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Mirabilis himalaica is an endemic Tibetan medicinal plant distributed from the Western Himalaya to the Hengduan Mountains, highly regarded for its abundant flavonoids. Traditional knowledge holds that its medicinal properties vary considerably with geographic origin, yet the genetic and metabolic basis of this differentiation remains poorly understood. Here, we integrated plastome resequencing of 134 individuals from 23 populations with metabolomic and transcriptomic analyses of three representative sites to investigate population genetic variation and flavonoid metabolic differentiation. Pan-plastome revealed a typical quadripartite structure (154,232–154,422 bp) containing 113 unique genes across M. himalaica. A total of 620 SNVs, 171 indels, and four small inversions were identified from the pan-plastome, and further analyses based on these variants supported the delineation of four genetic lineages across all individuals. Overall genetic diversity was high (HT = 0.985, HS = 0.580), with majority variation occurring among groups (71.038%). Both IBD and IBE analyses found a significantly positive correlation between genetic distance and geographic and environmental distance (IBD: r = 0.348, p = 0.001; IBE: r = 0.219, p = 0.016). Flavonoids represented the most abundant metabolites (19.5%) and showed significantly higher accumulation in high-altitude populations, where key biosynthetic genes (e.g., CHS) were upregulated. Notably, these altitude-associated metabolic patterns were observed independently of the plastome-based genetic lineages. Together, we propose defining four evolutionary lineages as conservation units and prioritizing populations with unique haplotypes. This study provides critical genomic resources for provenance tracing, quality evaluation, and conservation management of this endangered Tibetan medicinal plant, and offers preliminary insights into the parallel patterns of pan-plastome variation and altitude-related metabolic differentiation, though without evidencing a direct causal link between them.
He et al. (Sat,) studied this question.