Diosgenin saponins isolated from Dioscorea species such as Dioscorea zingiberensis exhibit a broad spectrum of pharmacological activities. Diosgenin, the aglycone of diosgenin saponins, is an important starting material for production of steroidal drugs. However, how plants produce diosgenin saponins, and the origin and evolution of diosgenin saponin biosynthetic pathway remain a mystery. Here, we report a high-quality, 629-Mb genome of D. zingiberensis anchored on 10 chromosomes with 30,322 protein-coding genes. We reveal that diosgenin is synthesized in leaves (“source”), then converted into diosgenin saponins, and finally transported to rhizomes (“sink”) for storage in plants. By evaluating the distribution and evolutionary patterns of diosgenin saponins in Dioscorea species, we find that diosgenin saponin-containing may be an ancestral trait in Dioscorea and is selectively retained. The results of comparative genomic analysis indicate that the tandem duplication coupled with a whole genome duplication event provide key evolutionary resources for the diosgenin saponin biosynthetic pathway in the D. zingiberensis genome. Furthermore, comparative transcriptome and metabolite analysis among 13 Dioscorea species suggest that specific gene expression patterns of pathway genes promote the differential evolution of the diosgenin saponin biosynthetic pathway in Dioscorea species. Our study provides important insights and valuable resources for further understanding the biosynthesis, evolution and utilization of plant specialized metabolites such as diosgenin saponins.

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