Root exudate-mediated plant–microbiome interactions determine plant health during disease infection

Understanding the interactions between plants and microbes during pathogen infection is crucial for plant health improvement. However, the integrated role of soil nutrients, root exudates, and plant microbiomes in plant health during disease outbreaks remains unclear. In this study, we hypothesized that root exudate-mediated healthy microbiomes (HealthyBiome) would facilitate the escape of soil-borne pathogen infection, whereas a root exudate-mediated disease-conductive microbiome (PathoBiome) would induce disease occurrence. Using watermelon wilt disease caused by Fusarium oxysporum as a model, we investigated these interactions and their implications in plant disease. We examined the pathogen load across plant compartments during the pathogen accumulation (AH) and disease outbreak periods. We analyzed the plant microbiomes and root exudates during the outbreak, which was associated with the emergence in both healthy (BH) and diseased (BD) plants. Compared with AH and BD plants, BH plants had the lowest F. oxysporum density in the root–soil system (0.74–0.84 times that of AH and BD plants). BD plants showed an elevated amino acid metabolism (2.84–3.38 times that of healthy plants), whereas BH plants showed a higher metabolism of phenolic compounds (1.73 times that of diseased plants). BH plants secreted more palmitic acid (1.53 times that of diseased plants) and recruited more nitrogen (N)-fixing bacteria (e.g., Paenarthrobacter, Sphingomonas), which potentially alleviated N scarcity in the soil, promoted plant growth, and improved the plant defense. Structural equation modeling highlighted the interactions among soil nutrients, root metabolites, and plant nutrients in recruiting pro-growth bacteria to the rhizosphere and roots for healthy plant growth. Our findings provide novel evidence of how root exudates influence plant–microbiome interactions during pathogen infections, highlighting the importance of a balanced root exudate profile and its associated “HealthyBiome” in promoting plant health and growth.