Soil microbial legacy mediated by buckwheat flavonoids enhances cabbage resistance to clubroot disease

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. 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. 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.