Characterization of a glycosyltransferase from Paris polyphylla for application in biosynthesis of rare ophiopogonins and ginsenosides

Phytochemistry. 2024 Sep:225:114173. doi: 10.1016/j.phytochem.2024.114173. Epub 2024 Jun 6.

Abstract

Saponins are bioactive components of many medicinal plants, possessing complicated chemical structures and extensive pharmacological activities, but the production of high-value saponins remains challenging. In this study, a 6'-O-glucosyltransferase PpUGT7 (PpUGT91AH7) was functionally characterized from Paris polyphylla Smith var. yunnanensis (Franch.) Hand. -Mazz., which can transfer a glucosyl group to the C-6' position of diosgenin-3-O-rhamnosyl-(1 → 2)-glucoside (1), pennogenin-3-O-rhamnosyl-(1 → 2)-glucoside (2), and diosgenin-3-O-glucoside (5). The KM and Kcat values of PpUGT7 towards the substrate 2 were 8.4 μM and 2 × 10-3 s-1, respectively. Through molecular docking and site-directed mutagenesis, eight residues were identified to interact with the sugar acceptor 2 and be crucial for enzyme activity. Moreover, four rare ophiopogonins and ginsenosides were obtained by combinatorial biosynthesis, including an undescribed compound ruscogenin-3-O-glucosyl-(1 → 6)-glucoside (10). Firstly, two monoglycosides 9 and 11 were generated using a known sterol 3-O-β-glucosyltransferase PpUGT80A40 with ruscogenin (7) and 20(S)-protopanaxadiol (8) as substrates, which were further glycosylated to the corresponding diglycosides 10 and 12 under the catalysis of PpUGT7. In addition, compounds 7-11 were found to show inhibitory effects on the secretion of TNF-α and IL-6 in macrophages RAW264.7. The findings provide valuable insights into the enzymatic glycosylation processes in the biosynthesis of bioactive saponins in P. polyphylla var. yunnanensis, and also serve as a reference for utilizing UDP-glycosyltransferases to construct high-value or rare saponins for development of new therapeutic agents.

Keywords: Biosynthesis; Ginsenosides; Glycosyltransferases; Melanthiaceae; Ophiopogonins; Paris polyphylla var. yunnanensis; Steroidal saponins.

MeSH terms

  • Animals
  • Ginsenosides* / biosynthesis
  • Ginsenosides* / chemistry
  • Ginsenosides* / metabolism
  • Glycosyltransferases* / chemistry
  • Glycosyltransferases* / metabolism
  • Liliaceae / chemistry
  • Melanthiaceae / chemistry
  • Melanthiaceae / enzymology
  • Melanthiaceae / metabolism
  • Mice
  • Molecular Docking Simulation
  • Molecular Structure
  • RAW 264.7 Cells
  • Saponins* / biosynthesis
  • Saponins* / chemistry
  • Saponins* / metabolism

Substances

  • Glycosyltransferases
  • Saponins
  • Ginsenosides