Soil microbial legacy mediated by buckwheat flavonoids enhances cabbage resistance to clubroot disease
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
Affiliations
Jiabing Wu
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Shilin Hu
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Jing Chen
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Lili Zhou
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Shengdie Yang
Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving fertilizers, Nanjing Agricultural University
Na Zhou
Chongqing Academy of Agricultural Sciences
Lei Wu
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Guoqing Niu
College of Agronomy and Biotechnology, Southwest University
Yong Zhang
College of Resources and Environment, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University
Xuesong Ren
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Qinfei Li
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Jun Yuan
Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Wastes, Educational Ministry Engineering Center of Resource-saving fertilizers, Nanjing Agricultural University
Hongyuan Song
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
Jun Si
College of Horticulture and Landscape Architecture, Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River, Ministry of Education, Key Laboratory of Plant Hormones and Molecular Breeding of Chongqing, Southwest University
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
