Ginsenosides in the Root Exudates of Ginseng Infected with Rusty Root Rot Improve the Infectivity of Pathogenic Ilyonectria Fungi

Rusty root rot of ginseng (Panax ginseng) caused by Ilyonectria spp. infection is a devastating soil-borne disease restricting the sustainable production of garden-cultivated ginseng (GCG) in Northeast China and causes severe yield and economic losses; GCG is far more susceptible to this pathogen than forest-cultivated ginseng (Lin-Xia-Shan-Shen, LXSS). Ginsenosides, the signature triterpenoid saponin defensive metabolites of ginseng, are characteristic dammarane-type triterpenoid defensive saponins represented by Re, Rg2, Rb1, Rd, and Rg1. These compounds are continuously secreted into the rhizosphere and widely participate in plant–microbe interactions, yet their functional roles in mediating Ilyonectria infection remain poorly clarified. This study aimed to clarify how rhizospheric ginsenosides regulate the infection process of pathogenic Ilyonectria strains. Two pathogenic strains, Ilyonectria sp. SYM-1 and Ilyonectria sp. SYM-2, were found isolated from diseased GCG roots and verified as causal agents via morphological observation, molecular ITS identification and artificial inoculation infection experiments. Interestingly, the concentrations of five ginsenosides, Re, Rg2, Rb1, Rd, and Rg1, in the rhizospheric soil of GCG with rusty root rot were significantly higher than those in the rhizospheric soil of healthy LXSS plants. In addition, the concentrations of ginsenosides in the LXSS rhizospheric soils decreased with increasing age of plants. Non-nutritive suspension co-culture assays showed that high concentrations of the ginsenosides Rg1 and Rd significantly promoted spore germination of the strains SYM-1 and SYM-2. However, Rb1 had a certain inhibitory effect on the growth of Ilyonectria sp. SYM-2. Host inoculation experiments further indicated that infection with either fungus significantly reduced the concentrations of ginsenosides produced in ginseng roots. These results demonstrate that the pathogenic fungi SYM-1 and SYM-2 of Ilyonectria can adapt to and utilize ginsenosides. Collectively, these findings prove that the two pathogenic Ilyonectria strains have evolved the capacity to adapt to and exploit rhizospheric ginsenosides to facilitate their infectivity. From an application perspective, reducing rhizospheric ginsenoside release may represent a promising theoretical strategy for ginseng cultivation and germplasm improvement, which warrants further verification by field or greenhouse experiments for validation.