Age-driven shifts in arbuscular mycorrhizal fungal communities associate with bioactive compound accumulation in Polygonum cuspidatum.

Arbuscular mycorrhizal fungi (AMF) play critical roles in plant secondary metabolism; however, their community dynamics across different growth years in medicinal plants such as Polygonum cuspidatum remain underexplored. This study investigated AMF community succession in the rhizosphere and roots of one-, two-, and four-year-old P. cuspidatum using high-throughput sequencing, quantified six bioactive compounds and soil nutrients, and analyzed transcript levels of resveratrol biosynthesis-related genes. Intraradical AMF colonization rates declined sharply with plant age. Rhizosphere AMF diversity peaked at two years, whereas root AMF diversity increased continuously with age. Glomus dominated the rhizosphere across all years, whereas root communities shifted from Glomus dominance to Paraglomus enrichment (peaking at two years), followed by a more diverse assemblage. Most bioactive compounds accumulated progressively with plant age, with resveratrol increasing nearly fourfold. The upstream gene PcPAL was strongly up-regulated in older roots, while several downstream genes peaked in one-year-old plants, indicating decoupled transcriptional regulation. Paraglomus in rhizosphere and Ambispora in roots exhibited positive association patterns with most bioactive compounds, while root-associated Paraglomus showed negative association patterns. Furthermore, Paraglomus and Ambispora showed positive correlation trends with most resveratrol biosynthesis-related genes, whereas Glomus was predominantly negatively correlated. Rhizosphere Glomus was positively associated with Olsen phosphorus, while Paraglomus exhibited positive associations with easily extractable glomalin-related soil protein. These findings demonstrate that plant age drives directional succession of AMF communities, and specific AMF taxa, particularly Paraglomus and Ambispora, may serve as candidate positive microbial indicators for bioactive compound accumulation in P. cuspidatum.