Jiabing Wu, Shilin Hu, Jing Chen, Lili Zhou, Shengdie Yang, Na Zhou, Lei Wu, Guoqing Niu, Yong Zhang, Xuesong Ren, Qinfei Li, Jun Yuan, Hongyuan Song, Jun Si
{"title":"Soil microbial legacy mediated by buckwheat flavonoids enhances cabbage resistance to clubroot disease.","authors":"Jiabing Wu, Shilin Hu, Jing Chen, Lili Zhou, Shengdie Yang, Na Zhou, Lei Wu, Guoqing Niu, Yong Zhang, Xuesong Ren, Qinfei Li, Jun Yuan, Hongyuan Song, Jun Si","doi":"10.1186/s40168-025-02166-y","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>The legacy of plant growth significantly impacts the health of subsequent plants, yet the mechanisms by which soil legacies in crop rotation systems influence disease resistance through rhizosphere plant-microbiome interactions remain unclear. Using a buckwheat-cabbage rotation model, we investigated how microbial soil legacies shape cabbage growth and clubroot disease resistance.</p><p><strong>Results: </strong>Three-year field trials revealed that buckwheat rotation sustainably reduced clubroot severity by 67%-97%, regardless of pathogen load. Soil sterilization eliminated this suppression, implicating a microbial basis. Using 16S rRNA sequencing, we identified buckwheat-enriched bacterial taxa (Microbacterium, Stenotrophomonas, Ralstonia) that colonized subsequent cabbage roots. Metabolomic profiling pinpointed buckwheat root-secreted flavonoids - 6,7,4'-trihydroxyisoflavone and 7,3',4'-trihydroxyflavone - as key drivers of microbial community restructuring. These flavonoids synergistically enhanced the efficacy of a synthetic microbial community (SynCom1, containing Microbacterium keratanolyticum, Stenotrophomonas maltophilia, and Ralstonia pickettii), boosting disease suppression by 34% in greenhouse trials. Co-application of flavonoids and SynCom1 improved bacterial colonization in root niches. Although SynCom1 partially activated jasmonic acid (JA)-associated defenses, its effectiveness depended primarily on flavonoid-driven microbial recruitment rather than direct immune induction.</p><p><strong>Conclusions: </strong>Buckwheat rotation induces flavonoid-mediated soil microbiomes that prime JA-dependent immunity in subsequent cabbage crops, thereby decoupling disease severity from pathogen load. This study elucidates how specialized metabolites orchestrate cross-crop microbial legacies for sustainable disease control, providing a blueprint for designing rotation systems through precision microbiome engineering. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"13 1","pages":"176"},"PeriodicalIF":12.7000,"publicationDate":"2025-07-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12309073/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-025-02166-y","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: The legacy of plant growth significantly impacts the health of subsequent plants, yet the mechanisms by which soil legacies in crop rotation systems influence disease resistance through rhizosphere plant-microbiome interactions remain unclear. Using a buckwheat-cabbage rotation model, we investigated how microbial soil legacies shape cabbage growth and clubroot disease resistance.
Results: Three-year field trials revealed that buckwheat rotation sustainably reduced clubroot severity by 67%-97%, regardless of pathogen load. Soil sterilization eliminated this suppression, implicating a microbial basis. Using 16S rRNA sequencing, we identified buckwheat-enriched bacterial taxa (Microbacterium, Stenotrophomonas, Ralstonia) that colonized subsequent cabbage roots. Metabolomic profiling pinpointed buckwheat root-secreted flavonoids - 6,7,4'-trihydroxyisoflavone and 7,3',4'-trihydroxyflavone - as key drivers of microbial community restructuring. These flavonoids synergistically enhanced the efficacy of a synthetic microbial community (SynCom1, containing Microbacterium keratanolyticum, Stenotrophomonas maltophilia, and Ralstonia pickettii), boosting disease suppression by 34% in greenhouse trials. Co-application of flavonoids and SynCom1 improved bacterial colonization in root niches. Although SynCom1 partially activated jasmonic acid (JA)-associated defenses, its effectiveness depended primarily on flavonoid-driven microbial recruitment rather than direct immune induction.
Conclusions: Buckwheat rotation induces flavonoid-mediated soil microbiomes that prime JA-dependent immunity in subsequent cabbage crops, thereby decoupling disease severity from pathogen load. This study elucidates how specialized metabolites orchestrate cross-crop microbial legacies for sustainable disease control, providing a blueprint for designing rotation systems through precision microbiome engineering. 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.