Hub metabolites at the root microbiome interface: Ecological targets for alleviating continuous cropping obstacles in Eleutherococcus senticosus

Continuous cropping often leads to yield decline and quality deterioration in medicinal plants due to altered rhizosphere environments. Eleutherococcus senticosus is a valuable medicinal resource that experiences pronounced replanting obstacles. However, the underlying root exudate–microbe interactions are poorly understood. In this study, a total of 18 rhizosphere soil samples were collected under continuous cropping (CC) and crop rotation (CR) systems across three developmental stages (spring, summer, and autumn). Subsequently, metagenomic sequencing and targeted metabolite analysis were combined to profile rhizosphere microbial communities and metabolites under CC and CR. Functional network analysis and in vitro assays were used to assess microbial function, metabolite–microbe associations, and plant responses. CC reduced microbial diversity, functional gene abundance (KEGG/CAZy), and network connectivity. Fusarium oxysporum and Rhizoctonia solani were isolated from CC soils and were able to cause seed rot. Correlation-based clustering of metabolites and species-level taxa identified two cooperative clusters: the CR-enriched cluster was associated with beneficial microbes and contained metabolites such as rutin and oleanolic acid, whereas the CC-enriched cluster was dominated by chlorogenic acid and ferulic acid, which were positively correlated with pathogens. A metabolite–microbe subnetwork highlighted close associations between these phenolic acids and fungal taxa. The infection of E. senticosus by both pathogens was suppressed by low concentrations of chlorogenic acid, while plant growth was inhibited at high concentrations. Finally, we propose a hypothetical model of “pathogen invasion–metabolite accumulation–coexistence of resistance and autotoxicity,” providing metabolic targets for mitigating replanting obstacles in medicinal plant systems. These findings provide insights into the regulation of plant–microbe interactions and optimize medicinal plant cultivation.