Multi-omics and in silico assessment of ecological risks posed by agrochemical coatings: Disruption of rhizosphere stress signaling and induction of bulb rot in Fritillaria cirrhosa

Agrochemical seed coatings are widely used to control soil-borne pathogens. However, their unintended ecological effects on rhizosphere interactions and plant health remain unclear. Here, we combined a field transplantation trial, multi-omics analyses, and molecular docking to investigate the effects of fungicide-based seed coatings on the rhizosphere microecology of Fritillaria cirrhosa.The field trial showed that coating treatment unexpectedly increased bulb rot incidence by 2.8-fold compared with untreated controls (P < 0.001). Multi-omics analyses further indicated that coating application disrupted rhizosphere microecology, as evidenced by a 25.1% decline in bacterial diversity, reduced network complexity, and enrichment of pathogenic Fusarium species. Metabolomic analysis revealed the accumulation of exogenous xenobiotics along with downregulation of pyrimidine metabolism pathway, suggesting altered plant-microbe chemical communication. Stress-related metabolites, including salicylic acid (SA), L-carnitine, and ethylmalonate, accumulated, whereas key signaling molecules, such as adenosine, monoacylglycerol (18:3), Lysophosphatidylethanolamine 15:1 were depleted (0.03-fold) in the treatment group. Moreover, the decrease in jasmonic acid coupled with an increase in SA suggests immune hijacking associated with necrotrophic pathogens such as Fusarium, a pathological cascade further supported by the accumulation of mycotoxins such as T-2 triol. Cross-domain network and molecular docking analyses further clarified interactions between hub metabolites and the microbial community. Notably, adenosine exhibited strong binding affinities (< -6.0 kcal/mol) to both plant defense-related proteins (JOX2 and CotA laccase) and fungal pathogenicity targets, indicating a key role for endogenous plant defense signals in maintaining rhizosphere ecological balance. Collectively, these findings provide robust correlative evidence linking agrochemical seed coatings to rhizosphere microecological dysbiosis, characterized by reduced metabolite-mediated recruitment of beneficial microbiota and disrupted interkingdom signaling. This pathogen-favoring environment highlights the often-overlooked ecological impacts of seed coatings and underscores the urgent need for microbiome-compatible disease management strategies in perennial bulbous crop production.