Succinic acid reduces tomato bacterial wilt disease by recruiting Sphingomonas sp

BACKGROUND: Root exudates are key mediators in maintaining plant health by mediating interactions with the rhizosphere microbiome. Plants release specific exudates to defend against pathogens, either directly by inhibiting pathogen growth or indirectly through alterations in the microbial community. However, the mechanisms by which root exudates influence the rhizosphere microbiome to enhance plant resistance remain poorly understood. In this study, we evaluated the effects of 23 root exudates on the growth of the pathogen Ralstonia solanacearum and tomato bacterial wilt. RESULTS: Seventeen of the exudates reduced the disease index, with most having neutral or even promotive effects on R. solanacearum growth. Notably, succinic acid (SA) completely suppressed bacterial wilt without directly affecting the pathogen or tomato plants in the absence of the rhizosphere microbiome. We further explored the impact of SA on the rhizosphere bacterial community in both tomato rhizosphere and bulk soil. Only the bacterial community in the rhizosphere responded significantly to SA addition, with indicator species and network analyses identifying Sphingomonas sp. WX113 as the key taxa associated with this response. A subsequent greenhouse experiment showed that co-applying Sphingomonas sp. WX113 with SA achieved 100% biocontrol efficiency, outperforming either treatment alone. In vitro assays further demonstrated that SA enhanced the antagonistic activity of Sphingomonas sp. WX113 against R. solanacearum. CONCLUSIONS: Our findings emphasize the host-mediated role of root exudates, such as succinic acid, in selectively promoting beneficial Sphingomonas sp., thereby enhancing plant resistance to bacterial wilt. These results offer new perspectives on the combination of beneficial microbes and their matching compounds for soil-borne diseases management.