Skip to main content
Log in

Functional Characterization of a Novel Glycosyltransferase (UGT73CD1) from Iris tectorum Maxim. for the Substrate promiscuity

  • Original Paper
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Glycosylflavonoids are a class of natural products with multiple pharmacological activities and a lot of glycosyltransferases from various plant species have been reported that they were involved in the biosynthesis of these phytochemicals. However, no corresponding glycosyltransferase has been identified from the famous horticultural and medicinal plant Iris tectorum Maxim. Here, UGT73CD1, a novel glycosyltransferase, was identified from I. tectorum. based on transcriptome analysis and functional identification. Phylogenetic analysis revealed that UGT73CD1 grouped into the clade of flavonoid 7-OH OGTs. Biochemical analysis showed that UGT73CD1 was able to glycosylate tectorigenin at 7-OH to produce tectoridin, and thus assigned as a 7-O-glycosyltransferase. In addition, it also possessed robust catalytic promiscuity toward 12 structurally diverse flavonoid scaffolds and 3, 4-dichloroaniline, resulting in forming O- and N-glycosides. This work will provide insights into efficient biosynthesis of structurally diverse flavonoid glycosides for drug discovery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Nabavi, S. M., Šamec, D., Tomczyk, M., Milella, L., Russo, D., Habtemariam, S., & Xu, S. W. (2020). Flavonoid biosynthetic pathways in plants: versatile targets for metabolic engineering. Biotechnology Advances, 38, 107316.

    Article  CAS  Google Scholar 

  2. Moharram, F. A., Nagy, M. M., El-Dib, R. A., El-Tantawy, M. M., El-Hossary, G. G., & El-Hosari, D. G. (2021). Pharmacological activity and flavonoids constituents of Artemisia judaica L aerial parts. Journal of Ethnopharmacology, 270, 1137.

    Article  Google Scholar 

  3. Kawser, H. M., Abdal, D. A., Han, J., Yin, Y., Kim, K., Kumar, S. S., & Cho, S. G. (2016). Molecular mechanisms of the anti-obesity and anti-diabetic properties of flavonoids. International Journal of Molecular Sciences, 17, 569.

    Article  Google Scholar 

  4. Dai, Y., Zhang, S. S., Liu, D. C., Li, H. M., Ma, T., Huo, Q., & Wu, C. Z. (2018). Enzymatic biosynthesis of novel bavachin glucosides via Bacillus UDP-glycosyltransferase. Phytochemistry Letters, 23, 9–14.

    Article  CAS  Google Scholar 

  5. Xiao, J., Capanoglu, E., Jassbi, A. R., & Miron, A. (2016). Advance on the flavonoid C-glycosides and health benefits. Critical Reviews in Food Science and Nutrition, 56(sup1), S29–S45.

    Article  CAS  Google Scholar 

  6. Cheynier, V., Comte, G., Davies, K. M., Lattanzio, V., & Martens, S. (2013). Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry, 72, 1–20.

    Article  CAS  Google Scholar 

  7. Li, J., Liu, X., Gao, Y., Zong, G., Wang, D., Liu, M. Z., & Shen, Y. Q. (2019). Identification of a UDP-glucosyltransferase favouring substrate-and regio-specific biosynthesis of flavonoid glucosides in Cyclocarya paliurus. Phytochemistry, 163, 75–88.

    Article  CAS  Google Scholar 

  8. Hostetler, G. L., Ralston, R. A., & Schwartz, S. J. (2017). Flavones: Food sources, bioavailability, metabolism, and bioactivity. Advances in Nutrition, 8, 423–435.

    Article  CAS  Google Scholar 

  9. Liang, D. M., Liu, J. H., Wu, H., Wang, B. B., Zhu, H. J., & Qiao, J. J. (2015). Glycosyltransferases: Mechanisms and applications in natural product development. Chemical Society Reviews, 44, 8350–8374.

    Article  CAS  Google Scholar 

  10. Jones, P., Messner, B., Nakajima, J., Schäffner, A. R., & Saito, K. (2003). UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. Journal of Biological Chemistry, 278, 43910–43918.

    Article  CAS  Google Scholar 

  11. Yonekura-Sakakibara, K., Tohge, T., Niida, R., & Saito, K. (2007). Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. Journal of Biological Chemistry, 282, 14932–14941.

    Article  CAS  Google Scholar 

  12. Kumar, R. J. S., Ruby, Singh, S., Sonawane, P. D., Vishwakarma, R. K., & Khan, B. M. (2013). Functional characterization of a glucosyltransferase specific to flavonoid 7-O-glucosides from Withania somnifera. Plant Molecular Biology Reporter, 31, 1100–1108.

    Article  CAS  Google Scholar 

  13. Liu, X., Lin, C., Ma, X., Tan, Y., Wang, J., & Zeng, M. (2018). Functional characterization of a flavonoid glycosyltransferase in sweet orange (Citrus sinensis). Frontiers in Plant Science, 9, 166.

    Article  Google Scholar 

  14. Funaki, A., Waki, T., Noguchi, A., Kawai, Y., Yamashita, S., Takahashi, S., & Nakayama, T. (2015). Identification of a highly specific isoflavone 7-O-glucosyltransferase in the soybean (Glycine max (L.) Merr.). Plant and Cell Physiology, 56, 1512–1520.

    Article  CAS  Google Scholar 

  15. Wang, X., Li, C., Zhou, Z., & Zhang, Y. (2019). Identification of Three (Iso)flavonoid glucosyltransferases from Pueraria lobata. Frontiers in Plant Science, 10, 28.

    Article  Google Scholar 

  16. Peng, M., Shahzad, R., Gul, A., Subthain, H., Shen, S., Lei, L., & Luo, J. (2017). Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance. Nature Communications, 8, 1975.

    Article  Google Scholar 

  17. Zhang, F., Guo, H., Huang, J., Yang, C., Li, Y., Wang, X., & Luo, J. (2020). A UV-B-responsive glycosyltransferase, OsUGT706C2, modulates flavonoid metabolism in rice. Science China Life Sciences, 63, 1037–1052.

    Article  CAS  Google Scholar 

  18. Xie, K., Chen, R., Li, J. H., Wang, R. S., Chen, D. W., Dou, X. X., & Dai, J. G. (2014). Exploring the catalytic promiscuity of a new glycosyltransferase from Carthamus tinctorius. Organic Letters, 16, 4874–4877.

    Article  CAS  Google Scholar 

  19. Xu, H. Y., Ren, J. H., Su, Y., Ren, F., Zhou, Y. J., Jiang, H., & Chen, J. (2020). Anti-hepatitis B virus activity of swertisin isolated from Iris tectorum Maxim. Journal of Ethnopharmacology, 257, 112787.

    Article  CAS  Google Scholar 

  20. Sun, Y., Li, W., & Wang, J. (2011). Ionic liquid based ultrasonic assisted extraction of isoflavones from Iris tectorum Maxim and subsequently separation and purification by high-speed counter-current chromatography. Journal of Chromatography B, 879, 975–980.

    Article  CAS  Google Scholar 

  21. Koch, W. K., Sieniawska, E., Widelski, J., Urjin, O., Głowniak, P., & Woźniak, K. S. (2015). Major secondary metabolites of Iris spp. Phytochemistry Reviews, 14, 51–80.

    Article  Google Scholar 

  22. Wu, Z., Ren, S., Chen, T., Hui, A., & Zhang, W. (2020). Separation and purification of six isoflavones from Iris tectorum Maxim by macroporous resin-based column chromatography coupled with preparative high-performance liquid chromatography. Separation Science and Technology, 55, 1686–1694.

    Article  CAS  Google Scholar 

  23. He, X. Z., Li, W. S., Blount, J. W., & Dixon, R. A. (2008). Regioselective synthesis of plant (iso)flavone glycosides in Escherichia coli. Applied Microbiology and Biotechnology, 80, 253–260.

    Article  CAS  Google Scholar 

  24. Chen, K., Hu, Z. M., Song, W., Wang, Z. L., He, J. B., Shi, X. M., & Ye, M. (2019). Diversity of O-glycosyltransferases contributes to the biosynthesis of flavonoid and triterpenoid glycosides in Glycyrrhiza uralensis. ACS Synthetic Biology, 8, 1858–1866.

    Article  CAS  Google Scholar 

  25. Homepage of the UGT Nomenclature Committee, Retrieved June 2, 2021 from http://prime.vetmed.wsu.edu/resources/udp-glucuronsyltransferase-homepage.

  26. Zhang, M., Li, F. D., Li, K., Wang, Z. L., Wang, Y. X., He, J. B., & Ye, M. (2020). Functional characterization and structural basis of an efficient Di-C-glycosyltransferase from Glycyrrhiza glabra. Journal of the American Chemical Society, 142, 3506–3512.

    Article  CAS  Google Scholar 

  27. Ha, D. T., Binh, B. T., Thu, N. T., Bich Thu, N. T., Thanh Tung, P. H., & Oh, W. K. (2019). Four new compounds isolated from the aerial part of Belamcanda chinensis (L.) and their effect on vascular smooth muscle cell (VSMC) Proliferation. Chemical & Pharmaceutical Bulletin, 67, 41–46.

    Article  CAS  Google Scholar 

  28. Monthakantirat, O., De-Eknamkul, W., Umehara, K., Yoshinaga, Y., Miyase, T., Warashina, T., & Noguchi, H. (2005). Phenolic constituents of the rhizomes of the Thai medicinal plant Belamcanda chinensis with proliferative activity for two breast cancer cell lines. Journal of Natural Products, 68, 361–364.

    Article  CAS  Google Scholar 

  29. Wang, C. L., Li, D., Wang, C. D., Xiao, F., Zhu, J. F., Shen, C., & Chen, X. D. (2017). Anti-inflammatory and anti-osteoarthritis effects of tectorigenin. Biology Open, 6, 1130–1136.

    Article  CAS  Google Scholar 

  30. Wang, J., Tang, Y., Lv, X., Zhang, J., Ma, B., Wen, X., & Wang, G. F. (2020). Tectoridin inhibits osteoclastogenesis and bone loss in a murine model of ovariectomy-induced osteoporosis. Experimental Gerontology, 140, 111057.

    Article  CAS  Google Scholar 

  31. Wen, C., Huang, W., Zhu, X. L., Li, X. S., Zhang, F., & Jiang, R. W. (2018). UGT74AN1, a permissive glycosyltransferase from Asclepias curassavica for the regiospecific steroid 3-O-glycosylation. Organic Letters, 20, 534–537.

    Article  CAS  Google Scholar 

  32. Chen, D. W., Chen, R., Wang, R., Li, J., Xie, K., Bian, C., & Dai, J. G. (2015). Probing the Catalytic promiscuity of a regio-and stereospecific C-glycosyltransferase from Mangifera indica. Angewandte Chemie International Edition, 54, 12678–12682.

    Article  CAS  Google Scholar 

  33. He, J. B., Zhao, P., Hu, Z. M., Liu, S., Kuang, Y., Zhang, M., & Ye, M. (2019). Molecular and structural characterization of a promiscuous C-glycosyltransferase from Trollius chinensis. Angewandte Chemie International Edition, 58, 11513–11520.

    Article  CAS  Google Scholar 

  34. Liu, X., Zhang, L., Feng, X., Lv, B., & Li, C. (2017). Biosynthesis of glycyrrhetinic acid-3-O-monoglucose using glycosyltransferase UGT73C11 from Barbarea vulgaris. Industrial & Engineering Chemistry Research, 56, 14949–14958.

    Article  CAS  Google Scholar 

  35. Chen, D. W., Fan, S., Chen, R., Xie, K., Yin, S., Sun, L., & Dai, J. G. (2018). Probing and engineering key residues for bis-C-glycosylation and promiscuity of a C-glycosyltransferase. ACS Catalysis, 8, 4917–4927.

    Article  CAS  Google Scholar 

  36. Xie, K., Zhang, X., Sui, S., Ye, F., & Dai, J. G. (2020). Exploring and applying the substrate promiscuity of a C-glycosyltransferase in the chemo-enzymatic synthesis of bioactive C-glycosides. Nature Communications, 11, 5162.

    Article  CAS  Google Scholar 

  37. Wang, X., Fan, R., Li, J., Li, C., & Zhang, Y. S. (2016). Molecular cloning and functional characterization of a novel (Iso)flavone 4′,7-O-diglucoside glucosyltransferase from Pueraria lobata. Frontiers in Plant Science, 7, 387.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhang, X., Zhu, Y., Ye, J., Ye, Z., Zhu, R., Xie, G., & Qin, M. J. (2021). Iris domestica (iso)flavone 7- and 3’-O-glycosyltransferases can be induced by CuCl2. Frontiers in Plant Science, 12, 632.

    Google Scholar 

Download references

Funding

This study was supported by Guangdong Key Laboratory for translational Cancer research of Chinese Medicine (No. 2018B030322011), the National Natural Science Foundation of China (CN) (No.81874333 and 82003895) and the Guangdong Basic and Applied Basic Research Foundation (No.2020A1515010926).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Lixin Duan or Aijia Ji.

Ethics declarations

Conflict of interest

All authors in this article indicated no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 760 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, J., Li, J., Yue, J. et al. Functional Characterization of a Novel Glycosyltransferase (UGT73CD1) from Iris tectorum Maxim. for the Substrate promiscuity. Mol Biotechnol 63, 1030–1039 (2021). https://doi.org/10.1007/s12033-021-00364-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-021-00364-1

Keywords

Navigation