Multi-omics reveals accumulation mechanisms underlying differences in sesquiterpenoid content across different growth environments of Atractylodes macrocephala rhizome

This study aimed to explore mechanisms driving differential sesquiterpenoid accumulation in Atractylodes macrocephala rhizome (AMR) under different growth environments. Root and rhizosphere soil samples were collected from wild, imitated wild, one- and two-year cultivated AMR. Combined metabolomic, transcriptomic and microbiomic profiling was carried out to investigate alterations in sesquiterpenoid levels, root-associated microbiota, and terpenoid biosynthetic genes under different growth environments. Metabolomics revealed that wild AMR exhibited higher pyruvate consumption and accumulated more atractylone and atractylenolides. Transcriptomic analysis demonstrated that the genes encoding key MEP pathway enzymes (DXS, DXR, MCT, HDS) and the genes encoding the sesquiterpenoid biosynthetic enzyme GDS were significantly upregulated in wild AMR. In contrast, the genes encoding triterpenoid synthetic enzymes (SQS, SQE, {beta}-AS) were downregulated, redirecting metabolic precursors toward sesquiterpenoid synthesis. Microbial community structures differed substantially across groups. Further analysis suggested rhizosphere microorganisms were important contributors to AMR medicinal quality, and sesquiterpenoid metabolites accumulated in AMR roots, together with the rhizosphere microenvironment, jointly shape specific rhizosphere fungal assembly. This study systematically revealed the synergistic regulatory relationships among sesquiterpenoids metabolism, gene expression, growth environment, and root-associated microbes, providing multi-omics evidence for clarifying the mechanism by which these factors coordinately regulate the quality of AMR.