Phosphorus availability restructures rhizosphere metabolite–microbiome interactions to modulate plant disease susceptibility

Agricultural intensification has led to excessive phosphorus fertilizer application, resulting in widespread legacy P accumulation in soils. While the role of P in plant nutrition is well-established, its influence on soil-borne disease dynamics—mediated through the rhizosphere microbiome—remains poorly understood. This study demonstrates that moderate P limitation enhances cucumber resistance to Fusarium wilt, whereas high P availability increases disease incidence by 62%. Using integrated amplicon sequencing and metabolomics, we found that low P conditions promote stochastic assembly of the rhizosphere microbiome, enriching beneficial bacterial genera (Bacillus, Devosia, Sphingopyxis, Cupriavidus) and fungal genera (Aspergillus, Amesia) with dual functions in phosphate solubilization and pathogen suppression. These taxa formed robust, stable cross-kingdom networks characterized by negative correlations and high modularity. In contrast, high P conditions led to deterministic assembly, reduced network stability, and increased pathogen abundance. Metabolomic profiling identified low P distinguished rhizosphere metabolites that recruit beneficial microbes, while high P enriched metabolites promoted pathogen growth. A SynCom constructed from key low P taxa, when combined with LPDRMs, reduced pathogen abundance by 85% and conferred disease suppression even under high P conditions. These findings reveal a P-driven mechanism where plant-mediated metabolic reprogramming and microbiome assembly collectively orchestrate rhizosphere immunity, offering novel strategies for sustainable disease management in high P agricultural systems.