Characterization of Panax ginseng UDP-glycosyltransferases catalyzing protopanaxatriol and biosyntheses of bioactive ginsenosides F1 and Rh1 in metabolically engineered yeasts

Molecular Plant

Volumn 8, Issue 9, 2015, Pages 1412-1424

  Wei, Wei ^a   Wang, Pingping ^a   Wei, Yongjun ^a   Liu, Qunfang ^b   Yang, Chengshuai ^a   Zhao, Guoping ^a   Yue, Jianmin ^b   Yan, Xing ^a   Zhou, Zhihua ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

ginsenoside F1; ginsenoside Rh1; Panax ginseng; protopanaxatriol; triterpenoids; UDP glycosyltransferase

Indexed keywords

AMINO ACID; GINSENOSIDE; GINSENOSIDE F1; GINSENOSIDE RH1; GLYCOSYLTRANSFERASE; MUTANT PROTEIN; PROTOPANAXATRIOL; SAPOGENIN; URIDINE DIPHOSPHATE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC ENGINEERING; GENETICS; KINETICS; METABOLIC ENGINEERING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PANAX; PLANT GENE; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; BIOCATALYSIS; CLONING, MOLECULAR; GENES, PLANT; GENETIC ENGINEERING; GINSENOSIDES; GLYCOSYLTRANSFERASES; KINETICS; METABOLIC ENGINEERING; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PANAX; SACCHAROMYCES CEREVISIAE; SAPOGENINS; SUBSTRATE SPECIFICITY; URIDINE DIPHOSPHATE;

EID: 84941192889     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.05.010     Document Type: Article

References (40)

1. L. Achnine, D.V. Huhman, M.A. Farag, L.W. Sumner, J.W. Blount, and R.A. Dixon Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula Plant J. 41 2005 875 887
2. A. Aharoni, L. Gaidukov, O. Khersonsky, S.M. Gould, C. Roodveldt, and D.S. Tawfik The 'evolvability' of promiscuous protein functions Nat. Genet. 37 2005 73 76
3. J.M. Augustin, S. Drok, T. Shinoda, K. Sanmiya, J.K. Nielsen, B. Khakimov, C.E. Olsen, E.H. Hansen, V. Kuzina, and C.T. Ekstrøm UDP-glycosyltransferases from the UGT73C subfamily in Barbarea vulgaris catalyze sapogenin 3-O-glucosylation in saponin-mediated insect resistance Plant Physiol. 160 2012 1881 1895
4. D. Bowles, E.-K. Lim, B. Poppenberger, and F.E. Vaistij Glycosyltransferases of lipophilic small molecules Annu. Rev. Plant Biol. 57 2006 567 597
5. M. Brazier-Hicks, W.A. Offen, M.C. Gershater, T.J. Revett, E.-K. Lim, D.J. Bowles, G.J. Davies, and R. Edwards Characterization and engineering of the bifunctional N-and O-glucosyltransferase involved in xenobiotic metabolism in plants Proc. Natl. Acad. Sci. USA 104 2007 20238 20243
6. S. Chen, H. Luo, Y. Li, Y. Sun, Q. Wu, Y. Niu, J. Song, A. Lv, Y. Zhu, and C. Sun 454 EST analysis detects genes putatively involved in ginsenoside biosynthesis in Panax ginseng Plant Cell Rep. 30 2011 1593 1601
7. L.P. Christensen Ginsenosides chemistry, biosynthesis, analysis, and potential health effects Adv. Food Nutr. Res. 55 2009 1 99
8. M. Fukuchi-Mizutani, H. Okuhara, Y. Fukui, M. Nakao, Y. Katsumoto, K. Yonekura-Sakakibara, T. Kusumi, T. Hase, and Y. Tanaka Biochemical and molecular characterization of a novel UDP-glucose: anthocyanin 3′-O-glucosyltransferase, a key enzyme for blue anthocyanin biosynthesis, from gentian Plant Physiol. 132 2003 1652 1663
9. J.Y. Han, Y.S. Kwon, D.C. Yang, Y.R. Jung, and Y.E. Choi Expression and RNA interference-induced silencing of the dammarenediol synthase gene in Panax ginseng Plant Cell Physiol. 47 2006 1653 1662
10. J.Y. Han, H.J. Kim, Y.S. Kwon, and Y.E. Choi The Cyt P450 enzyme CYP716A47 catalyzes the formation of protopanaxadiol from dammarenediol-II during ginsenoside biosynthesis in Panax ginseng Plant Cell Physiol. 52 2011 2062 2073
11. J.Y. Han, H.S. Hwang, S.W. Choi, H.J. Kim, and Y.E. Choi Cytochrome P450 CYP716A53v2 catalyzes the formation of protopanaxatriol from protopanaxadiol during ginsenoside biosynthesis in Panax ginseng Plant Cell Physiol. 53 2012 1535 1545
12. X.Z. He, X. Wang, and R.A. Dixon Mutational analysis of the Medicago glycosyltransferase UGT71G1 reveals residues that control regioselectivity for (iso)flavonoid glycosylation J. Biol. Chem. 281 2006 34441 34447
13. T. Hiromoto, E. Honjo, T. Tamada, N. Noda, K. Kazuma, M. Suzuki, and R. Kuroki Crystal structure of UDP-glucose:anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea J. Synchrotron Radiat. 20 2013 894 898
14. O. Jaillon, J.M. Aury, B. Noel, A. Policriti, C. Clepet, A. Casagrande, N. Choisne, S. Aubourg, N. Vitulo, C. Jubin, and et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla Nature 449 2007 463 467
15. S.C. Jung, W. Kim, S.C. Park, J. Jeong, M.K. Park, S. Lim, Y. Lee, W.T. Im, J.H. Lee, G. Choi, and et al. Two ginseng UDP-glycosyltransferases synthesize ginsenoside Rg3 and Rd Plant Cell Physiol. 55 2014 2177 2188
16. K. Kogawa, N. Kato, K. Kazuma, N. Noda, and M. Suzuki Purification and characterization of UDP-glucose: anthocyanin 3',5'-O-glucosyltransferase from Clitoria ternatea Planta 226 2007 1501 1509
17. A. Kubo, Y. Arai, S. Nagashima, and T. Yoshikawa Alteration of sugar donor specificities of plant glycosyltransferases by a single point mutation Arch. Biochem. Biophys. 429 2004 198 203
18. V. Kuzina, J.K. Nielsen, J.M. Augustin, A.M. Torp, S. Bak, and S.B. Andersen Barbarea vulgaris linkage map and quantitative trait loci for saponins, glucosinolates, hairiness and resistance to the herbivore Phyllotreta nemorum Phytochemistry 72 2011 188 198
19. L. Li, L.V. Modolo, L.L. Escamilla-Trevino, L. Achnine, R.A. Dixon, and X. Wang Crystal structure of Medicago truncatula UGT85H2-insights into the structural basis of a multifunctional (iso) flavonoid glycosyltransferase J. Mol. Biol. 370 2007 951 963
20. C. Li, Y. Zhu, X. Guo, C. Sun, H. Luo, J. Song, Y. Li, L. Wang, J. Qian, and S. Chen Transcriptome analysis reveals ginsenosides biosynthetic genes, microRNAs and simple sequence repeats in Panax ginseng CA Meyer BMC Genomics 14 2013 245
21. H. Luo, C. Sun, Y. Sun, Q. Wu, Y. Li, J. Song, Y. Niu, X. Cheng, H. Xu, and C. Li Analysis of the transcriptome of Panax notoginseng root uncovers putative triterpene saponin-biosynthetic genes and genetic markers BMC Genomics 12 2011 S5
22. D. Meesapyodsuk, J. Balsevich, D.W. Reed, and P.S. Covello Saponin biosynthesis in Saponaria vaccaria. cDNAs encoding β-amyrin synthase and a triterpene carboxylic acid glucosyltransferase Plant Physiol. 143 2007 959 969
23. L.V. Modolo, L. Li, H. Pan, J.W. Blount, R.A. Dixon, and X. Wang Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso) flavonoids J. Mol. Biol. 392 2009 1292 1302
24. P.J. O'Brien, and D. Herschlag Catalytic promiscuity and the evolution of new enzymatic activities Chem. Biol. 6 1999 R91 R105
25. W. Offen, C. Martinez-Fleites, M. Yang, E. Kiat-Lim, B.G. Davis, C.A. Tarling, C.M. Ford, D.J. Bowles, and G.J. Davies Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification EMBO J. 25 2006 1396 1405
26. J. Ogata, Y. Kanno, Y. Itoh, H. Tsugawa, and M. Suzuki Plant biochemistry: anthocyanin biosynthesis in roses Nature 435 2005 757 758
27. E. Ono, Y. Homma, M. Horikawa, S. Kunikane-Doi, H. Imai, S. Takahashi, Y. Kawai, M. Ishiguro, Y. Fukui, and T. Nakayama Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera) Plant Cell 22 2010 2856 2871
28. S.A. Osmani, S. Bak, and B.L. Moller Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling Phytochemistry 70 2009 325 347
29. B. Poppenberger, F. Berthiller, D. Lucyshyn, T. Sieberer, R. Schuhmacher, R. Krska, K. Kuchler, J. Glossl, C. Luschnig, and G. Adam Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana J. Biol. Chem. 278 2003 47905 47914
30. B. Poppenberger, S. Fujioka, K. Soeno, G.L. George, F.E. Vaistij, S. Hiranuma, H. Seto, S. Takatsuto, G. Adam, and S. Yoshida The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids Proc. Natl. Acad. Sci. USA 102 2005 15253 15258
31. A. Richman, A. Swanson, T. Humphrey, R. Chapman, B. McGarvey, R. Pocs, and J. Brandle Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana Plant J. 41 2005 56 67
32. H. Shao, X. He, L. Achnine, J.W. Blount, R.A. Dixon, and X. Wang Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula Plant Cell 17 2005 3141 3154
33. S. Shibata Chemistry and cancer preventing activities of ginseng saponins and some related triterpenoid compounds J. Korean Med. Sci. 16 2001 S28 S37
34. M. Shibuya, K. Nishimura, N. Yasuyama, and Y. Ebizuka Identification and characterization of glycosyltransferases involved in the biosynthesis of soyasaponin I in Glycine max FEBS Lett. 584 2010 2258 2264
35. C. Sun, Y. Li, Q. Wu, H. Luo, Y. Sun, J. Song, E. Lui, and S. Chen De novo sequencing and analysis of the American ginseng root transcriptome using a GS FLX Titanium platform to discover putative genes involved in ginsenoside biosynthesis BMC Genomics 11 2010 262
36. P. Tansakul, M. Shibuya, T. Kushiro, and Y. Ebizuka Dammarenediol-II synthase, the first dedicated enzyme for ginsenoside biosynthesis, in Panax ginseng FEBS Lett. 580 2006 5143 5149
37. P. Wang, Y. Wei, Y. Fan, Q. Liu, W. Wei, C. Yang, L. Zhang, G. Zhao, J. Yue, X. Yan, and et al. Production of bioactive ginsenosides Rh2 and Rg3 by metabolically engineered yeasts Metab. Eng. 29 2015 97 105
38. J.K. Weng, R.N. Philippe, and J.P. Noel The rise of chemodiversity in plants Science 336 2012 1667 1670
39. X. Yan, Y. Fan, W. Wei, P. Wang, Q. Liu, Y. Wei, L. Zhang, G. Zhao, J. Yue, and Z. Zhou Production of bioactive ginsenoside compound K in metabolically engineered yeast Cell Res. 24 2014 770 773
40. T.-K. Yun Panax ginseng-a non-organ-specific cancer preventive? Lancet Oncol. 2 2001 49 55