Metabolic changes in root exudates of plants with different disease severity affect plant resistance by regulating the rhizosphere microbiome

BACKGROUND: Root exudates play a critical role in plant-microorganism interactions. However, information on the metabolic change in root exudates of plants with different disease severities of bacterial wilt is limited. Here, we investigate the differential metabolic pathway and metabolites among root exudates secreted by the low-grade, moderately, and severely Ralstonia solanacearum-infected tobacco plants and healthy plants. RESULTS: Comparative analysis reveals a large divergence among metabolic profiles and rhizosphere microbial communities of the healthy plants and R. solanacearum-infected plants in terms of metabolic spectrum, community composition and diversity. The intensities of efetaal, 6-methylnicotinamide, proline, sinapinic acid, and syringic acid increase with increasing disease severity, which are chemoattractants of R. solanacearum and pathogen helpers Sphingobacterium and Stenotrophomonas, suggesting a potential role of metabolites in pathogen infection. Metabolites upregulated in R. solanacearum-infected plants inhibit the biofilm formation of antagonistic Bacillus amyloliquefaciens WH1. Metabolites elevated in healthy plants including N-acetyl-L-leucine, 3,3-dimethylglutaric acid, 4-ethylphenol, protocatechuic acid, pyridoxine, salicylic acid, trans-cinnamic acid, and tropine are chemoattractants of WH1, support cell growth and enhance biofilm formation and colonization of WH1. McpB and McpC3 are the major methyl-accepting chemotaxis proteins for salicylic acid and trans-cinnamic acid. Nutritional competition is present between WH1 and R. solanacearum. CONCLUSION: Root exudates regulate the rhizosphere microbiome and affect plant resistance. Metabolites upregulated in healthy plants recruit antagonistic bacteria to defend the plant from pathogen invasion. Metabolites upregulated in R. solanacearum-infected plants attract pathogens and their helpers, thus aggravating the disease. © 2025 Society of Chemical Industry.