Phosphorus availability drives rhizosphere metabolite-microbial community interactions to modulate cucumber susceptibility to Fusarium wilt

BACKGROUND: Agricultural intensification has led to excessive phosphorus fertilizer application on croplands, yet the causal linkage between soil phosphorus enrichment and soil-borne disease susceptibility mediated by rhizosphere microbial community remains unclear. This study aimed to decipher how phosphorus availability modulates cucumber susceptibility to Fusarium wilt by restructuring rhizosphere metabolite-microbial community interactions. RESULTS: We demonstrate that a moderately low phosphorus availability enhances cucumber resistance to Fusarium wilt. Amplicon sequencing analyses reveal that low phosphorus conditions promote microbial community stochastic assembly, enriching beneficial genera (bacterial genera Bacillus, Devosia, Sphingopyxis, Cupriavidus, and fungal genera Aspergillus and Amesia) with dual functions of phosphate solubilization and disease resistance, and enhancing cross-kingdom network robustness. In contrast, high phosphorus availability induced deterministic assembly and increased disease incidence by 62% compared to low phosphorus treatment. Metabolomics identified low phosphorus distinguished rhizosphere metabolites (succinic acid, azelaic acid, threonic acid, and methionine) that recruit beneficial taxa, whereas high phosphorus distinguished rhizosphere metabolites promoted pathogen growth. To validate the functional role of microbes-metabolites interaction, we constructed a synthetic microbial community composed of the signature taxa from the low phosphorus microbiota, which, when combined with low phosphorus metabolites, reduced pathogen abundance by 85% and conferred disease suppression under high phosphorus conditions. CONCLUSIONS: Our study establishes a phosphorus-driven mechanism whereby plant-metabolite-microbial community interactions orchestrate rhizosphere immunity. These findings provide new insights and potential strategies for sustainable disease management in agricultural systems with legacy phosphorus accumulation. Video Abstract.