PMID- 36445116 OWN - NLM STAT- MEDLINE DCOM- 20221227 LR - 20231020 IS - 2165-0497 (Electronic) IS - 2165-0497 (Linking) VI - 10 IP - 6 DP - 2022 Dec 21 TI - Foliar Pathogen Infection Manipulates Soil Health through Root Exudate-Modified Rhizosphere Microbiome. PG - e0241822 LID - 10.1128/spectrum.02418-22 [doi] LID - e02418-22 AB - Negative plant-soil feedback (NPSF) due to the buildup of soilborne pathogens in soil is a major obstacle in sustainable agricultural systems. Beneficial rhizosphere microfloras are recruited by plants, and mediating this has become a strategic priority to manipulate plant health. Here, we found that foliar infection of Panax notoginseng by Alternaria panax changed plant-soil feedback from negative to positive. Foliar infection modified the rhizosphere soil microbial community and reversed the direction of the buildup of the soilborne pathogen Ilyonectria destructans and beneficial microbes, including Trichoderma, Bacillus, and Streptomyces, in rhizosphere soil. These beneficial microbes not only showed antagonistic ability against the pathogen I. destructans but also enhanced the resistance of plants to A. panax. Foliar infection enhanced the exudation of short- and long-chain organic acids, sugars, and amino acids from roots. In vitro and in vivo experiments validated that short- and long-chain organic acids and sugars play dual roles in simultaneously suppressing pathogens but enriching beneficial microbes. In summary, foliar infection could change root secretion to drive shifts in the rhizosphere microbial community to enhance soil health, providing a new strategy to alleviate belowground disease in plants through aboveground inducement. IMPORTANCE Belowground soilborne disease is the main factor limiting sustainable agricultural production and is difficult to manage due to the complexity of the soil environment. Here, we found that aboveground parts of plants infected by foliar pathogens could enhance the secretion of organic acids, sugars, and amino acids in root exudates to suppress soilborne pathogens and enrich beneficial microbes, eventually changing the plant and soil feedback from negative to positive and alleviating belowground soilborne disease. This is an exciting strategy by which to achieve belowground soilborne disease management by manipulating the aboveground state through aboveground stimulation. 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Zhang, Junxing AU - Zhang J AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Ye, Chen AU - Ye C AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Li, Su AU - Li S AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Duan, Shengshuang AU - Duan S AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Wang, Zhengping AU - Wang Z AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - Deng, Weiping AU - Deng W AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. FAU - He, Xiahong AU - He X AD - State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, 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, China. AD - Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. AD - National Engineering Research Center for Applied Technology of Agricultural Biodiversity, College of Plant Protection, Yunnan Agricultural Universitygrid.410696.c, Kunming, China. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20221129 PL - United States TA - Microbiol Spectr JT - Microbiology spectrum JID - 101634614 RN - 0 (Soil) RN - 0 (Amino Acids) SB - IM MH - *Soil/chemistry MH - Rhizosphere MH - Plant Roots MH - Soil Microbiology MH - *Microbiota/physiology MH - Exudates and Transudates MH - Plants MH - Amino Acids PMC - PMC9769671 OTO - NOTNLM OT - Alternaria panax OT - Ilyonectria destructans OT - plant-soil feedback OT - plant-soil interaction OT - rhizosphere microbiome OT - root exudates OT - soilborne disease COIS- The authors declare no conflict of interest. EDAT- 2022/11/30 06:00 MHDA- 2022/12/28 06:00 PMCR- 2022/11/29 CRDT- 2022/11/29 09:05 PHST- 2022/11/30 06:00 [pubmed] PHST- 2022/12/28 06:00 [medline] PHST- 2022/11/29 09:05 [entrez] PHST- 2022/11/29 00:00 [pmc-release] AID - 02418-22 [pii] AID - spectrum.02418-22 [pii] AID - 10.1128/spectrum.02418-22 [doi] PST - ppublish SO - Microbiol Spectr. 2022 Dec 21;10(6):e0241822. doi: 10.1128/spectrum.02418-22. Epub 2022 Nov 29.