Haplotype-resolved genome and population genomics provide insights into dioscin biosynthesis and evolutionary history of the medicinal species Dioscorea nipponica

Dioscorea nipponica, a perennial herb widely distributed in the Sino-Japanese Floristic Region, is renowned for its medicinal properties, particularly its ability to produce dioscin. Here, we present a haplotype-resolved genome assembly of the diploid D. nipponica, comprising 511.41 Mb for Haplotype A and 498.29 Mb for Haplotype B, each organized into 10 chromosomes. The two haplotypes exhibited high similarity, with only 2.75% of the allelic genes exhibiting specific expression. Key genes in the dioscin biosynthesis pathway were identified, and expression analysis revealed that the majority (16/21) of genes involved in the first two stages were highly expressed in rhizomes. Notably, significant expansion of the CYP90, CYP94, and UGT73 gene families was observed in dioscin-producing species, highlighting their critical roles in dioscin biosynthesis. Additionally, genome size estimation and population genomic analyses of diverse D. nipponica accessions identified four principal clades in D. nipponica, corresponding to diploid, di-tetra-octoploid, tetraploid, and hexaploid accessions from various geographic regions, with clade A (diploids) further divided into five subclades. Demographic analysis of the diploid D. nipponica revealed a prolonged decline in effective population size from the Pleistocene to the Last Glacial Maximum, with population splits occurring during the mid-to-late Pleistocene. Selective sweep analysis identified key genes, including HD-Zip I, ADH1, SMT1, and CYPs that may contribute to adaptation to high-latitude environments and the geographical variations in dioscin content. Overall, this study enhances our understanding of the genomic architecture, biosynthetic pathways, and evolutionary dynamics of D. nipponica, providing valuable insights into its medicinal potential and evolution.