Leaf development is associated with coupled metabolome-fungi trajectories in the phyllosphere of Panax ginseng

BACKGROUND: Leaf development underpins physiological performance and secondary metabolite accumulation, yet its influence on phyllosphere fungal communities in perennial medicinal plants such as ginseng (Panax ginseng C.A. Meyer) remains poorly understood. Understanding how developmental stage affects leaf chemistry and microbial assembly is important for linking plant metabolism with aboveground microbial ecology. RESULTS: We analyzed ginseng leaves across four developmental stages (S1-S4) using physiological measurements, ginsenoside profiling, untargeted metabolomics, ITS amplicon sequencing, fungal association networks, and metabolite-fungus correlations. Leaf physiological traits and ginsenoside content peaked at stage S2, representing a developmental optimum. Metabolomics revealed early enrichment of sugar phosphates, nucleotide metabolites, and membrane lipids, followed by late accumulation of raffinose-family oligosaccharides, phenylpropanoids, flavonoids, oxylipin-related lipids, and brassinosteroid-linked metabolites. Fungal richness and evenness increased from S1 to S4, with communities shifting from Ascomycota-dominated at early stages to Basidiomycota-enriched on senescing leaves. Fungal association networks showed stage-related increases in network size and changes in topological organization. Integrative analyses indicated that stage-specific metabolic changes were closely associated with fungal community succession, with amino acid, carbohydrate, lipid, flavonoid, and terpenoid pathways potentially linked to stage-specific fungal association patterns. CONCLUSIONS: Ginseng leaf development was accompanied by coordinated physiological and metabolic reprogramming that was associated with shifts in phyllosphere fungal composition and inferred association networks. These findings highlight leaf developmental stage as an important context for aboveground microbial dynamics and provide a framework for linking plant metabolism with microbial ecology in perennial crops, while emphasizing that causal relationships between specific metabolites and fungal taxa require further experimental validation.