Abstract
BACKGROUND: Fungal communities play crucial roles in plant development and metabolite accumulation, especially in fully mycoheterotrophic medicinal plants like Gastrodia elata. While the importance of fungal symbiosis in G. elata is recognized, how fungal community dynamics evolve across its entire growth cycle and how they influence biomass and bioactive compound accumulation remain largely unclear. RESULTS: High-throughput sequencing combined with multi-omics analyses revealed that developmental progression significantly shapes fungal diversity and composition, thereby influencing biomass and metabolite accumulation in G. elata. These effects are mediated by stage-specific selective recruitment and dynamic remodeling of fungal communities in both rhizome and rhizosphere compartments. Structural equation modeling indicated that developmental stage, fungal α-diversity, and community structure exert both direct and indirect effects on biomass and the accumulation of bioactive compounds. High-resolution association network analyses further identified key functional fungal groups, particularly wood and soil saprotrophs, as major contributors to seed stem biomass regulation. Notably, the symbiotic fungus Armillaria showed the strongest positive correlation with gastrodin accumulation, while wood saprotrophs and plant pathogens also significantly influenced its levels. CONCLUSIONS: This study systematically elucidates the dynamic changes in fungal communities across different developmental stages of G. elata and their effects on biomass and bioactive metabolite accumulation. Our findings highlight the central role of microbe-plant-metabolite interactions in regulating biomass and bioactive metabolite production, offering valuable insight for optimizing the cultivation and quality of medicinal plants through microbiome-targeted strategies.