Plant pathological condition is associated with fungal community succession triggered by root exudates in the plant-soil system

Root-associated microbiota is important for plant health, but there is limited knowledge of how plant pathological condition influences the succession of soil microbial communities, especially the fungal community, in plant-soil systems. We investigated the fungal community succession across a gradient from bulk soil to the plant endosphere of diseased and healthy lisianthus plants using quantitative real-time PCR, amplicon sequencing, and metabolomics. Fungal diversity and richness gradually decreased from the bulk soil to root endosphere, and there were fewer fungi in the rhizosphere soil of diseased plants than healthy plants. While the rhizosphere fungal communities developed to be similar with that of the endosphere in both diseased and healthy plants from flowering to harvesting, the rhizosphere fungal community developed more quickly in diseased plants than healthy plants. More potential antifungal members were present in the bulk soil and rhizosphere of healthy plants, while potential pathogens were more prevalent in the diseased samples. There were significantly more F. oxysporum in the rhizosphere than the bulk soil, and the enrichment of F. oxysporum (i.e. Fusarium wilt pathogen) occurred more quickly in the rhizosphere of diseased plants than healthy plants. More importantly, the root relative electrical conductivity, the concentration of secreted short-chain organic acids like succinic and malic acids, and sugar alcohols were greater in diseased plants than healthy plants. These changes in plant physiology were associated with the faster development of the fungal community and more rapid increase in the pathogen population in the diseased rhizosphere. Taken together, our results highlight the importance of plant pathological condition for the assembly and development of fungal communities in plant-soil systems.