American ginseng (Panax quinquefolius L.) is an important cash crop, but long-term monoculture often results in serious root rot disease and yield reduction. The dynamics of soil phenolic acids perform an important function in soil microbe–plant interactions, but the extent to which changes in phenolic acids that occur under the continuous monoculture of American ginseng influence growth and the rhizosphere microbial community are unclear. In this study, American ginseng was planted in soil that had been used for 3 years of continuous monoculture (3 yr) and into a soil with no history of planting American ginseng (0 yr). Soil phenolic acids, rhizosphere microbiome characteristics, and pathogen suppression were analyzed. In the findings, the diversity and structure of the rhizosphere microbial community were affected by monoculture history, as the diversity of fungi and bacteria in 3 yr soil was higher than in 0 yr soil. The physiological performance of American ginseng in 3 yr soil was significantly lower than that in 0 yr soil. Soil phenolic acid contents decreased with the longer monoculture history, and high concentrations of phenolic acids suppressed the growth of American ginseng-specific pathogens. Soil phenolic acids appeared to modulate the pathogen population and the rhizosphere microbiome in American ginseng monocultures.

The infection of soil-borne diseases has the potential to modify root exudation and the rhizosphere microbiome. However, the extent to which these modifications occur in various monocropping histories remains inadequately explored. This study sampled healthy and diseased American ginseng (Panax quinquefolius L.) plants under 1–4 years of monocropping and analyzed the phenolic acids composition by HPLC, microbiome structure by high-throughput sequencing technique, and the abundance of pathogens by quantitative PCR. First, the fungal pathogens of Fusarium solani and Ilyonectria destructans in the rhizosphere soil were more abundant in the diseased plants than the healthy plants. The healthy American ginseng plants exudated more phenolic acid, especially p-coumaric acid, compared to the diseased plants after 1–2 years of monocropping, while this difference gradually diminished with the increase in monocropping years. The pathogen abundance was influenced by the exudation of phenolic acids, e.g., total phenolic acids (r = −0.455), p-coumaric acid (r = −0.465), and salicylic acid (r = −0.417), and the further in vitro test confirmed that increased concentration of p-coumaric acid inhibited the mycelial growth of the isolated pathogens for root rot. The healthy plants had a higher diversity of rhizosphere bacterial and fungal microbiome than the diseased plants only after a long period of monocropping. Our study has revealed that the cropping history of American ginseng has altered the effect of pathogens infection on rhizosphere microbiota and root exudation.