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

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. 16b_bZ4HJNvGoZ2_HTzqi1Video Abstract