Multi-Omics Analysis Reveals Molecular Responses of Alkaloid Content Variations in Lycoris radiata Across Different Locations

The Amaryllidaceae geophyte Lycoris radiata is a primary botanical source of high-value medicinal alkaloids, including the Alzheimer’s therapeutic galanthamine. However, the accumulation of these compounds exhibits immense spatial and geographical variation. To elucidate the regulatory networks driving this divergence, we investigated three geographically distinct ecotypes (Hubei, HB; Guangxi, GX; Yunnan, YN) using an integrative multi-omics approach. Untargeted metabolomics revealed highly region-specific accumulation patterns of key alkaloids, such as galanthamine and lycorine. Interestingly, transcriptomic profiling uncovered a regional paradox: the Yunnan population exhibited the highest expression of core alkaloid biosynthetic genes despite possessing relatively lower target alkaloid contents, suggesting the involvement of post-transcriptional or environmental regulation. Furthermore, 16S and ITS amplicon sequencing of the rhizosphere revealed distinctly partitioned bacterial and fungal communities across regions, with the Yunnan ecotype exhibiting reduced diversity and highly specialized microbial taxa. Integrating these multi-omics datasets with 32 soil physicochemical indices demonstrated that trace metals and soil pH strongly correlated with local microbiome assembly. Mantel tests revealed that the environmental factors associated with the transcriptional activation of alkaloid biosynthetic genes were largely uncoupled from the factors correlating with terminal metabolite accumulation. Overall, this study details the profound region-specific transcriptomic, metabolomic, and micro-ecological variations in L. radiata , highlighting a complex environmental decoupling between genetic potential and final alkaloid accumulation.