Multi-omics reveals the molecular regulatory mechanisms underlying the formation of geo-authentic quality in Chrysanthemum morifolium ‘Chuju’

Chrysanthemum morifolium ‘ Chuju ’ (CJ), a renowned traditional Chinese medicinal herb, has a history of widespread use spanning over 3000 years. Although prior studies have indicated that medicinal plants cultivated in geo-authentic production areas tend to exhibit superior quality compared with those from non-genuine regions, the regulatory mechanisms underlying this divergence remain incompletely characterized. Here, inflorescences and rhizosphere soil samples of CJ were collected from three production regions - Chuzhou (CZ), Hefei (HF), and Bozhou (BZ) - and subjected to integrated metabolomic, transcriptomic, and microbiota analyses. The results suggest that the chemical signatures delineating the geo-authenticity of CJ, as reflected by elevated levels of total flavonoids, total phenolic acids, and flavor-associated amino acids, are closely correlated with the origin-specific soil microenvironment. The weakly acidic, nitrogen-rich, and organic-matter-abundant soil characteristic of the CZ production area appeared to selectively favor the enrichment of distinct rhizosphere microbial assemblages, with Actinomycetota and Arthrobacter as the predominant taxa. Integrative transcriptomic and metabolomic profiling further indicated that this rhizosphere microenvironment was accompanied by specific expression patterns in the phenylpropanoid biosynthetic pathway of CJ: genes including 4CL , F3H , and FLS exhibited upregulated expression, coinciding with elevated accumulation of highly bioactive flavonols such as nicotiflorin and astragalin. By contrast, under the alkaline soil conditions prevailing in the BZ production area, sucrose-related metabolites tended to accumulate to a greater extent, whereas flavonoid metabolite levels remained comparatively low. Multi-omics network analysis further uncovered two principal environmental association patterns: soil available nitrogen content was correlated with the enrichment of beneficial microbial groups and the upregulation of flavonoid biosynthetic genes, whereas soil pH was linked to the accumulation of stress-responsive metabolites and a potential shift in carbon metabolic direction. Taken together, these findings contribute to a multi-level “soil-microbe-plant” association framework that characterizes the formation of geo-authentic quality in CJ. This framework may serve as a data-driven reference for elucidating the mechanisms of geo-authenticity in medicinal plants and for informing their ecological cultivation.