The genome of <i>Dioscorea zingiberensis</i> sheds light on the biosynthesis, origin and evolution of the medicinally important diosgenin saponins

Abstract

Diosgenin saponins isolated from <i>Dioscorea</i> species such as <i>D. zingiberensis</i> exhibit a broad spectrum of pharmacological activities. Diosgenin, the aglycone of diosgenin saponins, is an important starting material for the production of steroidal drugs. However, how plants produce diosgenin saponins and the origin and evolution of the diosgenin saponin biosynthetic pathway remain a mystery. Here we report a high-quality, 629-Mb genome of <i>D</i>. <i>zingiberensis</i> 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 <i>Dioscorea</i> species, we find that diosgenin saponin-containing may be an ancestral trait in <i>Dioscorea</i> and is selectively retained. The results of comparative genomic analysis indicate that tandem duplication coupled with a whole-genome duplication event provided key evolutionary resources for the diosgenin saponin biosynthetic pathway in the <i>D</i>. <i>zingiberensis</i> genome. Furthermore, comparative transcriptome and metabolite analysis among 13 <i>Dioscorea</i> species suggests that specific gene expression patterns of pathway genes promote the differential evolution of the diosgenin saponin biosynthetic pathway in <i>Dioscorea</i> 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.