tripartite defense mechanism where microbial consortia 1) reprogram phenylpropanoid channeling to prioritize defensive metabolites over structural polymers, 2) elicit tissue-specific immune transcription, and 3) sustain resistance via flavonoid-mediated microbiome recruitment. This phyto-microbial loop paradigm advances the design of synthetic communities for microbiome-assisted crop protection.