Habitat-specific modulation of sesquiterpenoid and polyacetylene biosynthesis in Atractylodes lancea (Thunb.) DC under understory cultivations: Implication for optimized plant morphology and bioactivity

Atractylodes lancea (Thunb.) DC is a Chinese herbal medicine with high medicinal value, and its dried rhizomes are widely utilized in traditional medicine. The primary active constituents of A. lancea include sesquiterpenoids and polyacetylenes, such as atractylodin, atractylon, and β-eudesmol. The preponderance of A. lancea available in the commercial market is cultivated in fields, resulting in diminished concentrations of active components and inconsistencies in the quality of the medicinal materials. Nonetheless, understory cultivation has been demonstrated to enhance the content of active components in A. lancea and to align its phenotypic characteristics more closely with those of the wild type. However, research on the molecular mechanisms underlying the formation of quality in A. lancea during understory cultivation remains limited. This study employed transcriptomic and metabolomic approaches to systematically investigate the gene expression and metabolite synthesis of A. lancea across diverse habitats. The results demonstrated that understory cultivation enhances farnesyl diphosphate (FPP) biosynthesis and increases the content of sesquiterpene-related metabolites by upregulating the expression of genes involved in terpene skeleton biosynthesis, while downregulating downstream sesquiterpene genes, such as FLDH, ICMT, and FNTA. Additionally, the content of atractylodin was elevated through the upregulation of FAB2 and FAD2 gene expression. In addition to identifying differentially expressed genes and metabolites, this study constructed the regulatory network between transcription factors, genes, and metabolites. Furthermore, it hypothesized the sesquiterpenoid biosynthetic pathway, exemplified by atractylon and β-eudesmol, as well as the polyacetylene biosynthetic pathway, represented by atractylodin. This study provides significant insights that will inform future, more detailed investigations into the biosynthetic pathways of A. lancea. It offers a theoretical foundation for understanding the "excellent shape and high quality" characteristics of A. lancea.