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

Abstract

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.

Steroidal saponin profiles and their key genes for synthesis and regulation in Asparagus officinalis L. by joint analysis of metabolomics and transcriptomics

“…4 A B). This suggested that there is a conserved evolution of the CYP90 family gene in both monocotyledons and dicotyledons, in which these CYP90 genes may be evaluated from their common ancestor CYP90B, whose copies evolved with duplication followed by loss of function or neofunctionalization [ 10 , 22 ]. The CYP72A and CYP94D were predicted as S26H in several plants.…”

“…It is reported that, compared with leaves and rhizomes, almost all genes related to diosgenin synthesis were highly expressed in leaves of D. zingiberensis , suggesting that the diosgenin may have been synthesized in leaves (source), then converted into diosgenin saponins, and finally transported to its rhizomes (sink) for storage [ 22 ]. While in this study, most DSSP genes of green and purple asparagus are highly expressed in the Rs, which is consistent with the high accumulation of saponins in Rs.…”

Comparative transcriptome analysis reveals key genes for polyphyllin difference in five Paris species

“…Pennogenin‐type saponins (polyphyllin VI, polyphyllin VII, 17‐hydroxygracillin, and polyphyllin H) in leaves exerted a negative effect on the accumulation of diosgenin‐type saponins in rhizomes, implying a competitive relationship between these two kinds of steroidal saponins (Figure 2). According to previous research, cholesterol was proven to be the substrate for the biosynthesis of steroidal saponins and β ‐sitosterol might be the candidate intermediate for polyphyllin biosynthesis (Cheng et al, 2021; Li et al, 2022). Therefore, those sterols might be used to simultaneously biosynthesize both diosgenin‐type saponins and pennogenin‐type saponins, which may affect the resource allocation to these two kinds of metabolites.…”

Integrated evolutionary pattern analyses reveal multiple origins of steroidal saponins in plants

“…Together with orthologs of genes previously characterized to be involved in steroidal saponin biosynthesis in plants (Christ et al, 2019;Li et al, 2022Li et al, , 2023Moses et al, 2014;Yin et al, 2023;Zhou et al, 2022), our study resulted in a total of 211 genes made up SSAM in D. zingiberensis (Table S6). Based on the above results, we propose a steroidal saponin biosynthetic pathway in plants (Figure 2).…”

“…According to the methods previously reported (Augustin et al, 2012;Li et al, 2020Li et al, , 2022, we determined the content of steroidal saponins and their aglycone (diosgenin) in the samples treated by MeJA and drought, as well as 22 collected SSP species. Briefly, we performed metabolites analysis using the Vanquish ultra-high performance liquid chromatography coupled to a Q Exactive Hybrid Quadrupole-Orbitrap Mass Spectrometer (Thermo Scientific, Waltham, MA, USA).…”