Metabolic landscape of panax ginseng under forest cultivation across multiple growth years: Associations with soil microbiota and regulatory networks governing ginsenoside accumulation

This study unveils the rhizosphere microbiome-driven cascading mechanism governing ginsenoside biosynthesis in Ginseng Under Forest across a 9–24 year growth cycle through integrated multi-omics analysis. Key findings reveal: (1) Rhizosphere microbiota undergoes predictable succession, forming four functional phases: organic matter-degrading consortia (e.g., Vicinamibacteraceae) at ≤ 9 years; a Chloroflexi bacterium HSB_OF53-F07 and Acidobacteria Subgroup_2 co-dominated degradation bottleneck phase at 12 years; Actinobacteria-enriched symbiotic communities (e.g., MB-A2–108) at 15–18 years; and ginsenoside-synthesizing functional consortia (Gemmatimonadota and Acidobacteriae) at maturity (24 years). (2) These microbiota remodel host metabolic landscapes by elevating lipid/nitrogen compounds—notably benzoate derivatives (e.g., Benzoicacid+1 O,O-Hex) and aspartate—which subsequently activate biosynthesis pathways for rare ginsenosides Rg5 (effect loading: 0.952) and F3 (0.857). (3) Structural equation modeling quantified microbial dominance: microbiota exerted the highest total effect on ginsenoside accumulation (0.849, explaining 73.3 % variance), with metabolites exhibiting dual roles—serving as precursors (direct microbial effect: 0.72) while imposing feedback inhibition on biosynthesis (path coefficient: –0.156). This work establishes a theoretical foundation for quality optimization in ginseng under forest cultivation. • Rhizosphere succession (9-24 yr) steers host metabolism to elevate rare ginsenosides (Rg5, F3). • Four functional phases identified: decomposer (9y), bottleneck (12y), symbiotic (15-18y), and synthesizer (24y). • Microbiota dominates synthesis (total effect: 0.849), with metabolites acting as both precursors and inhibitors.