Dual functions of apigenin in suppressing Phytophthora capsici and shaping the pepper microbiome

BACKGROUND: Plant resistance to soil-borne pathogens is shaped by the interactions among host genetics, root exudates, and rhizosphere microbiomes. Flavonoids are widely recognized for their antimicrobial and signaling functions, yet their role in mediating metabolite-microbiome-pathogen interactions in pepper (Capsicum frutescens) remains poorly understood. RESULTS: Through integrated microbiome, transcriptome, and metabolome analyses, we compared resistant (CA53) and susceptible (CA476) pepper cultivars under challenge by Phytophthora capsici in the pepper rhizosphere. Resistant plants maintained relatively stable transcriptional and metabolic profiles, whereas susceptible plants exhibited a pronounced suppression of the flavonoid biosynthesis pathway, with a marked decline in apigenin levels. Exogenous application of apigenin significantly enhanced pepper resistance by disrupting sporangial cell membrane integrity and thereby inhibiting zoospore release (95% reduction in zoospore release). In addition, apigenin functioned as a central hub metabolite, selectively enriching disease-suppressive rhizosphere microbes and reinforcing host protection. CONCLUSION: Our findings uncover a dual role of apigenin in pepper resistance: directly inhibiting pathogen propagation and indirectly reinforcing the recruitment of protective microbiota. These insights highlight the ecological functions of root-derived metabolites in shaping plant-microbiome interactions and provide potential avenues for metabolite-informed strategies in sustainable crop protection. Video Abstract.