Monoterpenoid Indole Alkaloid Biosynthesis

Plant Metabolism and Biotechnology

Volumn , Issue , 2011, Pages 263-291

  De Luca, Vincenzo ^a  

^a BROCK UNIVERSITY   (Canada)

Author keywords

Deoxyxylulose 5 phosphate reductoisomerase (DXR); Jasmonate and elicitor responsive promoter element (JERE); Monoterpenoid Indole Alkaloid (MIA) Biosynthesis; Monoterpenoid Indole Alkaloid Biosynthesis; Monoterpenoid indole alkaloids (MIAs); Tryptophan decarboxylase (TDC)

Indexed keywords

EID: 84866521533     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781119991311.ch10     Document Type: Chapter

References (120)

1. Aerts, R. and De Luca, V. (1992) Phytochrome is involved in the light-activation of vindoline biosynthesis in Catharanthus. Plant Physiol., 100, 1029-1032.
2. Ayora-Talavera, T., Chappell, J., Lozoya-Gloria, E. and Loyola-Vargas, V.M. (2002) Overexpression in Catharanthus roseus hairy roots of a truncated hamster 3-hydroxy-3-methylglutaryl-CoA reductase gene. App. Biochem. Biotech., 97, 135-145.
3. Barleben, L., Panjikar, S., Ruppert, M., Koepke, J., Stöckigt J. (2007) Molecular architecture of strictisidine glucosidase: the gateway to the biosynthesis of the monoterpenoid indole alkaloid family. Plant Cell, 19, 2886-2897.
4. Balsevich, J., DeLuca, V. and Kurz, W.G.W. (1986) Altered alkaloid pattern in dark-grown seedlings of Catharanthus roseus. Isolation and characterization of 4-desacetoxyvindoline, a novel indole alkaloid and proposed precursor of vindoline. Heterocycles, 24, 2415-2421.
5. Beninger, C.W., Cloutier, R.R., Monteiro, M.A. and Grodzinski, B. (2007) The distribution of two major iridoids in different organs of Antirrhinum majus L. at selected stages of development. J. Chem. Ecol., 33, 731-747.
6. Bernhardt, P., McCoy, E. and O'Connor, S.E. (2007) Rapid identification of enzyme variants for reengineered alkaloid biosynthesis in periwinkle. Chem. Biol., 14, 888-897.
7. Burlat, V., Oudin, A., Courtois, M., Rideau, M., St-Pierre, B. (2004) Co-expression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J., 38, 131-141.
8. Burse, A., Schmidt, A., Frick, S., Kuhn, J., Gershenzon, J., Boland, W. (2007) Iridoid biosynthesis in Chrysomelina larvae: fat body produces early terpenoid precursors. Insect Biochem. Mol. Biol., 37, 255-265.
9. Cacacea, S., Schröder, G., Wehingera, E., Strack, D., Schmidt, J., Schröder, J. (2003) A flavonol O-methyltransferase from Catharanthus roseus. Phytochemistry, 62, 127-137.
10. Canel, C., Lopes-Cardoso, I., Whitmer, S., van der Fits, L., Pasquali, G., van der Heijden, R., Hoge, J.H.C., Verpoorte, R. (1998) Effects of over-expression of strictosidine synthase and tryptophan decarboxylase on alkaloid production by cell cultures of Catharanthus roseus. Planta, 205, 414-419.
11. Chahed, K., Oudin, A., Guivarc'h, N., Hamdi, S., Chénieux, J.C., Rideau, M., Clastre, M. (2000) 1-deoxy-D-xylulose-5-phosphate synthase from perwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant. Physiol. Biochem., 38, 559-566.
12. Chen, S., Galan, M.C., Coltharp, C. and O'Connor, S.E. (2006) Redesign of a central enzyme in alkaloid biosynthesis. Chem. Biol., 13, 1137-1141.
13. Collu, G., Unver, N., Peltenburg-Looman, A.M., van der Heijden, R., Verpoorte, R., Memelink, J. (2001) Geraniol-10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis. FEBS Lett., 508, 215-220.
14. Contin, A., van der Heijden, R., Lefeber, A.W. and Verpoorte, R. (1998) The iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture. FEBS Lett., 434, 413-416.
15. Courdavault, V., Thiersault, M., Courtois, M., Gantet, P., Oudin, A., Doireau, P., St-Pierre, B., Giglioli-Guivarc'h, N. (2005) CaaX-prenyltransferases are essential for expression of genes involved in the early stages of monoterpenoid biosynthetic pathway in Catharanthus roseus cells. Plant Mol. Biol., 57, 855-870.
16. Courdavault, V., Burlat, V., St-Pierre, B. and Giglioli-Guivarc'h, N. (2009) Proteins prenylated by type I protein geranylgeranyltransferase act positively on the jasmonate signalling pathway triggering the biosynthesis of monoterpene indole alkaloids in Catharanthus roseus. Plant Cell Rep., 28, 83-93.
17. De Luca, V., Balsevich, J., Tyler, R.T., Eilert, U., Panchuk, B., Kurz, W.G.W. (1986) Biosynthesis of indole alkaloids: developmental regulation of the biosynthetic pathway from tabersonine to vindoline in Catharanthus roseus. J. Plant Physiol., 125, 147-156.
18. De Luca, V. and Cutler, A.J. (1987) Subcellular localization of enzymes involved in indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol., 85, 1099-1102.
19. De Luca V., Fernandez J.A., Campbell D. and Kurz W.G.W. (1988) Developmental regulation of enzymes of indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol., 86, 447-450.
20. De Luca, V., Marineau, C. and Brisson, N. (1989) Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases. Proc. Natl. Acad. Sci. USA, 86, 2582-2586.
21. De Luca, V. and St-Pierre, B. (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci., 5, 349-364.
22. Dethier, M. and De Luca, V. (1993) Partial purification of an N-methyltransferase involved in vindoline biosynthesis in Catharanthus roseus. Phytochemistry, 32, 673-678.
23. Dutta, A., Batra, J., Pandey-Rai, S., Singh, D., Kumar, S., Sen, J. (2005) Expression of terpenoid indole alkaloid biosynthetic pathway genes corresponds to accumulation of related alkaloids in Catharanthus roseus (L.) G. Don. Planta, 220, 376-383.
24. El-Sayed, M. and Verpoorte, R. (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem. Rev., 6, 277-305.
25. Facchini, P.J. and De Luca, V. (2008) Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant J., 54, 763-784.
26. Fernandez, J.A., Owen, T.G., Kurz, W.G.W. and De Luca, V. (1989) Immunological detection and quantitation of tryptophan decarboxylase in developing Catharanthus roseus seedlings. Plant Physiol., 91, 79-84.
27. Froehlich, J.E., Itoh, A. and Howe, G.A. (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol., 125, 306-317.
28. Gantet, P., Imbault, N., Thiersault, M. and Doireau, P. (1998) Necessity of a functional octadecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant Cell Physiol., 39, 220-225.
29. Geerlings, A., Ibanez, M.M., Memelink, J., van der Heijden, R., Verpoorte, R. (2000). Molecular cloning and analysis of strictosidine β-D-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J. Biol. Chem., 275, 3051-3056.
30. Goossens, A. and Rischer, H. (2007) Implementation of functional genomics for gene discovery in alkaloid producing plants. Phytochem. Rev., 6, 35-49.
31. Guirimand. G., Burlat, V., Oudin, A., Lanoue, A., St-Pierre. B., Courdavault, V. (2009) Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and its application to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep., 28, 1215-1234.
32. Guiso, M. and Scarpati, M.L. (1969) Iridoids.VI. Isolation of 5-O-β-glucosylantirrhinoside from Antirrhinum majus or tortuosum. Gazz. Chim. Ital., 99, 800-806.
33. Hedhili, S., Courdavault, V., Giglioli-Guivarc'h, N. and Gantet, P. (2007) Regulation of the terpene moiety biosynthesis of Catharanthus roseus terpene indole alkaloids Phytochem. Rev., 6, 341-351.
34. Helliwell, C.A., Sullivan, J.A., Mould R.M., Gray J.C., Peacock W.J., Dennis E.S. (2001) A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastid and endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J., 28, 201-208.
35. Hisiger, S. and Jolicoeur, M. (2007) Analysis of Catharanthus roseus alkaloids by HPLC. Phytochem. Rev., 6, 207-234.
36. Hsiang, Y.H. Hertzberg, R., Hecht, S. and Liu, L.F. (1985) Camptothecin induces proteinlinked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem., 260, 14873-14878.
37. Hughes, E.H., Hong, S.B., Gibson, S.I., Shanks, J.V., San, K.Y. (2004) Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab. Eng., 6, 268-276.
38. + oxidoreductase of Rauwolfia serpentina cells: the key enzyme in biosynthesis of monoterpene alcohols. J. Biochem., 109, 341-347.
39. Irmler, S., Schröder, G. St-Pierre, B., Crouch, N.P., Hotze, M., Schmidt, J., Strack, D., Mattern, U. Schröder, J. (2000) Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A2 as secologanin synthase. Plant J., 24, 797-804.
40. Katano, N., Yamamoto, H., Iio, R. and Inoue, K. (2001) 7-deoxyloganin 7-hydroxylase in Lonicera japonica cell cultures. Phytochemistry, 58, 53-58.
41. Kutchan, T.M. (1989) Expression of enzymically active cloned strictosidine synthase from the higher plant Rauvolfia serpentina in Escherichia coli. FEBS Lett., 257, 127-130.
42. Laflamme, P., St-Pierre, B. and De Luca, V. (2001) Molecular and biochemical analysis of a Madagascar periwinkle root-specific minovincinine-19-hydroxy-O-acetyltransferase. Plant Physiol., 125, 189-198.
43. Lange, B.M., Wildung, M.R., Stauber, E.J., Sanchez, C., Pouchnik, D., and Croteau, R. (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc. Natl. Acad. Sci. USA, 97, 2934-2939.
44. Levac, D., Murata, J., Kim, W.S. and De Luca, V. (2008) Application of carborundum abrasion for investigating leaf epidermis: molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase. Plant J., 53, 225-236.
45. Lopez-Meyer, M. and Nessler, C.L. (1997) Tryptophan decarboxylase is encoded by two autonomously regulated genes in Camptotheca acuminata which are differentially expressed during development and stress. Plant J., 11, 1167-1175.
46. Lorence, A. and Nessler, C.L. (2004) Camptothecin: over four decades of surprising findings. Phytochemistry, 65, 2735-2749.
47. Loris, E.A., Panjikar, S., Ruppert, M., Barleben, L., Unger, M., Schuebel, H., Stöckigt, J. (2007) Structure-based engineering of strictosidine synthase: auxiliary for alkaloid libraries. Chem. Biol., 14, 979-985.
48. Loyola-Vargas, V.M., Galaz-Ávalos, R.M. and Kú-Cauich, R. (2007) Catharanthus biosynthetic enzymes: the road ahead. Phytochem. Rev., 6, 307-339.
49. Ma, X., Koepke, J., Bayer, A., Fritzsch, G., Michel, H., Stöckigt, J. (2005) Crystallization and preliminary X-ray analysis of native and selenomethionyl vinorine synthase from Rauvolfia serpentina. Acta Crystallogr. D Biol. Crystallogr., 61, 694-696.
50. Ma, X., Panjikar, S., Koepke, J., Loris, E., Stöckigt, J. (2006) The structure of Rauvolfia serpentina strictosidine synthase is a novel six-bladed beta-propeller fold in plant proteins. Plant Cell, 18, 907-920.
51. Madyastha, K.M., Guarnaccia, R., Baxter, C. and Coscia, C.J. (1973) S-adenosyl-Lmethionine: loganic acid methyltransferase. J. Biol. Chem., 248, 2497-2501.
52. Magnotta, M., Murata, J., Chen, J. and De Luca, V. (2006) Identification of a low vindoline accumulating cultivar of Catharanthus roseus (L.) G. Don by alkaloid and enzymatic profiling. Phytochemistry, 67, 1758-1764.
53. Magnotta, M., Murata, J., Chen, J. and De Luca V. (2007) Expression of deacetylvindoline-4-O-acetyltransferase in Catharanthus roseus hairy roots. Phytochemistry, 68, 1922-1931.
54. Mahroug, S., Courdavault, V., Thiersault, M., St-Pierre, B., Burlat, V. (2006) Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs. Planta, 223, 1191-1200.
55. Mahroug, S., Burlat, V. and St-Pierre, B. (2007) Cellular and sub-cellular organisation of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Phytochem. Rev., 6, 363-381.
56. McCoy, E. and O'Connor, S.E. (2006) Directed biosynthesis of alkaloid analogs in the medicinal plant Catharanthus roseus. J. Am. Chem. Soc., 128, 14276-14277.
57. McKnight, T.D., Roessner, C.A., Devagupta, R., Scott, A.I., Nessler, C.L. (1990) Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus. Nucleic Acids Res., 18, 4939.
58. McKnight, T.D., Bergey, D.R., Burnett, R.J. and Nessler, C.L. (1991) Expression of enzymatically active and correctly targeted strictosidine synthase in transgenic tobacco plants. Planta, 185, 148-152.
59. Memelink, J. (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry, 70, 1560-1570.
60. Memelink, J. and Gantet, P. (2007) Transcription factors involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Phytochem. Rev., 6, 353-362.
61. Menke, F.L.H., Champion, A., Kijne, J.W. and Memelink, J. (1999) A novel jasmonateand elicitor-responsive element in the periwinkle secondarymetabolite biosynthetic gene Str interacts with a jasmonate-and elicitor inducible AP2-domain transcription factor, ORCA2. EMBO J., 18, 4455-4463.
62. Morgan, J. and Shanks, J. (1999) Inhibitor studies of tabersonine metabolism in C. roseus hairy roots. Phytochemistry, 51, 61-68.
63. Moyano, E., Osuna, L., Bonfill, M., Cusido, R.M., Palazon, J., Tortoriello, J., Pinol, M.T. (2005) Bioproduction of triterpenes on plant cell cultures of Panax ginseng and Galphimia glauca. Rec. Res. Devel. Plant Sci., 3, 195-213.
64. Murata, J. and De Luca, V. (2005) Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant J., 44, 581-594.
65. Murata, J., Bienzle, D., Brandle, J.E., Sensen, C.W., De Luca, V. (2006) Expressed sequence tags from Madagascar periwinkle (Catharanthus roseus). FEBS Lett., 580, 4501-4507.
66. Murata, J., Roepke J., Gordon, H. and De Luca V. (2008) 'Surfaceome' analysis of leaf epidermal cells in Catharanthus roseus reveals its biochemical specialization. Plant Cell, 38, 131-141.
67. O'Connor, S.E. and Maresh, J.M. (2006) Chemistry and biology of terpene indole alkaloid biosynthesis. Nat. Prod. Rep,. 23, 532-547.
68. Oudin, A., Courtois, M., Rideau, M. and Clastre, M. (2007a) The iridoid pathway in Catharanthus roseus alkaloid biosynthesis. Phytochem. Rev., 6, 259-276.
69. Oudin, A., Mahroug, S., Courdavault, V., Hervouet, N., Zelwer, C., Rodriguez-Concepcion, M., St-Pierre, B., Burlat, V. (2007b) Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Mol. Biol., 65, 13-30.
70. Ouwerkerk, P.B.F. and Memelink, J. (1999) AG-box element from the Catharanthus roseus strictosidine synthase (Str) gene promoter confers seed-specific expression in transgenic tobacco plants. Mol. Gen. Genet., 261, 635-643.
71. Pasquali, G., Porto, D.D. and Fett-Neto, A.G. (2006) Metabolic engineering of cell cultures versus whole plant complexity in production of bioactive monoterpene indole alkaloids: recent progress related to an old dilemma. J. Biosci. Bioeng., 101, 287-296.
72. Pauw, B., Hilliou, F.A.O., Sandonis, M.V., Chatel, G., de Wolf, C.J.F., Champion, A., Pré, M., van Duijn, B., Kijne, J.W., Van Der Fits, L., Memelink, J. (2004). Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. J. Biol. Chem., 279, 52940-52948.
73. Pereira, D.M., Ferreres, F., Oliveira, J.M., Gaspar L, Faria J, Valentão P, Sottomayor M, Andrade PB. (2010) Pharmacological effects of Catharanthus roseus root alkaloids in acetylcholinesterase inhibition and cholinergic neurotransmission. Phytomedicine, 153, 980-987.
74. Ramani, S. and Jayabaskaran, C. (2008) Enhanced catharanthine and vindoline production in suspension cultures of Catharanthus roseus by ultraviolet-B light. J. Mol. Signal., 3, 1-9.
75. Rischer, H., Oreši, M., Seppänen-Laakso, T., Katajamaa, M., Lammertyn, F., Ardiles-Diaz, W., Van Montagu, M.C.E., Inzé, D., Oksman-Caldentey, K.M., Goossens, A. (2006) Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells. Proc. Natl. Acad. Sci. USA, 103, 5614-5619.
76. Rodriguez, S., Compagnon, V., Crouch, N.P., St. Pierre, B., De Luca, V. (2003) Jasmonateinduced epoxidation of tabersonine by cytochrome P-450 in hairy root cultures of Catharanthus roseus. Phytochemistry, 64, 401-409.
77. Rosenthal, C., Mueller, U., Panjikar, S., Sun, L., Ruppert, M., Zhao, Y., Stöckigt, J. (2006) Expression, purification, crystallization and preliminary X-ray analysis of perakine reductase, a new member of the aldo-keto reductase enzyme superfamily from higher plants. Acta Crystallogr., F62, 1286-1289.
78. Roytrakul, S. and Verpoorte, R. (2007) Role of vacuolar transporter proteins in plant secondary metabolism: Catharanthus roseus cell culture. Phytochem. Rev., 6, 383-396.
79. Runguphan, W., Maresh, J.J. and O'Connor, S.E. (2009) Silencing of tryptamine biosynthesis for production of nonnatural alkaloids in plant culture. Proc. Nat. Acad. Sci. USA, 106, 13673-13678.
80. Ruppert, M., Ma, X. and Stöckigt, J. (2005) Alkaloid biosynthesis in Rauvolfia - cDNA cloning of major enzymes of the ajmaline pathway. Curr. Org. Chem., 9, 1431-1444.
81. Ruppert, M., Panjikar, S., Barleben, L. and Stöckigt, J. (2006) Heterologous expression, purification, crystallization and preliminary X-ray analysis of raucaffricine glucosidase, a plant enzyme specifically involved in Rauvolfia alkaloid biosynthesis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 62, 257-260.
82. Sampaio-Santosa, I. and Kaplan, A.C. (2001) Biosynthetic significance of iridoids in chemosystematics. J. Bras. Chem. Soc., 12, 144-153.
83. Sanchez Iturbe, P., Galaz Avalos, R.M. and Loyola Vargas, V.M. (2005) Determination and partial purification of a monoterpene cyclase from Catharanthus roseus hairy roots. Phyton, 55-69.
84. Schilmiller, A.L., Last, R.L. and Pichersky, E. (2008) Harnessing plant trichome biochemistry for the production of useful compounds. Plant J., 54, 702-711.
85. Schröder, G., Unterbusch, E., Kaltenbach, M., Schmidt, J., Strack, D., De Luca, V., Schröder, J. (1999) Light-induced cytochrome P450-dependent enzyme in indole alkaloid biosynthesis: tabersonine-16-hydroxylase. FEBS Lett., 458, 97-102.
86. Schröder, G., Wehinger, E., Lukačin, R., Wellmann, F., Seefelder, W., Schwab, W. and Schröder, J. (2004) Flavonoid methylation: a novel 4'-O-methyltransferase from Catharanthus roseus, and evidence that partially methylated flavanones are substrates of four different flavonoid dioxygenases. Phytochemistry, 65, 1085-1094.
87. Shanks, J.V., Bhadra, R., Morgan, J., Rijhwani, S., Vani, S. (1998) Quantification of metabolites in the indole alkaloid pathways of Catharanthus roseus: implications for metabolic engineering. Biotechnol. Bioeng., 58, 333-338.
88. Shukla, A.K., Shasany, A.K., Gupta, M.M. and Khanuja, S.P.S. (2006) Transcriptome analysis in Catharanthus roseus leaves and roots for comparative terpenoid indole alkaloid profiles. J. Exp. Bot., 57, 3921-3932.
89. Sirikantaramas, S., Asano, T., Sudo, H., Yamazaki, M., Saito, K. (2007) Camptothecin: therapeutic potential and biotechnology. Curr. Pharm. Biotech., 8, 196-202.
90. Sirikantaramas, S., Yamazaki, M. and Saito, K. (2008) Mutations in topoisomerase I as a self-resistance mechanism coevolved with the production of the anticancer alkaloid camptothecin in plants. Proc. Nat Acad. Sci. USA, 105, 6782-6786.
91. Sottomayor, M., Lopez-Serrano, M., DiCosmo, F. and Ros Barcelo, A. (1998) Purification and characterization of alpha-3',4'-anhydrovinblastine synthase (peroxidase-like) from Catharanthus roseus (L.) G. Don. FEBS Lett., 428, 299-303.
92. Stevens, L.H., Blom, T.J.M. and Verpoorte, R. (1993) Subcellular localization of tryptophan decarboxylase, strictosidine synthase and strictosidine glucosidase in suspensioncultured cells of Catharanthus roseus and Tabernaemontana divaricata. Plant Cell Rep., 12, 573-576.
93. Stöckigt, J., Panjikar, S., Ruppert, M., Barleben, L., Ma, X., Loris, E., Hill, M. (2007) The molecular architecture of major enzymes from ajmaline biosynthetic pathway. Phytochem. Rev., 6, 15-34.
94. St-Pierre, B. and De Luca, V. (1995) A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol., 109, 131-139.
95. St-Pierre, B., Laflamme, P., Alarco, A.M. and De Luca, V. (1998) The terminal Oacetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. Plant J., 14, 703-713.
96. St-Pierre, B., Vazquez-Flota, F.A. and De Luca, V. (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell, 11, 887-900.
97. Tabata, H. (2004) Paclitaxel production by plant-cell-culture technology. Adv. Biochem. Engineer. Biotechnol., 7, 1-23.
98. Tian, L., Musetti, V., Kim, J., Magallanes-Lundback, M., DellaPenna, D. (2003) The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid ε-ring hydroxylation activity. Proc. Natl. Acad. Sci. USA, 101, 402-407.
99. Uesato, S., Ogawa, Y., Inouye, H., Saiki, K., Zenk, M.H. (1986) Synthesis of iridodial by cell-free extracts from Rauwolfia serpentina cell suspension cultures. Tetrahedron Lett., 27, 2893-2896.
100. Uesato, S., Ikeda, H., Fujita, T., Inouye, H., Zenk, M.H. (1987) Elucidation of iridodial formation mechanism. Partial purification and characterization of the novel monoterpene cyclase from Rauwolfia serpentina cell suspension cultures. Tetrahedron Lett., 28, 4431-4434.
101. Usia, T., Watabe, T., Kadota, S. and Tezuka, Y. (2005) Cytochrome P450 2D6 (CYP2D6) inhibitory constituents of Catharanthus roseus. Biol. Pharm. Bull., 28, 1021-1024.
102. van der Fits, L. and Memelink, J. (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289, 295-297.
103. van der Fits, L., Zhang, H., Menke, F.L.H., Deneka, M., Memelink, J. (2000) A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a jasmonateindependent signal transduction pathway. Plant Mol. Biol., 44, 675-685.
104. van der Fits, L., Hilliou, F. and Memelink, J. (2001) T-DNA activation tagging as a tool to isolate regulators of a metabolic pathway from a genetically non-tractable plant species. Transgenic Res., 10, 513-521.
105. van der Heijden, R., Jacobs, D.I., Snoeijer, W., Hallard, D., Verpoorte R. (2004) The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr. Med. Chem., 11, 607-628.
106. Vazquez-Flota, F., De Carolis, E., Alarco, A.M. and De Luca, V. (1997) Molecular cloning and characterization of desacetoxyvindoline-4-hydroxylase, a 2-oxoglutarate dependentdioxygenase involved in the biosynthesis of vindoline in Catharanthus roseus (L.) G. Don. Plant Mol. Biol., 34, 935-948.
107. Vazquez-Flota, F. and De Luca, V. (1998) Developmental and light regulation of desacetoxyvindoline-4-hydroxylase in Catharanthus roseus (L.) G. Don. Plant Physiol., 117, 1351-1362.
108. Vazquez-Flota, F., De Luca, V., Carrillo-Pech, M., Canto-Flick, A., De Lourdes Miranda-Ham, M. (2002) Vindoline biosynthesis is transcriptionally blocked in Catharanthus roseus cell suspension cultures. Mol. Biotech., 22, 1-8.
109. Veau, B., Courtois, M., Oudin, A., Chénieux, J.C., Rideau, M., Clastre, M. (2000) Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochim. Biophys. Acta, 1517, 159-163.
110. Vom Endt, D., Soares e Silva, M., Kijne, J.W., Pasquali, G., Memelink, J. (2007) Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-Hook DNA-binding proteins. Plant Physiol,. 144, 1680-1689.
111. Wang, W., Wang, Y., Zhang, Q., Qi, Y, Guo, D. (2009) Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. BMC Genomics, 10, 465.
112. Whitmer, S., Canel, C., Hallard, D., Goncalves, C., Verpoorte, R. (1998) Influence of precursor availability on alkaloid accumulation by a transgenic cell line of Catharanthus roseus. Plant Physiol., 116, 853-857.
113. Yamamoto, H., Katano, N., Ooi, A. and Inoue, K. (1998) Transformation of loganin and 7-deoxyloganin into secologanin by Lonicera japonica cell suspension cultures. Phytochemistry, 50, 417-422.
114. Yamamoto, H., Katano, N., Ooi, A. and Inoue, K. (2000) Secologanin synthase, which catalyzes the oxidative cleavage of loganin into secologanin, is a cytochrome P450. Phytochemistry, 53, 7-12.
115. Yamazaki, Y., Sudo, H., Yamazaki, M., Aimi, N., Saito, K. (2003) Camptothecin biosynthetic genes in hairy roots of Ophiorrhiza pumila: cloning, characterization and differential expression in tissues and by stress compounds. Plant Cell Physiol., 44, 395-403.
116. 13C] glucose. Plant Physiol., 134, 161-170.
117. Zagrobelny, M., Scheibye-Alsing, K., Bjerg Jensen, N., Lindberg Moller, B, Gorodkin, J, Bak, S. (2009) 454 pyrosequencing based transcriptome analysis of Zygaena filipendulae with focus on genes involved in biosynthesis of cyanogenic glucosides. BMC Genomics, 10, 574.
118. Zárate, R. and Verpoorte, R. (2007) Strategies for the genetic modification of the medicinal plant Catharanthus roseus (L.) G. Don. Phytochem. Rev., 6, 475-491.
119. Zhao, J. and Verpoorte, R. (2007) Manipulating indole alkaloid production by Catharanthus roseus cell cultures in bioreactors: from biochemical processing to metabolic engineering. Phytochem. Rev., 6, 435-457.
120. Zhou, M.L., Shao, J.R. and Tang, Y.X. (2009) Production and metabolic engineering of terpenoid indole alkaloids in cell cultures of the medicinal plant Catharanthus roseus (L.) G. Don (Madagascar periwinkle). Biotechnol. Appl. Biochem., 52, 313-323.