There is a concerted understanding of the accumulation of soil pathogens as the major driving factor of negative plant-soil feedback (NPSF). However, our knowledge of the connection between plant growth, pathogen build-up and soil microbiome assemblage is limited. In this study, significant negative feedback between the soil and sanqi ( Panax notoginseng ) was found, which were caused by the build-up of the soil-borne pathogens Fusarium oxysporum , F. solani , and Monographella cucumerina . Soil microbiome analysis revealed that the rhizospheric fungal and bacterial communities were changed with the growth of sanqi. Deep analysis of the phylum and genus levels corroborated that rhizospheric fungal Ascomycota, including the soil-borne pathogens F. oxysporum , F. solani , and especially M. cucumerina , were significantly enriched with the growth of sanqi. However, the bacteria Firmicutes and Acidobacteria, including the genera Pseudomonas , Bacillus, Acinetobacter and Burkholderia , were significantly suppressed with the growth of sanqi. Using microbial isolation and in vitro dual culture tests, we found that most isolates derived from the suppressed bacterial genera showed strong antagonistic ability against the growth of sanqi soil-borne pathogens. Interestingly, inoculation of these suppressed isolates in consecutively cultivated soil could significantly alleviate NPSF. In summary, sanqi growth can suppress antagonistic bacteria through re-assemblage of the rhizosphere microbiome and cause the accumulation of soil-borne pathogens, eventually building negative feedback loops between the soil and plants.

Autotoxic ginsenosides, secreted by sanqi into soil, could enrich Burkholderia sp. to alleviate negative plant-soil feedback (NPSF) by degrading autotoxins and antagonizing the root rot pathogen. In detail, ginsenosides could stimulate the growth and biofilm formation of Burkholderia sp.

Plants can recruit beneficial microbes to help improve their fitness under abiotic or biotic stress. Our previous studies found that Panax notoginseng could enrich beneficial Burkholderia sp. B36 in the rhizosphere soil under autotoxic ginsenoside stress. Here, we clarified that ginsenoside stress activated the phenylpropanoid biosynthesis and α-linolenic acid metabolism pathways of roots to increase the secretion of cinnamic acid, 2-dodecenoic acid, and 12-oxo-phytodienoic acid. These metabolites could promote the growth of B36. Importantly, cinnamic acid could simultaneously promote the chemotaxis and growth of B36, enhance the colonization of B36 in the rhizosphere, and eventually increase the survival rate of P. notoginseng. Overall, the plants could promote the growth and colonization of beneficial bacteria through key metabolites in root exudates under autotoxin stress. This finding will facilitate the practical application of beneficial bacteria in agricultural production and lead to successful and reproducible biocontrol efficacy by the exogenous addition of key metabolites.