Triterpenoid-biosynthetic UDP-glycosyltransferases from plants

Biotechnology Advances

Volumn 37, Issue 7, 2019, Pages

  Rahimi, Shadi ^a,b,c   Kim, Jaewook ^a,d   Mijakovic, Ivan ^c,e   Jung, Ki Hong ^f   Choi, Giltsu ^a   Kim, Sun Chang ^a,b   Kim, Yu Jin ^f  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Intelligent Synthetic Biology Center   (South Korea)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^d KYUSHU UNIVERSITY   (Japan)

^e Chalmers University of Technology   (Denmark)

^f Kyung Hee University   (South Korea)

Author keywords

Ginsenosides; Panax ginseng; Saponin; Triterpenoid; Uridine diphosphate glycosyltransferase

Indexed keywords

AMINO ACIDS; CATALYST ACTIVITY; GLYCOSYLATION; MOLECULES; PHYSICOCHEMICAL PROPERTIES; PLANTS (BOTANY);

GINSENOSIDES; GLYCOSYL TRANSFERASE; PANAX GINSENG; SAPONIN; TRITERPENOIDS;

ENZYMES;

BIOACTIVITY; CATALYSIS; DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; PHYSICOCHEMICAL PROPERTY; TERPENE;

ARABIDOPSIS THALIANA; BARBAREA VULGARIS; GLYCINE MAX; MEDICAGO TRUNCATULA; PANAX GINSENG; VACCARIA HISPANICA;

GLYCOSYLTRANSFERASE; TRITERPENE; URIDINE DIPHOSPHATE;

GLYCOSYLATION; METABOLISM; PANAX; PHYLOGENY;

GLYCOSYLATION; GLYCOSYLTRANSFERASES; PANAX; PHYLOGENY; TRITERPENES; URIDINE DIPHOSPHATE;

EID: 85065906439     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2019.04.016     Document Type: Review

References (106)

1. Achnine, L., Huhman, D.V., Farag, M.A., Sumner, L.W., Blount, J.W. and Dixon, R.A., 2005. Genomics‐based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant J. 41(6), 875-887.
2. Augustin, J.M., Kuzina, V., Andersen, S.B. and Bak, S., 2011. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72(6), 435-457.
3. Augustin, J.M., Bak, S.D., Shinoda, T., Sanmiya, K., Nielsen, J.K., Khakimov, B., Olsen, C.E., Hansen, E.H., Kuzina, V., Ekstrøm, C.T. and Hauser, T.P., 2012. UDP-glycosyltransferases from the UGT73C Subfamily in Barbarea vulgaris catalyse Sapogenin 3-O-glucosylation in Saponin-mediated Insect resistance. Plant Physiol. 160, 1881–1895.
4. Baeg, I.H. and So, S.H., 2013. The world ginseng market and the ginseng (Korea). J. Ginseng Res. 37(1), 1-7.
5. Barvkar, V.T., Pardeshi, V.C., Kale, S.M., Kadoo, N.Y. and Gupta, V.S., 2012. Phylogenomic analysis of UDP glycosyltransferase 1 multigene family in Linum usitatissimum identified genes with varied expression patterns. BMC genomics 13(1), 175.
6. Bönisch, F., Frotscher, J., Stanitzek, S., Rühl, E., Wüst, M., Bitz, O., Schwab, W., 2014. A UDP-glucose: monoterpenol glucosyltransferase adds to the chemical diversity of the grapevine metabolome (Vitis vinifera L). Plant Physiol. 165, 561–581.
7. Brazier-Hicks, M., Offen, W.A., Gershater, M.C., Revett, T.J., Lim, E.K., Bowles, D.J., Davies, G.J. and Edwards, R. (2007) Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proc. Natl. Acad. Sci. USA 104, 20238–20243.
8. Brazier-Hicks, M., Gershater, M., Dixon, D., Edwards, R., 2018. Substrate specificity and safener inducibility of the plant UDP-glucose-dependent family 1 glycosyltransferase super-family. Plant Biotechnol. J. 16(1), 337-348.
9. Breton, C., Najdrova, L.S., Jeanneau, C., Koca, J., Imberty, A., 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16, 29–37.
10. Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V. and Henrissat, B., 2008. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37(suppl_1), D233-D238.
11. Caputi, L., Lim, E.K. and Bowles, D.J., 2008. Discovery of new biocatalysts for the glycosylation of terpenoid scaffolds. Chem. Eur. J. 14(22), 6656-6662.
12. Caputi, L., Malnoy, M., Goremykin, V., Nikiforova, S. and Martens, S., 2012. A genome‐wide phylogenetic reconstruction of family 1 UDP‐glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J. 69(6), 1030-1042.
13. Chang, A., Singh, S., Phillips Jr, G.N. and Thorson, J.S., 2011. Glycosyltransferase structural biology and its role in the design of catalysts for glycosylation. Curr. Opin. Biotechnol. 22(6), 800-808.
14. Chen, S., Luo, H., Li, Y., Sun, Y., Wu, Q., Niu, Y., Song, J., Lv, A., Zhu, Y., Sun, C. and Steinmetz, A., 2011. 454 EST analysis detects genes putatively involved in ginsenoside biosynthesis in Panax ginseng. Plant Cell Rep. 30(9), 1593.
15. Dai, L., Liu, C., Zhu, Y., Zhang, J., Men, Y., Zeng, Y. and Sun, Y., 2015. Functional characterization of cucurbitadienol synthase and triterpene glycosyltransferase involved in biosynthesis of mogrosides from Siraitia grosvenorii. Plant Cell Physiol. 56(6), 1172-1182.
16. De Costa, F., Barber, C.J., Kim, Y.B., Reed, D.W., Zhang, H., Fett-Neto, A.G. and Covello, P.S., 2017. Molecular cloning of an ester-forming triterpenoid: UDP-glucose 28-O-glucosyltransferase involved in saponin biosynthesis from the medicinal plant Centella asiatica. Plant Sci. 262, 9-17.
17. Edgar, R.C., 2004a. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5), 1792-1797.
18. Edgar, R.C., 2004b. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. (5), 113.
19. Gachon, C.M., Langlois-Meurinne, M. and Saindrenan, P., 2005. Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci. 10(11), 542-549.
20. Han, S.H., Kim, B.G., Yoon, J.A., Chong, Y., and Ahn, J.H., 2014. Synthesis of flavonoid O-pentosides by Escherichia coli through engineering of nucleotide sugar pathways and glycosyltransferase. Appl. Environ. Microbiol. 80, 2754-2762.
21. Hans, J., Brandt, W., Vogt, T., 2004. Site-directed mutagenesis and protein 3D-homology modelling suggest a catalytic mechanism for UDP-glucose-dependent betanidin 5-O-glucosyltransferase from Dorotheanthus bellidiformis. Plant J. 39, 319–333.
22. Hayashi, H., Nishiyama, Y., Tomizawa, N., Hiraoka, N. and Ikeshiro, Y., 1996. UDP-glucuronic acid: triterpene glucuronosyltransferase activity in cultured licorice cells. Phytochemistry 42(3), 665-666.
23. Hayashi, H., Huang, P. and Inoue, K., 2003. Up-regulation of soyasaponin biosynthesis by methyl jasmonate in cultured cells of Glycyrrhiza glabra. Plant Cell Physiol. 44(4), 404-411.
24. He, J., Chen, K., Hu, Z.M., Li, K., Song, W., Yu, L.Y., Leung, C.H., Ma, D.L., Qiao, X. and Ye, M., 2018. UGT73F17, a new glycosyltransferase from Glycyrrhiza uralensis, catalyzes the regiospecific glycosylation of pentacyclic triterpenoids. Chem. Commun. 54(62), 8594-8597.
25. Hiromoto, T., Honjo, E., Tamada, T., Noda, N., Kazuma, K., Suzuki, M. and Kuroki, R., 2013. Crystal structure of UDP-glucose: anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. J. Synchrotron Radiat. 20(6), 894-898.
26. Huhman, D.V., Berhow, M.A. and Sumner, L.W., 2005. Quantification of saponins in aerial and subterranean tissues of Medicago truncatula. J. Agric. Food Chem. 53(6), 1914-1920.
27. Hwang, H.S., Lee, H. and Choi, Y.E., 2015. Transcriptomic analysis of Siberian ginseng (Eleutherococcus senticosus) to discover genes involved in saponin biosynthesis. BMC genomics 16(1), 180.
28. Itkin, M., Davidovich-Rikanati, R., Cohen, S., Portnoy, V., Doron-Faigenboim, A., Oren, E., Freilich, S., Tzuri, G., Baranes, N., Shen, S., Petreikov, M., 2016. The biosynthetic pathway of the nonsugar, high-intensity sweetener mogroside V from Siraitia grosvenorii. Proc. Natl. Acad. Sci. U.S.A. 113(47), E7619-E7628.
29. Jaillon, O., Aury, J.M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C. and Vezzi, A., 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161), 463–467.
30. James, J. and Dubery, I., 2009. Pentacyclic triterpenoids from the medicinal herb, Centella asiatica (L.) Urban. Molecules 14(10), 3922-3941.
31. Jeena, G.S., Fatima, S., Tripathi, P., Upadhyay, S. and Shukla, R.K., 2017. Comparative transcriptome analysis of shoot and root tissue of Bacopa monnieri identifies potential genes related to triterpenoid saponin biosynthesis. BMC genomics 18(1), 490.
32. Jiang, X., Yang, C., Baosheng, L., Shuiming, X., Qinggang, Y., Rui, B., He, S., Linlin, D., Xiwen, L., Jun, Q. and Jingjing, Z., 2017. Panax ginseng genome examination for ginsenoside biosynthesis. GigaScience. 6(11), 2017, 1–15.
33. Jung, S.C., Kim, W., Park, S.C., Jeong, J., Park, M.K., Lim, S., Lee, Y., Im, W.T., Lee, J.H., Choi, G. and Kim, S.C., 2014. Two ginseng UDP-glycosyltransferases synthesize ginsenoside Rg3 and Rd. Plant Cell Physiol. 55(12), 2177-2188.
34. Kang, K.B., Jayakodi, M., Lee, Y.S., Nguyen, V.B., Park, H.S., Koo, H.J., Choi, I.Y., Kim, D.H., Chung, Y.J., Ryu, B. and Lee, D.Y., 2018. Identification of candidate UDP-glycosyltransferases involved in protopanaxadiol-type ginsenoside biosynthesis in Panax ginseng. Sci. Rep. 8(1), 11744.
35. Kesselmeier J. and Urban B., Subcellular localization of saponins in green and etiolated leaves and green protoplasts of oat (Avena sativa L.), Protoplasma, 114(1-2), 1983, 133-140.
36. Khorolragchaa, A., Kim, Y.J., Rahimi, S., Sukweenadhi, J., Jang, M.G. and Yang, D.C., 2014. Grouping and characterization of putative glycosyltransferase genes from Panax ginseng Meyer. Gene 536(1), 186-192.
37. Kim, O.T., Bang, K.H., Kim, Y.C., Hyun, D.Y., Kim, M.Y. and Cha, S.W., 2009. Upregulation of ginsenoside and gene expression related to triterpene biosynthesis in ginseng hairy root cultures elicited by methyl jasmonate. Plant Cell Tissue Organ Cult. (PCTOC) 98(1), 25-33.
38. Kim, O.T., Yoo, N.H., Kim, G.S., Kim, Y.C., Bang, K.H., Hyun, D.Y., Kim, S.H. and Kim, M.Y., 2013. Stimulation of Rg3 ginsenoside biosynthesis in ginseng hairy roots elicited by methyl jasmonate. Plant Cell Tissue Organ Cult (PCTOC) 112(1), 87-93.
39. Kim, O.T., Um, Y., Jin, M.L., Kim, Y.C., Bang, K.H., Hyun, D.Y., Lee, H.S. and Lee, Y., 2014. Analysis of expressed sequence tags from Centella asiatica (L.) Urban hairy roots elicited by methyl jasmonate to discover genes related to cytochrome P450s and glucosyltransferases. Plant Biotechnol. Rep. 8(2), 211-220.
40. Kim, Y.J., Zhang, D. and Yang, D.C., 2015b. Biosynthesis and biotechnological production of ginsenosides. Biotechnol. Ad. 33(6), 717-735.
41. Kim, S.C., Choi, G., Jung, S.C., Kim, W., Lim, S., Im, W.T., 2015a. U.S. Patent Application No. 14/857,703.
42. Kim, O.T., Jin, M.L., Lee, D.Y., Jetter, R., 2017. Characterization of the Asiatic Acid Glucosyltransferase, UGT73AH1, Involved in Asiaticoside Biosynthesis in Centella asiatica (L.) Urban. Int. J. Mol. Sci. 18:2630.
43. Kurosawa, Y., Takahara, H. and Shiraiwa, M., 2002. UDP-glucuronic acid: soyasapogenol glucuronosyltransferase involved in saponin biosynthesis in germinating soybean seeds. Planta 215(4), 620-629.
44. Lairson, L.L., Henrissat, B., Davies, G.J. and Withers, S.G., 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77.
45. Li, L., Modolo, L.V., Escamilla-Trevino, L.L., Achnine, L., Dixon, R.A. and Wang, X., 2007. Crystal structure of Medicago truncatula UGT85H2–insights into the structural basis of a multifunctional (iso) flavonoid glycosyltransferase. J. Mol. Biol. 370(5), 951-963.
46. Li, Y., Luo, H.M., Sun, C., Song, J.Y., Sun, Y.Z., Wu, Q., Wang, N., Yao, H., Steinmetz, A. and Chen, S.L., 2010. EST analysis reveals putative genes involved in glycyrrhizin biosynthesis. BMC genomics 11(1), 268.
47. Li, C., Zhu, Y., Guo, X., Sun, C., Luo, H., Song, J., Li, Y., Wang, L., Qian, J. and Chen, S., 2013. Transcriptome analysis reveals ginsenosides biosynthetic genes, microRNAs and simple sequence repeats in Panax ginseng CA Meyer. BMC genomics 14(1), 245.
48. 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. Chem. Soc. Rev. 44(22), 8350-8374.
49. Liu, C., Dai, L., Liu, Y., Dou, D., Sun, Y. and Ma, L., 2018. Pharmacological activities of mogrosides. Future Med. Chem. 10(8), 845-850.
50. Louveau T., Orme A., Pfalzgraf H., Stephenson M.J., Melton R., Saalbach G., Hemmings A.M., Leveau A., Rejzek M., Vickerstaff R.J. and Langdon T., Analysis of Two New Arabinosyltransferases Belonging to the Carbohydrate-Active Enzyme (CAZY) Glycosyl Transferase Family1 Provides Insights into Disease Resistance and Sugar Donor Specificity, The Plant Cell 30(12), 2018, 3038-3057.
51. Louveau T., Leitao C., Green S., Hamiaux C., Van der Rest B., Dechy‐Cabaret O., Atkinson R.G. and Chervin C., Predicting the substrate specificity of a glycosyltransferase implicated in the production of phenolic volatiles in tomato fruit, The FEBS journal, 278(2), 2011, 390-400.
52. Lu, C., Zhao, S., Wei, G., Zhao, H. and Qu, Q., 2017a. Functional regulation of ginsenoside biosynthesis by RNA interferences of a UDP-glycosyltransferase gene in Panax ginseng and Panax quinquefolius. Plant Physiol. Biochem. 111, 67-76.
53. Lu, C., Zhao, S.J. and Wang, X.S., 2017a. Functional regulation of a UDP-glucosyltransferase gene (Pq3-O-UGT1) by RNA interference and overexpression in Panax quinquefolius. Plant Cell Tissue Organ Cult. (PCTOC) 129(3), 445-456.
54. Luo, H., Sun, C., Sun, Y., Wu, Q., Li, Y., Song, J., Niu, Y., Cheng, X., Xu, H., Li, C. and Liu, J., 2011. Analysis of the transcriptome of Panax notoginseng root uncovers putative triterpene saponin-biosynthetic genes and genetic markers. BMC genomics 12(5), S5–S19.
55. Matsuda, H., Morikawa, T., Ueda, H. and Yoshikawa, M., 2001. Medicinal foodstuffs. XXVII. Saponin constituents of gotu kola (2): structures of new ursane-and oleanane-type triterpene oligoglycosides, centellasaponins B, C, and D, from Centella asiatica cultivated in Sri Lanka. Chem. Pharm. Bull. 49(10), 1368-1371.
56. Meesapyodsuk, D., Balsevich, J., Reed, D.W. and Covello, P.S., 2007. Saponin biosynthesis in Saponaria vaccaria. cDNAs encoding β-amyrin synthase and a triterpene carboxylic acid glucosyltransferase. Plant Physiol. 143(2), 959-969.
57. Modolo, L.V., Li, L., Pan, H., Blount, J.W., Dixon, R.A. and Wang, X., 2009. Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso) flavonoids. J. Mol. Biol. 392(5), 1292-1302.
58. Mugford, S.T. and Osbourn, A., 2012. Saponin synthesis and function, in: Isoprenoid Synthesis in Plants and Microorganisms, Springer, New York, pp. 405-424.
59. Mylona P., Owatworakit A., Papadopoulou K., Jenner H., Qin B., Findlay K., Hill L., Qi X., Bakht S., Melton R. and Osbourn A., Sad3 and Sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20, 2008, 201–212.
60. Nagatoshi, M., Terasaka, K., Nagatsu, A. and Mizukami, H., 2011. Iridoid-specific glucosyltransferase from Gardenia jasminoides. J. Biol. Chem. 286(37), 32866-32874.
61. Naoumkina, M.A., Modolo, L.V., Huhman, D.V., Urbanczyk-Wochniak, E., Tang, Y., Sumner, L.W. and Dixon, R.A., 2010. Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell 22(3), 850-866.
62. Nielsen, N.J., Nielsen, J., Staerk, D., 2010. New resistance-correlated saponins from the insect-resistant crucifer Barbarea vulgaris. J. Agric. Food Chem. 58, 5509–5514.
63. Noguchi, A., Saito, A., Homma, Y., Nakao, M., Sasaki, N., Nishino, T., Takahashi, S. and Nakayama, T., 2007. A UDP-glucose: isoflavone 7-O-glucosyltransferase from the roots of soybean (Glycine max) seedlings purification, gene cloning, phylogenetics, and an implication for an alternative strategy of enzyme catalysis. J. Biol. Chem. 282(32), 23581-23590.
64. Offen, W., Martinez‐Fleites, C., Yang, M., Kiat‐Lim, E., Davis, B.G., Tarling, C.A., Ford, C.M., Bowles, D.J. and Davies, G.J., 2006. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 25(6), 1396-1405.
65. Ono, E., Homma, Y., Horikawa, M., Kunikane-Doi, S., Imai, H., Takahashi, S., Kawai, Y., Ishiguro, M., Fukui, Y. and Nakayama, T., 2010. Functional differentiation of the glycosyltransferases that contribute to the chemical diversity of bioactive flavonol glycosides in grapevines (Vitis vinifera). Plant Cell tpc-110.
66. Osmani, S.A., Bak, S., Imberty, A., Olsen, C.E. and Møller, B.L., 2008. Catalytic key amino acids and UDP-sugar donor specificity of a plant glucuronosyltransferase, UGT94B1: molecular modeling substantiated by site-specific mutagenesis and biochemical analyses. Plant Physiol. 148(3), 1295-1308.
67. Osmani, S.A., Bak, S. and Møller, B.L., 2009. Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 70(3), 325-347.
68. Owatworakit, A., Townsend, B., Louveau, T., Jenner, H., Rejzek, M., Hughes, R.K., Saalbach, G., Qi, X., Bakht, S., Roy, A.D. and Mugford, S.T., 2013. Glycosyltransferases from oat (Avena) implicated in the acylation of avenacins. J. Biol. Chem. 288(6), 3696-3704.
69. Rahimi, S., Kim, Y.J. and Yang, D.C., 2015. Production of ginseng saponins: elicitation strategy and signal transductions. Appl. Microbiol. Biotechnol. 99(17), 6987-6996.
70. Rahimi, S., Kim, Y.J., Devi, B.S.R., Oh, J.Y., Kim, S.Y., Kwon, W.S. and Yang, D.C., 2016a. Sodium nitroprusside enhances the elicitation power of methyl jasmonate for ginsenoside production in Panax ginseng roots. Res. Chem. Intermediat. 42(4), 2937-2951.
71. Rahimi, S., Kim, Y.J., Sukweenadhi, J., Zhang, D. and Yang, D.C., 2016b. PgLOX6 encoding a lipoxygenase contributes to jasmonic acid biosynthesis and ginsenoside production in Panax ginseng. J. Exp. Bot. 67(21), 6007-6019.
72. Saha, S., Walia, S., Kumar, J. and Parmar, B.S., 2010. Structure–biological activity relationships in triterpenic saponins: the relative activity of protobassic acid and its derivatives against plant pathogenic fungi. Pest Manag. Sci. 66(8), 825-831.
73. Sawada, S.Y., Suzuki, H., Ichimaida, F., Yamaguchi, M.A., Iwashita, T., Fukui, Y., Hemmi, H., Nishino, T. and Nakayama, T., 2005. UDP-glucuronic acid: anthocyanin glucuronosyltransferase from red daisy (Bellis perennis) flowers enzymology and phylogenetics of a novel glucuronosyltransferase involved in flower pigment biosynthesis. J. Biol. Chem. 280(2), 899-906.
74. Sawai, S. and Saito, K., 2011. Triterpenoid biosynthesis and engineering in plants. Front. Plant Sci. 2, 25.
75. Sayama, T., Ono, E., Takagi, K., Takada, Y., Horikawa, M., Nakamoto, Y., Hirose, A., Sasama, H., Ohashi, M., Hasegawa, H. and Terakawa, T., 2012. The Sg-1 glycosyltransferase locus regulates structural diversity of triterpenoid saponins of soybean. Plant Cell tpc-111.
76. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J. and Xu, D., 2010. Genome sequence of the palaeopolyploid soybean. Nature 463(7278), 178–183.
77. Scholz, M., Prüfer, D., Müller, K.J. and FhG, I.M.E., Cloning and Molecular Characterization of Two Triterpene Glycosyltransferases from Black Cumin (Nigella sativa L.).
78. Schramek, N., Huber, C., Schmidt, S., Dvorski, S.E., Kmispel, N., Ostrozhenkova, E., Pena-Rodriguez, L.M., Cusido, R.M., Wischmann, G., Eisenreich, W., 2014. Biosynthesis of ginsenosides in field-grown Panax ginseng. JSM Biotechnol. Biomed. Eng. 2(1), 1033.
79. Seki, H., Tamura, K. and Muranaka, T., 2015. P450s and UGTs: key players in the structural diversity of triterpenoid saponins. Plant Cell Physiol. 56(8), 1463-1471.
80. Shabani, L., Ehsanpour, A.A., Asghari, G. and Emami, J., 2009. Glycyrrhizin production by in vitro cultured Glycyrrhiza glabra elicited by methyl jasmonate and salicylic acid. Russ. J. Plant Physiol. 56(5), 621-626.
81. Shao, H., He, X., Achnine, L., Blount, J.W., Dixon, R.A. and Wang, X., 2005. Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17(11), 3141-3154.
82. Shibuya, M., Nishimura, K., Yasuyama, N. and Ebizuka, Y., 2010. Identification and characterization of glycosyltransferases involved in the biosynthesis of soyasaponin I in Glycine max. FEBS lett. 584(11), 2258-2264.
83. Shimoyamada, M., Kudo, S., Okubo, K., Yamauchi, F. and Harada, K., 1990. Distributions of saponin constituents in some varieties of soybean plant. Agric. Biol. Chem. 54(1), 77-81.
84. Song, C., Gu, L., Liu, J., Zhao, S., Hong, X., Schulenburg, K. and Schwab, W., 2015. Functional characterization and substrate promiscuity of UGT71 glycosyltransferases from strawberry (Fragaria× ananassa). Plant Cell Physiol. 56(12), 2478-2493.
85. Sui, C., Zhang, J., Wei, J., Chen, S., Li, Y., Xu, J., Jin, Y., Xie, C., Gao, Z., Chen, H. and Yang, C., 2011. Transcriptome analysis of Bupleurum chinense focusing on genes involved in the biosynthesis of saikosaponins. BMC genomics 12(1), 539.
86. Sun, C., Li, Y., Wu, Q., Luo, H., Sun, Y., Song, J., Lui, E.M. and Chen, S., 2010. 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(1), 262.
87. Sun, H., Li, F., Xu, Z., Sun, M., Cong, H., Qiao, F. and Zhong, X., 2017. De novo leaf and root transcriptome analysis to identify putative genes involved in triterpenoid saponins biosynthesis in Hedera helix L. PloS one 12(8), e0182243.
88. Takada, Y., Sayama, T., Kikuchi, A., Kato, S., Tatsuzaki, N., Nakamoto, Y., Suzuki, A., Tsukamoto, C. and Ishimoto, M., 2010. Genetic analysis of variation in sugar chain composition at the C-22 position of group A saponins in soybean, Glycine max (L.) Merrill. Breed. Sci. 60(1), 3-8.
89. Tang, Q., Ma, X., Mo, C., Wilson, I.W., Song, C., Zhao, H., Yang, Y., Fu, W. and Qiu, D., 2011. An efficient approach to finding Siraitia grosvenorii triterpene biosynthetic genes by RNA-seq and digital gene expression analysis. BMC genomics 12(1), 343.
90. Tanaka T., Antonio B.A. and Kikuchi S., The rice annotation project database (RAP-DB): 2008 update, Nucleic Acids Res. 36, 2008, D1028–D1033.
91. Thimmappa, R., Geisler, K., Louveau, T., O'Maille, P. and Osbourn, A., 2014. Triterpene biosynthesis in plants. Annu. Rev. Plant Biol. 65.
92. Tiwari, P., Sangwan, R.S. and Sangwan, N.S., 2016. Plant secondary metabolism linked glycosyltransferases: an update on expanding knowledge and scopes. Biotechnol. Ad. 34(5), 714-739.
93. Tuskan, G.A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A. and Schein, J., 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793), 1596-1604.
94. Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S.K., Troggio, M., Pruss, D. and Salvi, S., 2010. The genome of the domesticated apple (Malus× domestica Borkh.). Nat. Genet. 42(10), 833–839.
95. Vincken, J.-P., Heng, L., de Groot, A., Gruppen, H., 2007. Saponins, classification and occurence in the plant kingdom. Phytochemistry 68, 275–297.
96. Wang, X., 2009. Structure, mechanism and engineering of plant natural product glycosyltransferases. FEBS Lett. 583(20), 3303-3309.
97. Wang, J. and Hou, B., 2009. Glycosyltransferases: key players involved in the modification of plant secondary metabolites. Front. Biol. (Beijing) 4(1), 39-46.
98. Wang, H., Wang, C., Fan, W., Yang, J., Appelhagen, I., Wu, Y., Zhang, P., 2018. A novel glycosyltransferase catalyses the transfer of glucose to glucosylated anthocyanins in purple sweet potato. J. Exp. Bot. 69(22), 5444-5459.
99. Weadge, J.T., Palcic M.M., 2009. Chemistry of Glycosyltransferases, Vol 2. Wiley Encyclopedia of Chemical Biology, pp. 198–211.
100. Wei, W., Wang, P., Wei, Y., Liu, Q., Yang, C., Zhao, G., Yue, J., Yan, X. and Zhou, Z., 2015. Characterization of Panax ginseng UDP-glycosyltransferases catalyzing protopanaxatriol and biosyntheses of bioactive ginsenosides F1 and Rh1 in metabolically engineered yeasts. Mol. Plant 8(9), 1412-1424.
101. Wrabl, J., Grishin, N., 2001. Homology between O-linked GlcNAc transferases and proteins of the glycogen phosphorylase superfamily. J. Mol. Biol. 314, 365–374.
102. Xiang, L., Guo, X., Niu, Y.Y., Chen, S.L. and Luo, H.M., 2012. Full-length cDNA cloning and bioinformatics analysis of PnUGT1 gene in Panax notoginseng. Acta Pharm Sin B. 47(8), 1085-1091.
103. Yan, X., Fan, Y., Wei, W., Wang, P., Liu, Q., Wei, Y., Zhang, L., Zhao, G., Yue, J. and Zhou, Z., 2014. Production of bioactive ginsenoside compound K in metabolically engineered yeast. Cell Res. 24(6), 770–3.
104. Yazaki, K., Arimura, G.I. and Ohnishi, T., 2017. ‘Hidden'terpenoids in Plants: their biosynthesis, localization and ecological roles. Plant Cell Physiol. 58(10), 1615-1621.
105. Yonekura-Sakakibara, K. and Hanada, K., 2011. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 66(1), 182-193.
106. Yue, C.J. and Zhong, J.J., 2005. Purification and characterization of UDPG: ginsenoside Rd glucosyltransferase from suspended cells of Panax notoginseng. Process Biochem. 40(12), 3742-3748.