PMID- 34756064 OWN - NLM STAT- MEDLINE DCOM- 20220223 LR - 20220223 IS - 2165-0497 (Electronic) IS - 2165-0497 (Linking) VI - 9 IP - 3 DP - 2021 Dec 22 TI - Enrichment of Burkholderia in the Rhizosphere by Autotoxic Ginsenosides to Alleviate Negative Plant-Soil Feedback. PG - e0140021 LID - 10.1128/Spectrum.01400-21 [doi] LID - e01400-21 AB - 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 (Rb(1), Rg(1), 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. FAU - Luo, Lifen AU - Luo L AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Wang, Luotao AU - Wang L AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Deng, Linmei AU - Deng L AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Mei, Xinyue AU - Mei X AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Liu, Yixiang AU - Liu Y AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Huang, Huichuan AU - Huang H AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Du, Fei AU - Du F AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Zhu, Shusheng AU - Zhu S AUID- ORCID: 0000-0003-0659-3794 AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. FAU - Yang, Min AU - Yang M AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. AD - Key Laboratory for Agro-Biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural Universitygrid.410696.c, Kunming, Yunnan, China. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20211110 PL - United States TA - Microbiol Spectr JT - Microbiology spectrum JID - 101634614 RN - 0 (Ginsenosides) RN - 0 (Glycosides) RN - 0 (RNA, Ribosomal, 16S) RN - Ilyonectria destructans SB - IM MH - Antibiosis/*physiology MH - Burkholderia/growth & development/*metabolism MH - Ginsenosides/*metabolism MH - Glycosides/metabolism MH - Hypocreales/*growth & development MH - Microbiota/physiology MH - Panax notoginseng/*microbiology MH - Plant Diseases/microbiology MH - Plants MH - RNA, Ribosomal, 16S/genetics MH - Rhizosphere MH - Soil Microbiology MH - Stress, Physiological/physiology PMC - PMC8579924 OTO - NOTNLM OT - autotoxicity OT - microbiological degradation OT - microbiome OT - plant disease OT - plant-microbe interactions OT - soilborne disease COIS- We declare no conflicts of interest. EDAT- 2021/11/11 06:00 MHDA- 2022/02/24 06:00 PMCR- 2021/11/10 CRDT- 2021/11/10 13:05 PHST- 2021/11/11 06:00 [pubmed] PHST- 2022/02/24 06:00 [medline] PHST- 2021/11/10 13:05 [entrez] PHST- 2021/11/10 00:00 [pmc-release] AID - 01400-21 [pii] AID - spectrum.01400-21 [pii] AID - 10.1128/Spectrum.01400-21 [doi] PST - ppublish SO - Microbiol Spectr. 2021 Dec 22;9(3):e0140021. doi: 10.1128/Spectrum.01400-21. Epub 2021 Nov 10.