Steviol glycoside biosynthesis

Phytochemistry

Volumn 68, Issue 14, 2007, Pages 1855-1863

  Brandle, J E ^a   Telmer, P G ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Asteraceae; Biosynthesis; Diterpene glycoside; Glucosyltransferase; P450; Stevia; Stevia rebaudiana; Terpene cyclase

Indexed keywords

GLYCOSIDE; GLYCOSYLTRANSFERASE; KAURANE DERIVATIVE; MULTIENZYME COMPLEX; STEVIOL; TERPENE;

ARTICLE; BIOSYNTHESIS; CELL VACUOLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; DITERPENES, KAURANE; GLYCOSIDES; GLYCOSYLTRANSFERASES; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; TERPENES; VACUOLES;

ASTERACEAE; STEVIA REBAUDIANA;

EID: 34447101720     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2007.02.010     Document Type: Article

References (80)

1. Achnine L., Huhman D.V., Farag M.A., Sumner L.W., Blount J.W., and Dixon R.A. Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant J. 41 (2005) 875-887
2. Alves L.M., and Ruddat M. The presence of gibberellin A20 in Stevia rebaudiana and its significance for the biological activity of steviol. Plant Cell Physiol. 20 (1979) 123-130
3. Bartholomew D.M., Van Dyk D.E., Lau S.M., O'Keefe D.P., Rea P.A., and Viitanen P.V. Alternate energy-dependent pathways for the vacuolar uptake of glucose and glutathione conjugates. Plant Physiol. 130 (2002) 1562-1572
4. Beneford D.J., DiNovi M., and Schlatter J. Steviol glycosides. Safety Evaluation of Certain Food Additives. WHO Food Additive Series (2006), WHO, Geneva pp. 117-143
5. Bennett R.D., Lieber E.R., and Heftmann E. Biosynthesis of steviol from (-)-kaurene. Phytochemistry 6 (1967) 1107-1110
6. Bondarev N.I., Sukhanova M.A., Reshetnyak O.V., and Nosov A.M. Steviol glycoside content in different organs of Stevia rebaudiana and its dynamics during ontogeny. Biol. Planta. 47 (2003) 261-264
7. Brandle J.E., Richman A., Swanson A.K., and Chapman B.P. Leaf Ests from Stevia rebaudiana: a resource for gene discovery in diterpene synthesis. Plant Mol. Biol. 50 (2002) 613-622
8. Brandle J.E., and Rosa N. Heritability for yield, leaf: stem ratio and stevioside content estimated from a landrace cultivar of Stevia rebaudiana. Can. J. Plant Sci. 72 (1992) 1263-1266
9. Brandle J.E., Starratt A.N., and Gijzen M. Stevia rebaudiana: its agricultural, biological, and chemical properties. Can. J. Plant Sci. 78 (1998) 527-536
10. Davidson S.E., Swain S.M., and Reid J.B. Regulation of the early GA biosynthesis pathway in pea. Planta 222 (2005) 1010-1019
11. Debeaujon I., Peeters A.J., Leon-Kloosterziel K.M., and Koornneef M. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13 (2001) 853-871
12. DuBois G.E., and Stephenson R.A. Diterpenoid sweeteners. Synthesis and sensory evaluation of stevioside analogues with improved organoleptic properties. J. Med. Chem. 28 (1985) 93-98
13. Firn R.D., and Jones C.G. Natural products - a simple model to explain chemical diversity. Nat. Prod. Rep. 20 (2003) 382-391
14. Fleet C.M., Yamaguchi S., Hanada A., Kawaide H., David C.J., Kamiya Y., and Sun T.P. Overexpression of AtCPS and AtKS in Arabidopsis confers increased ent-kaurene production but no increase in bioactive gibberellins. Plant Physiol. 132 (2003) 830-839
15. Fukuchi-Mizutani M., Okuhara H., Fukui Y., Nakao M., Katsumoto Y., Yonekura-Sakakibara K., Kusumi T., Hase T., and Tanaka Y. Biochemical and molecular characterization of a novel UDP-glucoseanthocyanin 3′-O-glucosyltransferase, a key enzyme for blue anthocyanin biosynthesis, from gentian. Plant Physiol. 132 (2003) 1652-1663
16. Geuns J.M.C. Safety of stevia and stevioside. Recent Res. Dev. Phytochem. 4 (2000) 75-88
17. Geuns J.M.C. Stevioside. Phytochemistry 64 (2003) 913-921
18. Geuns J.M.C., Buyse J., Vankeirsbilck A., Temme E.H.M., Compernolle F., and Toppet S. Identification of steviol glucuronide in human urine. J. Agric. Food Chem. 54 (2006) 2794-2798
19. Geuns J.M.C., Buyse J., Vankeirsbilck A., and Temme E.H.M. Metabolism of stevioside by healthy volunteers. Exp. Biol. Med. 232 (2007) 164-173
20. Goodman C.D., Casati P., and Walbot V. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16 (2004) 1812-1826
21. Gregersen S., Jeppesen P.B., Holst J.J., and Hermansen K. Antihyperglycemic effects of stevioside in type 2 diabetic subjects. Metab. Clin. Exp. 53 (2004) 73-76
22. Grotewold E. The challenges of moving chemicals within and out of cells: insights into the transport of plant natural products. Planta 219 (2004) 906-909
23. Guevara-Garcia A., San Roman C., Arroyo A., Cortes M.E., de la Luz Gutierrez-Nava M., and Leon P. Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-d-erythritol 4-phosphate pathway. Plant Cell 17 (2005) 628-643
24. Hansen K.S., Kristensen C., Tattersall D.B., Jones P.R., Olsen C.E., Bak S., and Moller B.L. The in vitro substrate regiospecificity of recombinant UGT85B1, the cyanohydrin glucosyltransferase from Sorghum bicolor. Phytochemistry 64 (2003) 143-151
25. Hanson J.R., and White A.F. Studies in terpenoid biosynthesis-II: the biosynthesis of steviol. Phytochemistry 7 (1968) 595-597
26. Harada K., Miyasaki T., and Tamura Y. Feeding attraction activity of stevioside for aqautic animals. Nippon Suisan Gakkaishi 59 (1993) 1955
27. Hedden P., and Phillips A.L. Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 5 (2000) 523-530
28. Helliwell C.A., Poole A., Peacock W.J., and Dennis E.S. Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol. 119 (1999) 507-510
29. Helliwell C.A., Sullivan J.A., Mould R.M., Gray J.C., Peacock W.J., and Dennis E.S. A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J. 28 (2001) 201-208
30. Hemmerlin A., Hoeffler J.F., Meyer O., Tritsch D., Kagan I.A., Grosdemange-Billiard C., Rohmer M., and Bach T.J. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J. Biol. Chem. 278 (2003) 26666-26676
31. Hsieh M.H., Chan P., Sue Y.M., Liu J.C., Liang T.H., Huang T.Y., Tomlinson B., Chow M.S., Kao P.F., and Chen Y.J. Efficacy and tolerability of oral stevioside in patients with mild essential hypertensiona two-year, randomized, placebo-controlled study. Clin. Ther. 25 (2003) 2797-2808
32. Hsieh M.H., and Goodman H.M. Functional evidence for the involvement of Arabidopsis IspF homolog in the nonmevalonate pathway of plastid isoprenoid biosynthesis. Planta 223 (2006) 779-784
33. Humphrey T.V., Richman A.S., Menassa R., and Brandle J.E. Spatial organisation of four enzymes from Stevia rebaudiana that are involved in steviol glycoside synthesis. Plant Mol. Biol. 61 (2006) 47-62
34. Huxtable R.J. Pharmacology and toxicology of stevioside, rebaudioside A, and steviol. In: Kinghorn A.D. (Ed). Stevia: The Genus Stevia (2002), Taylor and Francis, London and New York 160-177
35. Hvorup R.N., Winnen B., Chang A.B., Jiang Y., Zhou X.F., and Saier Jr. M.H. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur. J. Biochem. 270 (2003) 799-813
36. Jorgensen K., Rasmussen A.V., Morant M., Nielsen A.H., Bjarnholt N., Zagrobelny M., Bak S., and Moller B.L. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8 (2005) 280-291
37. Julliard J.H., and Douce R. Biosynthesis of the thiazole moiety of thiamin (vitamin B1) in higher plant chloroplasts. Proc. Natl. Acad. Sci. USA 88 (1991) 2042-2045
38. Kasai R., Kaneda N., Tanaka O., Yamasaki K., Sakamoto I., Morimoto K., Okada S., Kitahata S., and Furukawa H. Sweet diterpene-glycosides of leaves of Stevia rebaudiana Bertoni. Synthesis and structure-sweetness relationship of rebaudiosides-A, D, E and their related glycosides. Nippon Kagakukaishi 5 (1981) 726-735 (In Japanese, English abstract)
39. Kim K.K., Sawa Y., and Shibata H. Hydroxylation of ent-kaurenoic acid to steviol in Stevia rebaudiana Bertoni - purification and partial characterization of the enzyme. Arch. Biochem. Biophys. 332 (1996) 223-230
40. Kinghorn A.D., and Soejarto D.D. Current status of stevioside as a sweetening agent for human use. In: Wagner H., Hikino H., and Farnsworth N.R. (Eds). Economic and Medicinal Plant Research vol. 1 (1985), London Academic Press 1-52
41. Klein M., Martinoia E., Hoffmann-Thoma G., and Weissenbock G. A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J. 21 (2000) 289-304
42. Klein M., Martinoia E., and Weissenbock G. Directly energized uptake of beta-estradiol 17-(beta-d-glucuronide) in plant vacuoles is strongly stimulated by glutathione conjugates. J. Biol. Chem. 273 (1998) 262-270
43. Klein M., Weissenbock G., Dufaud A., Gaillard C., Kreuz K., and Martinoia E. Different energization mechanisms drive the vacuolar uptake of a flavonoid glucoside and a herbicide glucoside. J. Biol. Chem. 271 (1996) 29666-29671
44. Lange B.M., and Croteau R. Isoprenoid biosynthesis via a mevalonate-independent pathway in plantscloning and heterologous expression of 1-deoxy-d-xylulose-5-phosphate reductoisomerase from peppermint. Arch. Biochem. Biophys. 365 (1999) 170-174
45. Lange B.M., Wildung M.R., McCaskill D., and Croteau R. A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. USA 95 (1998) 2100-2104
46. Laule O., Fürholz A., Chang H.-S., Zhu T., Wang X., Heifetz P.B., Gruissem W., and Lange B.M. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100 (2003) 6866-6871
47. Lichtenhalter H.K. The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 (1999) 47-65
48. Lim E.K., Higgins G.S., Li Y., and Bowles D.J. Regioselectivity of glucosylation of caffeic acid by a UDP-glucoseglucosyltransferase is maintained in planta. Biochem. J. 373 (2003) 987-992
49. Martinoia E., Massonneau A., and Frangne N. Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol. 41 (2000) 1175-1186
50. McGarvey D.J., and Croteau R. Terpenoid metabolism. Plant Cell 7 (1995) 1015-1026
51. Mitsuhashi N., Ohnishi M., Sekiguchi Y., Kwon Y.U., Chang Y.T., Chung S.K., Inoue Y., Reid R.J., Yagisawa H., and Mimura T. Phytic acid synthesis and vacuolar accumulation in suspension-cultured cells of Catharanthus roseus induced by high concentration of inorganic phosphate and cations. Plant Physiol. 138 (2005) 1607-1614
52. Mosettig E., Beglinger U., Dolder F., Lichti H., Quitt P., and Waters J.A. The absolute configuration of steviol and isosteviol. J. Am. Chem. Soc. 85 (1963) 2305-2309
53. Mu-zuan C., Wei-lan H., Shao-pang C., and De-yao W. Observations of the leaf cell vacuole of Stevia rebaudiana Bertoni under the electron microscope. Acta Bot. Sinica 25 (1983) 426-432 (Chinese, English abstract)
54. Nanayakkara N.P.D., Klocke J.A., Compadre C.M., Hussain R.A., Pezzuto J.M., and Kinghorn A.D. Characterization and feeding deterrent effects on the aphid, Schizaphis graminum, of some derivatives of the sweet compounds, stevioside and rebaudioside A. J. Nat. Prod. 50 (1987) 434-441
55. Otani M., Shitan N., Sakai K., Martinoia E., Sato F., and Yazaki K. Characterization of vacuolar transport of the endogenous alkaloid berberine in Coptis japonica. Plant Physiol. 138 (2005) 1939-1946
56. Pao S.S., Paulsen I.T., and Saier Jr. M.H. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62 (1998) 1-34
57. Pezzuto J.M., Compadre C.M., Swanson S.M., Nanayakkara N.P.D., and Kinghorn A.D. Metabolically activated steviol, the aglycone of stevioside, in mutagenic. Proc. Natl. Acad. Sci. USA 82 (1985) 2478-2482
58. Phillips K.C. Stevia: steps in developing a new sweetener. In: Grenby T.H. (Ed). Developments in Sweeteners-3 (1987), Elsevier Applied Scinece, London and New York 1-27
59. Planas G.M., and Kuc J. Contraceptive properties of Stevia-rebaudiana. Science 162 (1968) 1007
60. Pompon D., Louerat B., Bronine A., and Urban P. Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol. 272 (1996) 51-64
61. Querol J., Campos N., Imperial S., Boronat A., and Rodriguez-Concepcion M. Functional analysis of the Arabidopsis thaliana GCPE protein involved in plastid isoprenoid biosynthesis. FEBS Lett. 514 (2002) 343-346
62. Rea P.A., Li Z.S., Lu Y.P., Drozdowicz Y.M., and Martinoia E. From vacuolar GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 (1998) 727-760
63. Richman A.S., Gijzen M., Starratt A.N., Yang Z., and Brandle J.E. Diterpene synthesis in Stevia rebaudiana: recruitment and up-regulation of key enzymes from the gibberellin biosynthetic pathway. Plant J. 19 (1999) 411-421
64. Richman A., Swanson A., Humphrey T., Chapman R., McGarvey B., Pocs R., and Brandle J. Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J. 41 (2005) 56-67
65. Rodríguez-Concepción M., and Boronat A. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130 (2004) 1079-1089
66. Rohdich F., Wungsintaweekul J., Eisenreich W., Richter G., Schuhr C.A., Hecht S., Zenk M.H., and Bacher A. Biosynthesis of terpenoids: 4-diphosphocytidyl-2C-methyl-d-erythritol synthase of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97 (2000) 6451-6456
67. Rohdich F., Wungsintaweekul J., Luttgen H., Fischer M., Eisenreich W., Schuhr C.A., Fellermeier M., Schramek N., Zenk M.H., and Bacher A. Biosynthesis of terpenoids: 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase from tomato. Proc. Natl. Acad. Sci. USA 97 (2000) 8251-8256
68. Ruddat M., Heftmann E., and Lang A. Biosynthesis of steviol. Arch. Biochem. Biophys. 110 (1965) 496-499
69. Schmitt L., and Tampe R. Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12 (2002) 754-760
70. Shibata H., Sawa Y., Oka T., Sonoke S., Kim K.K., and Yoshioka M. Steviol and steviol-glycosideglucosyltransferase activities in Stevia rebaudiana Bertoni-purification and partial characterization. Arch. Biochem. Biophys. 321 (1995) 390-396
71. Shibata H., Sonoke S., Ochiai H., Nishihashi H., and Yamada M. Glucosylation of steviol and steviol-glucosides in extracts from Stevia rebaudiana Bertoni. Plant Physiol. 95 (1991) 152-156
72. Soejarto D.D. Botany of Stevia and Stevia rebaudiana. In: Kinghorn A.D. (Ed). Stevia: The genus Stevia (2002), Taylor and Francis, London and New York 18-39
73. Soejarto D.D. Ethnobotany of Stevia and Stevia rebaudiana. In: Kinghorn A.D. (Ed). Stevia: The Genus Stevia (2002), Taylor and Francis, London and New York 40-67
74. Starratt A.N., Kirby C.W., Pocs R., and Brandle J.E. Rebaudioside F, a diterpene glycoside from Stevia rebaudiana. Phytochemistry 59 (2002) 367-370
75. Synder B.A., and Nicholson R.L. Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248 (1990) 1637-1639
76. Tanaka O. Improvement of taste of natural sweeteners. Pure Appl. Chem. 69 (1997) 675-683
77. Tanaka T., Kohda H., Tanaka O., Chen F.-H., Chou W.-H., and Leu J.-L. Rubusoside (β-d-glucosyl ester of 13-O-β-d-glucosyl-steviol), a sweet principle of Rubus chingii hu (Rosaceae). Agric. Biol. Chem. 45 (1981) 2165-2166
78. Totté N., Charon L., Rohmer M., Compernolle F., Baboeuf I., and Geuns J.M.C. Biosynthesis of the diterpenoid steviol, an ent-kaurene derivative from Stevia rebaudiana Bertoni, via the methylerythritol phosphate pathway. Tetrahedron Lett. 41 (2000) 6407-6410
79. Totté N., Van den Ende W., Van Damme E.J.M., Compernolle F., Baboeuf I., and Geuns J.M.C. Cloning and heterologous expression of early genes in gibberellin and steviol biosynthesis via the methylerythritol phosphate pathway in Stevia rebaudiana. Can. J. Bot. 81 (2003) 517-522
80. Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64 (2003) 3-19