Functional Characterization of a New Tea (Camellia sinensis) Flavonoid Glycosyltransferase

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 10, 2017, Pages 2074-2083

  Zhao, Xianqian ^a   Wang, Peiqiang ^a   Li, Mingzhuo ^a   Wang, Yeru ^a   Jiang, Xiaolan ^a   Cui, Lilan ^a   Qian, Yumei ^a   Zhuang, Juhua ^a   Gao, Liping ^a   Xia, Tao ^a  

^a ANHUI AGRICULTURAL UNIVERSITY   (China)

Author keywords

Camellia sinensis; flavonoids glycosyltransferase; multisite glycosidation

Indexed keywords

ESCHERICHIA COLI; GLYCOSYLATION; TOBACCO;

BIOCHEMICAL CHARACTERIZATION; CAMELLIA SINENSIS; FUNCTIONAL CHARACTERIZATION; GLYCOSIDATIONS; GLYCOSYL TRANSFERASE; GLYCOSYLATION REACTIONS; KINETIC ANALYSIS; NICOTIANA TABACUM;

FLAVONOIDS;

FLAVANONE DERIVATIVE; FLAVONOID; GLYCOSYLTRANSFERASE; KAEMPFERIDE; KAEMPFEROL; KAEMPFEROL DERIVATIVE; NARINGENIN; PLANT PROTEIN;

CAMELLIA SINENSIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM;

CAMELLIA SINENSIS; ENZYME STABILITY; FLAVANONES; FLAVONOIDS; GLYCOSYLTRANSFERASES; KAEMPFEROLS; KINETICS; PLANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 85015617322     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b05619     Document Type: Article

References (50)

1. Li, J.; Oulee, T. M.; Raba, R.; Amundson, R. G.; Last, R. L. Arabidopsis Flavonoid Mutants Are Hypersensitive to UV-B Irradiation Plant Cell 1993, 5, 171-179 10.2307/3869583
2. Harborne, J. B.; Williams, C. A. Advances in flavonoid research since 1992 Phytochemistry 2000, 55, 481-504 10.1016/S0031-9422(00)00235-1
3. Albert, N. W.; Lewis, D. H.; Zhang, H.; Irving, L. J.; Jameson, P. E.; Davies, K. M. Light-induced vegetative anthocyanin pigmentation in Petunia J. Exp. Bot. 2009, 60, 2191-202 10.1093/jxb/erp097
4. Yamazaki, M.; Gong, Z.; Fukuchi-Mizutani, M.; Fukui, Y.; Tanaka, Y.; Kusumi, T.; Saito, K. Molecular cloning and biochemical characterization of a novel anthocyanin 5-O-glucosyltransferase by mRNA differential display for plant forms regarding anthocyanin J. Biol. Chem. 1999, 274, 7405-11 10.1074/jbc.274.11.7405
5. Auvichayapat, P.; Prapochanung, M.; Tunkamnerdthai, O.; Sripanidkulchai, B. O.; Auvichayapat, N.; Thinkhamrop, B.; Kunhasura, S.; Wongpratoom, S.; Sinawat, S.; Hongprapas, P. Effectiveness of green tea on weight reduction in obese Thais: A randomized, controlled trial Physiol. Behav. 2008, 93, 486-91 10.1016/j.physbeh.2007.10.009
6. Nagao, T.; Hase, T.; Tokimitsu, I. A Green Tea Extract High in Catechins Reduces Body Fat and Cardiovascular Risks in Humans Obesity 2007, 15, 1473-1483 10.1038/oby.2007.176
7. Setiawan, V. W.; Zhang, Z. F.; Yu, G. P.; Lu, Q. Y.; Li, Y. L.; Lu, M. L.; Wang, M. R.; Guo, C. H.; Yu, S. Z.; Kurtz, R. C. Protective effect of green tea on the risks of chronic gastritis and stomach cancer Int. J. Cancer 2001, 92, 600-4 10.1002/ijc.1231
8. Soobrattee, M. A.; Bahorun, T.; Aruoma, O. I. Chemopreventive actions of polyphenolic compounds in cancer BioFactors 2006, 27, 19-35 10.1002/biof.5520270103
9. Wang, H. F.; Provan, G. J.; Helliwell, K. Tea flavonoids: their functions, utilisation and analysis Trends Food Sci. Technol. 2000, 11, 152-160 10.1016/S0924-2244(00)00061-3
10. Kumar, S.; Pandey, A. K. Chemistry and Biological Activities of Flavonoids: An Overview Sci. World J. 2013, 2013, 1 10.1155/2013/162750
11. Lim, E. K.; Ashford, D. A.; Hou, B.; Jackson, R. G.; Bowles, D. J. Arabidopsis glycosyltransferases as biocatalysts in fermentation for regioselective synthesis of diverse quercetin glucosides Biotechnol. Bioeng. 2004, 87, 623-31 10.1002/bit.20154
12. Wang, J.; Hou, B. Glycosyltransferases: key players involved in the modification of plant secondary metabolites Front. Biol. in China 2009, 4, 39-46 10.1007/s11515-008-0111-1
13. Meßner, B.; Thulke, O.; Schäffner, A. R. Arabidopsis glucosyltransferases with activities toward both endogenous and xenobiotic substrates Planta 2003, 217, 138-146
14. Pflugmacher, S.; Sandermann, H. Taxonomic distribution of plant glucosyltransferases acting on XENOBIOTICS fn1 in honour of professor G. H. neil towers 75TH birthday Phytochemistry 1998, 49, 507-511 10.1016/S0031-9422(98)00139-3
15. Achnine, L.; Huhman, D. V.; Farag, M. A.; Sumner, L. W.; Blount, J. W.; Dixon, R. A. Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula Plant J. 2005, 41, 875-887 10.1111/j.1365-313X.2005.02344.x
16. Radominskapandya, A.; Czernik, P. J.; Little, J. M.; Battaglia, E.; Mackenzie, P. I. Structural and functional studies of UDP-glucuronosyltransferases Drug Metab. Rev. 1999, 31, 817-99 10.1081/DMR-100101944
17. Devaiah, S. P.; Owens, D. K.; Sibhatu, M. B.; Sarkar, T. R.; Strong, C. L.; Mallampalli, V. K.; Asiago, J.; Cooke, J.; Kiser, S.; Lin, Z. Identification, recombinant expression, and biochemical analysis of putative secondary product glucosyltransferases from Citrus paradisi J. Agric. Food Chem. 2016, 64, 1957 10.1021/acs.jafc.5b05430
18. Owens, D. K.; Mcintosh, C. A. Identification, recombinant expression, and biochemical characterization of a flavonol 3-O-glucosyltransferase clone from Citrus paradisi Phytochemistry 2009, 70, 1382-1391 10.1016/j.phytochem.2009.07.027
19. Yin, R.; Messner, B.; Faus-Kessler, T.; Hoffmann, T.; Schwab, W.; Hajirezaei, M. R.; von Saint Paul, V.; Heller, W.; Schäffner, A. R. Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation J. Exp. Bot. 2012, 63, 2465-2478 10.1093/jxb/err416
20. Hirotani, M.; Kuroda, R.; Suzuki, H.; Yoshikawa, T. Cloning and expression of UDP-glucose: flavonoid 7- O -glucosyltransferase from hairy root cultures of Scutellaria baicalensis Planta 2000, 210, 1006-1013 10.1007/PL00008158
21. Kumar, R. J. S.; Singh, S.; Sonawane, P. D.; Vishwakarma, R. K.; Khan, B. M. Functional Characterization of a Glucosyltransferase Specific to Flavonoid 7- O -Glucosides from Withania somnifera Plant Mol. Biol. Rep. 2013, 31, 1100-1108 10.1007/s11105-013-0573-4
22. Pang, Y.; Dixon, R. A. A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 14210-5 10.1073/pnas.0805954105
23. Cartwright, A. M.; Lim, E. K.; Kleanthous, C.; Bowles, D. J. A kinetic analysis of regiospecific glucosylation by two glycosyltransferases of Arabidopsis thaliana: domain swapping to introduce new activities J. Biol. Chem. 2008, 283, 15724-31 10.1074/jbc.M801983200
24. Kramer, C. M.; Prata, R. T. N.; Willits, M. G.; Luca, V. D.; Steffens, J. C.; Graser, G. Cloning and regiospecificity studies of two flavonoid glucosyltransferases from Allium cepa Phytochemistry 2003, 64, 1069-76 10.1016/S0031-9422(03)00507-7
25. Kim, B. G.; Sung, S. H.; Ahn, J. H. Biological synthesis of quercetin 3- O-N -acetylglucosamine conjugate using engineered Escherichia coli expressing UGT78D2 Appl. Microbiol. Biotechnol. 2012, 93, 2447-2453 10.1007/s00253-011-3747-8
26. Kim, B. G.; Kim, H. J.; Ahn, J. H. Production of bioactive flavonol rhamnosides by expression of plant genes in Escherichia coli J. Agric. Food Chem. 2012, 60, 11143-8 10.1021/jf302123c
27. Cui, L.; Yao, S.; Dai, X.; Yin, Q.; Liu, Y.; Jiang, X.; Wu, Y.; Qian, Y.; Pang, Y.; Gao, L. Identification of UDP-glycosyltransferases involved in the biosynthesis of astringent taste compounds in tea (Camellia sinensis) J. Exp. Bot. 2016, 67, 2285-2297 10.1093/jxb/erw053
28. Gachon, C. M.; Langlois-Meurinne, M.; Henry, Y.; Saindrenan, P. Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications Plant Mol. Biol. 2005, 58, 229-45 10.1007/s11103-005-5346-5
29. Werner, S. R.; Morgan, J. A. Controlling selectivity and enhancing yield of flavonoid glycosides in recombinant yeast Bioprocess Biosyst. Eng. 2010, 33, 863-871 10.1007/s00449-010-0409-7
30. Quiel, J. A.; Bender, J. Glucose Conjugation of Anthranilate by the Arabidopsis UGT74F2 Glucosyltransferase Is Required for Tryptophan Mutant Blue Fluorescence J. Biol. Chem. 2003, 278, 6275-81 10.1074/jbc.M211822200
31. Moraga, á. R.; Mozos, A. T.; Ahrazem, O.; Gómez-Gómez, L. Cloning and characterization of a glucosyltransferase from Crocus sativusstigmas involved in flavonoid glucosylation BMC Plant Biol. 2009, 9, 1-16 10.1186/1471-2229-9-109
32. Lim, E. K.; Bowles, D. J. A class of plant glycosyltransferases involved in cellular homeostasis EMBO J. 2004, 23, 2915-2922 10.1038/sj.emboj.7600295
33. Lim, E. K. Plant glycosyltransferases: their potential as novel biocatalysts Chem.-Eur. J. 2005, 11, 5486-94 10.1002/chem.200500115
34. Jiang, H.; Engelhardt, U. H.; Thräne, C.; Maiwald, B.; Stark, J. Determination of flavonol glycosides in green tea, oolong tea and black tea by UHPLC compared to HPLC Food Chem. 2015, 183, 30-35 10.1016/j.foodchem.2015.03.024
35. Finger, A.; Engelhardt, U. H.; Wray, V. Flavonol glycosides in tea-kaempferol and quercetin rhamnodiglucosides J. Sci. Food Agric. 1991, 55, 313-321 10.1002/jsfa.2740550216
36. Lin, L. Z.; Chen, P.; Harnly, J. M. New Phenolic Components and Chromatographic Profiles of Green and Fermented Teas J. Agric. Food Chem. 2008, 56, 8130-40 10.1021/jf800986s
37. Jiang, X.; Liu, Y.; Li, W.; Zhao, L.; Meng, F.; Wang, Y.; Tan, H.; Yang, H.; Wei, C.; Wan, X. Tissue-specific, development-dependent phenolic compounds accumulation profile and gene expression pattern in tea plant [Camellia sinensis] PLoS One 2013, 8, e62315-e62315 10.1371/journal.pone.0062315
38. Maiti, I. B.; Hunt, A. G.; Wagner, G. J. Seed-transmissable expression of mammalian metallothionein in transgenic tobacco Biochem. Biophys. Res. Commun. 1988, 150, 640-7 10.1016/0006-291X(88)90440-8
39. Mackenzie, P. I.; Owens, I. S.; Burchell, B.; Bock, K. W.; Bairoch, A.; Belanger, A.; Gigleux, S. F.; Green, M.; Hum, D. W.; Iyanagi, T.; Lancet, D.; Louisot, P.; Magdalou, J.; Roy Chowdhury, J.; Ritter, J. K.; Schachter, H.; Tephly, T. R.; Tipton, K. F.; Nebert, D. W. The UDP glycosyltransferase gene superfamily: recommended nomenclature update based on evolutionary divergence Pharmacogenetics 1997, 7, 255-69 10.1097/00008571-199708000-00001
40. Fraissinet-Tachet, L.; Baltz, R.; Chong, J.; Kauffmann, S.; Fritig, B.; Saindrenan, P. Two tobacco genes induced by infection, elicitor and salicylic acid encode glucosyltransferases acting on phenylpropanoids and benzoic acid derivatives, including salicylic acid FEBS Lett. 1998, 437, 319-323 10.1016/S0014-5793(98)01257-5
41. Chong, J.; Beffa; Saindrenan, P. Downregulation of a pathogen-responsive tobacco UDP-Glc: Phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance Plant Cell 2002, 14, 1093-107 10.1105/tpc.010436
42. Griesser, M.; Vitzthum, F.; Fink, B.; Bellido, M. L.; Raasch, C.; Munoz-Blanco, J.; Schwab, W. Multi-substrate flavonol O-glucosyltransferases from strawberry (Fragaria x ananassa) achene and receptacle J. Exp. Bot. 2008, 59, 2611-2625 10.1093/jxb/ern117
43. Noguchi, A.; Sasaki, N.; Nakao, M.; Fukami, H.; Takahashi, S.; Nishino, T.; Nakayama, T. cDNA cloning of glycosyltransferases from Chinese wolfberry (Lycium barbarum L.) fruits and enzymatic synthesis of a catechin glucoside using a recombinant enzyme (UGT73A10) J. Mol. Catal. B: Enzym. 2008, 55, 84-92 10.1016/j.molcatb.2008.02.001
44. Kim, H. J.; Kim, B. G.; Ahn, J. H. Regioselective synthesis of flavonoid bisglycosides using Escherichia coli harboring two glycosyltransferases Appl. Microbiol. Biotechnol. 2013, 97, 5275-82 10.1007/s00253-013-4844-7
45. Offen, W.; Martinez-Fleites, C.; Yang, M.; Kiat-Lim, E.; Davis, B. G.; Tarling, C. A.; Ford, C. M.; Bowles, D. J.; Davies, G. J. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification EMBO J. 2006, 25, 1396-1405 10.1038/sj.emboj.7600970
46. Yin, Q.; Shen, G.; Chang, Z.; Tang, Y.; Gao, H.; Pang, Y. Involvement of three putative glucosyltransferases from the UGT72 family in flavonol glucoside/rhamnoside biosynthesis in Lotus japonicus seeds J. Exp. Bot. 2016, erw420 10.1093/jxb/erw420
47. Poppenberger, B.; Fujioka, S.; Soeno, K.; George, G. L.; Vaistij, F. E.; Hiranuma, S.; Seto, H.; Takatsuto, S.; Adam, G.; Yoshida, S.; Bowles, D. The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 15253-8 10.1073/pnas.0504279102
48. von Saint Paul, V.; Zhang, W.; Kanawati, B.; Geist, B.; Faus-Keßler, T.; Schmitt-Kopplin, P.; Schäffner, A. R. The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence Plant Cell 2011, 23, 4124-45 10.1105/tpc.111.088443
49. Mo, T.; Liu, X.; Liu, Y.; Wang, X.; Zhang, L.; Wang, J.; Zhang, Z.; Shi, S.; Tu, P. Expanded investigations of the aglycon promiscuity and catalysis characteristic of flavonol 3-O-rhamnosyltransferase AtUGT78D1 from Arabidopsis thaliana RSC Adv. 2016, 6, 84616-84626 10.1039/C6RA16251G
50. Pei, J.; Dong, P.; Wu, T.; Zhao, L.; Fang, X.; Cao, F.; Tang, F.; Yue, Y. Metabolic Engineering of Escherichia coli for Astragalin Biosynthesis J. Agric. Food Chem. 2016, 64, 7966 10.1021/acs.jafc.6b03447