Apple replant disease (ARD) is a major threat to the sustainable development of China’s apple industry. It is primarily caused by the accumulation of phloridzin and the pathogen Fusarium proliferatum f.sp. malus domestica MR5 (Fpmd MR5). MdUGT88F1-mediated phloridzin biosynthesis is known to enhance disease resistance, but its role in shaping the rhizosphere microbiome and conferring resistance against Fpmd MR5 remains unclear. In this study, we used wild-type (WT) and MdUGT88F1 transgenic apple lines to systematically investigate the mechanism by which MdUGT88F1 regulates the rhizosphere microbiome to mitigate ARD. Compared with WT and MdUGT88F1-OE plants, MdUGT88F1-RNAi plants exhibited enhanced tolerance to ARD, as indicated by reduced disease severity, decreased abundance of Fpmd MR5 in the rhizosphere soil, and lower phloridzin content. Further greenhouse experiments demonstrated that the rhizosphere bacterial communities were triggered mainly by changes in community composition. Multi-omics joint analysis revealed that members of the family Bacillaceae with multiple plant growth-promoting traits were enriched in the MdUGT88F1-RNAi plant rhizosphere but only upon Fpmd MR5 invasion. MdUGT88F1-RNAi plants exhibited significantly higher exudation of D-tagatose, D-galactose, sucrose, 3-O-methyl-D-glucose, and maltitol. Interestingly, exogenous application of these compounds promoted the proliferation of Bacillus, enhancing plant resistance to Fpmd MR5. In vitro assays demonstrated that the recruited Bacillus significantly inhibited the hyphal growth and fumonisin B1 production of Fpmd MR5 and alleviated plant disease symptoms. We experimentally validated this observation by inoculating a synthetic microbial community (Bacillus velezensis, Bacillus mojavensis, Bacillus subtilis, Bacillus amyloliquefaciens, and Bacillus licheniformis) into replanted soil, which led to a significant reduction in pathogen Fusarium abundance and promoted plant growth. Overall, these findings highlight that plant disease resistance is a complex trait driven by dynamic interactions among the host genetic background, rhizospheric microbial communities, and pathogens. Targeted modulation of the rhizospheric microbiome represents a potent “prebiotic” strategy. This approach can indirectly enhance plant disease resistance by fostering beneficial microbial activity in the rhizosphere. This study also provides a theoretical basis and practical solutions for the green control of ARD through prebiotics and synthetic microbial communities.
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