Autotoxic Ginsenoside Stress Induces Changes in Root Exudates to Recruit the Beneficial Burkholderia Strain B36 as Revealed by Transcriptomic and Metabolomic Approaches.

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.

Enrichment of Burkholderia in the Rhizosphere by Autotoxic Ginsenosides to Alleviate Negative Plant-Soil Feedback.

The accumulation of autotoxins and soilborne pathogens in soil was shown to be the primary driver of negative plant-soil feedback (NPSF). There is a concerted understanding that plants could enhance their adaptability to biotic or abiotic stress by modifying the rhizosphere microbiome. However, it is not clear whether autotoxins could enrich microbes to degrade themselves or antagonize soilborne pathogens. Here, we found that the microbiome degraded autotoxic ginsenosides, belonging to triterpenoid glycosides, and antagonized pathogens in the rhizosphere soil of Panax notoginseng (sanqi). Deep analysis by 16S rRNA sequencing showed that the bacterial community was obviously changed in the rhizosphere soil and identified the Burkholderia-Caballeronia-Paraburkholderia (BCP) group as the main ginsenoside-enriched bacteria in the rhizosphere soil. Eight strains belonging to the BCP group were isolated, and Burkholderia isolate B36 showed a high ability to simultaneously degrade autotoxic ginsenosides (Rb1, Rg1, and Rd) and antagonize the soilborne pathogen Ilyonectria destructans. Interestingly, ginsenosides could stimulate the growth and biofilm formation of B36, eventually enhancing the antagonistic ability of B36 to I. destructans and the colonization ability in the rhizosphere soil. In summary, autotoxic ginsenosides secreted by P. notoginseng could enrich beneficial microbes in the rhizosphere to simultaneously degrade autotoxins and antagonize pathogen, providing a novel ecological strategy to alleviate NPSF. IMPORTANCE 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. B36, eventually enhancing the antagonistic ability of Burkholderia sp. B36 to a soilborne pathogen and the colonization of B36 in soil. This ecological strategy could alleviate NPSF by manipulating the rhizosphere microbiome to simultaneously degrade autotoxins and antagonize pathogen.

Negative Plant-Soil Feedback Driven by Re-assemblage of the Rhizosphere Microbiome With the Growth of Panax notoginseng.

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.