{"title":"MdUGT88F1 enhances plant resistance to Fusarium proliferatum f.sp. malus domestica MR5 via root exudate-mediated assembly of disease-suppressive rhizosphere microbiota.","authors":"Yanan Duan, Ziqing Ma, Yiting Liu, Yiwei Jia, Zhijun Zhang, Chao Yang, Xiaoqing Gong, Zhiquan Mao, Chao Li, Fengwang Ma","doi":"10.1186/s40168-026-02416-7","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>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.</p><p><strong>Results: </strong>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.</p><p><strong>Conclusion: </strong>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. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":" ","pages":""},"PeriodicalIF":12.7000,"publicationDate":"2026-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-026-02416-7","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: 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.
Results: 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.
Conclusion: 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. Video Abstract.
期刊介绍：
Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
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