The iridoid pathway in Catharanthus roseus alkaloid biosynthesis

Phytochemistry Reviews

Volumn 6, Issue 2-3, 2007, Pages 259-276

  Oudin, Audrey ^a   Courtois, Martine ^a   Rideau, Marc ^a   Clastre, Marc ^a  

^a UNIVERSITÉ DE TOURS   (France)

Author keywords

Cross talk; Madagascar periwinkle; Methyl erythritol phosphate pathway; Mevalonate pathway; Secologanin derived monoterpene indole alkaloids; Terpenoid pathway

Indexed keywords

CAROTENOID; COMPLEMENTARY DNA; DEOXYLOGANIC ACID; DIMETHYLALLYL DIPHOSPHATE; ENZYME; FOSMIDOMYCIN; GERANIOL 10 HYDROXYLASE; HORMONE; INDOLE ALKALOID; IRIDOID; ISOPENTENYL DIPHOSPHATE; ISOPRENOID; LOGANIC ACID; LOGANIN; METHYLERYTHRITOL PHOSPHATE; MEVALONIC ACID; MEVINOLIN; SECOLOGANIC ACID; SECOLOGANIN; SECOLOGANIN SYNTHASE; SERPENTINE; SITOSTEROL; STEROL DERIVATIVE; TERPENE DERIVATIVE; TRANSCRIPTION FACTOR; TRYPTAMINE; UNCLASSIFIED DRUG;

BIOSYNTHESIS; BIOTECHNOLOGY; CATHARANTHUS ROSEUS; CYTOSOL; DNA DETERMINATION; DRUG SYNTHESIS; GENE CONTROL; GENE FUNCTION; ISOMERIZATION; METABOLIC ENGINEERING; METABOLISM; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENYLATION; PRIORITY JOURNAL; REGULATOR GENE; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

APOCYNACEAE; CATHARANTHUS ROSEUS;

EID: 34249874591     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-006-9054-9     Document Type: Review

References (110)

1. Arigoni D, Sagner S, Latzel C, Eisenreich W, Bacher A, Zenk MH (1997) Terpenoid biosynthesis from 1-deoxy-d-xylulose in higher plants by intramolecular skeletal rearrangement. Proc Natl Acad Sci USA 94:10600-10605
2. Arvy MP, Imbault N, Naudascher F, Thiersault M, Doireau P (1994) 2,4-d and alkaloid accumulation in periwinkle cell suspensions. Biochimie 76:410-416
3. Botella-Pavia P, Besumbes O, Phillips MA, Carratero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188-199
4. Bouvier F, Suire C, d'Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24:241-252
5. Brechbühler-Bader S, Coscia CJ, Loew P, von Szczepanski Ch, Arigoni D (1968) The chemistry and biosynthesis of loganin. Chem Commun:136-137
6. Bruneton J (1999) Pharmacognosie, phytochimie, plantes médicinales, Lavoisier ed, Paris, 1136 pp
7. Burke C, Croteau R (2002) Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch Biochem Biophys 405:130-136
8. 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
9. Campbell M, Hahn FM, Poulter CD, Leustek T (1997) Analysis of the isopentenyl diphosphate isomerase gene family from Arabidopsis thaliana. Plant Mol Biol 36:323-328
10. Canel C, Lopez-Cardoso MI, Whitmer S, van der Fits L, Pasquali G, van der Heijden R, Hoge JHC, 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. Canto-Canché BB, Loyola-Vargas VM (2001) Multiple forms of NADPH-cytochrome P450 oxidoreductases in the Madagascar periwinkle Catharanthus roseus. In vitro Cell Dev Biol 37:622-628
12. Canto-Canché BB, Meijer AH, Collu G, Verpoorte R, Loyola-Vargas VM (2005) Characterization of a polyclonal antiserum against the monoterpene monooxygenase, geraniol 10-hydroxylase from Catharanthus roseus. J. Plant Physiol 162:393-402
13. Chahed K, Oudin A, Guivarc'h N, Hamdi S, Chénieux JC, Rideau M, Clastre M (2000) 1-deoxy-d-xylulose-5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole-producing cells. Plant Physiol Biochem 38:559-566
14. Clastre M (1993) Purification et caractérisation de la géranyldiphosphate synthétase de cellules de Vitis vinifera L. cv. Muscat de Frontignan cultivées in vitro. Thèse d'Université, Ecole Nationale Supérieure Agronomique de Toulouse, 81 pp
15. Clastre M, Bantignies B, Feron G, Soler E, Ambid C (1993) Purification and characterization of geranyl diphosphate synthase from Vitis vinifera L. cv. Muscat de Frontignan cell cultures. Plant Physiol 102:205-211
16. Collu G, Bink HHJ, Moreno PRH, van der Heijden R, Verpoorte R (1999) Determination of the activity of the cytochrome P450 enzyme geraniol 10-hydroxylase in plants by high-performance liquid chromatography. Phytochem Anal 10:314-318
17. Collu G, Unver N, Peltenburg-Looman AMG, 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
18. Collu G, Garcia AA, van der Heijden R, Verpoorte R (2002) Activity of the cytochrome P450 enzyme geraniol 10-hydroxylase and alkaloid production in plant cell cultures. Plant Sci 162:165-172
19. Contin A, van der Heijden R, ten Hoopen HJG, Verpoorte R (1998a) The inoculum size triggers tryptamine or secologanin biosynthesis in a Catharanthus roseus cell culture. Plant Sci 139:205-211
20. Contin A, van der Heijden R, Lefeber AWM, Verpoorte R (1998b) The iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture. FEBS Lett 434:413-416
21. Contin A, van der Heijden R, Verpoorte R (1999a) Effects of alkaloid precursor feeding and elicitation on the accumulation of secologanin in a Catharanthus roseus cell suspension culture. Plant Cell Tiss Org Cult 56:111-119
22. Contin A, Collu G, van der Heijden R, Verpoorte R (1999b) The effects of phenobarbital and ketonazole on the alkaloid biosynthesis in Catharanthus roseus cell suspension cultures. Plant Physiol Biochem 37:139-144
23. Contin A, van der Heijden R, Verpoorte R (1999c) Accumulation of loganin and secologanin in vacuoles from suspension cultured Catharanthus roseus cells. Plant Sci 147:177-183
24. Courdavault V, Burlat V, St-Pierre B, Giglioli-Guivarc'h N (2005) Characterisation of CaaX-prenyl transferases in Catharanthus roseus: relationships with the expression of genes involved in the early stages of monoterpenoid biosynthetic pathway. Plant Sci 168:1097-1107
25. Cunningham FX Jr, Lafond TP, Gantt E (2000) Evidence of a role for LytB in the non-mevalonate pathway of isoprenoid biosynthesis. J Bacteriol 182:5841-5848
26. 13C NMR study on the monoterpene loganin. Phytochemistry 51:223-226
27. Eisenreich W, Rodhich F, Bacher A (2001) Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci 6:78-84
28. Estevez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276:22901-22909
29. Facchini PJ, DiCosmo F (1991) Secondary metabolite biosynthesis in cultured cells of Catharanthus roseus (L) G Don immobilized by adhesion to glass fibres. Appl Microbiol Biotechnol 35:382-392
30. Galichet A, Fuerholz A, Laule O, Beemster G, Gruissem W (2004) Developmental coordination of MVA and MEP isoprene pathways requires protein prenylation. In: Conferences Jacques-Monod: Integrative Biology, dissecting cross talk between plant signalling pathway, 15-19 May 2004, Abstract 9
31. Gantet P, Imbault N, Thiersault M, Doireau P (1998) Necessity of a functional octodecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant Cell Physiol 39:220-225
32. Gantet P, Memelink J (2002) Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. Trends Pharmacol Sci 23:563-569
33. Guarnaccia R, Coscia CJ (1971) Occurrence and biosynthesis of secologanic acid in Vinca rosea. J Am Chem Soc 93:6320-6321
34. Guevara-García A, San Román C, Arroyo A, Cortés ME, de la Luz Gutiérrez-Nava M, León P (2005) Characterization of the Arabidopsis clb6 mutant illustrates the importance of post transcriptional regulation of the methyl-d-erythritol 4-phosphate pathway. Plant Cell 17:628-643
35. + oxidoreductase from catmint (Nepeta racemosa). Arch Biochem Biophys 318:105-112
36. Hallard D, van der Heijden R, Contin A, Tomas Jiménéz EM, Snoeijer W, Verpoorte R, Jensen SR, Lopez Cardoso MI, Pasquali G, Memelink J, Hoge JHC (1998) An assay for secologanin in plant tissues based on enzymatic conversion into strictosidine. Phytochem Anal 9:162-167
37. Hedhili S, Courdavault V, Giglioli-Guivarc'h N, Gantet P (2005) Regulation of the terpene moiety biosynthesis of Catharanthus roseus terpene indole alkaloids. Phytochem Rev this issue
38. Hong SB, Hughes EH, Shanks JV, San KY, Gibson SI (2003) Role of the nonmevalonate pathway in indole alkaloid production by Catharanthus roseus hairy roots. Biotechnol Prog 19:1105-1108
39. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY (2004a) Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab Eng 6:268-276
40. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY (2004b) Expression of a feedback-resistant anthranilate synthase in Catharanthus roseus hairy roots provides evidence for tight regulation of terpenoid indole levels. Biotechnol Bioeng 86:718-727
41. Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E (2004) The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol 136:3724-3736
42. + oxidoreductase of Rauwolfia serpentina cells: the key enzyme in biosynthesis of monoterpene alcohols. J Biochem 109:341-347
43. Imbault N, Thiersault M, Dupéron P, Benabdelmouna A, Doireau P (1996) Pravastatin: a tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspensions. Physiol Plant 98:803-809
44. Irmler S, Schröder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strack D, Matern U, Schröder J (2000) Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase. Plant J 24:797-804
45. Jacobs DI, Gaspari M, van der Greet J, van der Heijden R, Verpoorte R (2005) Proteome analysis of the medicinal plant Catharanthus roseus. Planta 221:690-704
46. Katano N, Yamamoto H, Ilio R, Inoue K (2001) 7-deoxyloganin 7-hydroxylase in Lonicera japonica cell cultures. Phytochemistry 58:53-58
47. Krepkiy D, Miziorko HM (2004) Identification of active site residues in mevalonate diphosphate decarboxylase: implications for a family of phosphotransferases. Protein Sci 13:1875-1881
48. Krueger RJ, Carew DP (1978) Catharanthus roseus tissue culture: the effects of precursors on growth and alkaloid production. Lloydia 41:327-331
49. Laule O, Fürholz A, Chang H-S, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange BM (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 100:6866-6871
50. Leivar P, Gonzalez VM, Castel S, Trelease RN, Lopez-Iglesias C, Arro M, Boronat A, Campos N, Ferrer A, Fernandez-Busquets X (2005) Subcellular localization of Arabidopsis 3-hydroxy-3-methylglutaryl-Coenzyme A reductase. Plant Physiol 137:57-69
51. Lois LM, Rodríguez-Concepción M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J 22:503-513
52. Lopez Cardoso MI, Meijer AH, Rueb S, Machado JA, Memelink J, Hoge JH (1997) A promoter region that controls basal and elicitor-inducible expression level of the NADPH:cytochrome P450 reductase gene (Cpr) from Catharanthus roseus binds nuclear factor GT-1. Mol Gen Genet 256:674-681
53. Madyastha KM, Guarnaccia R, Baxter C, Coscia CJ (1973) S-adenosyl-l-methionine: loganic acid methyltransferase. A carboxyl-alkylating enzyme from Vinca rosea. J Biol Chem 248:2497-2501
54. Madyastha KM, Coscia CJ (1979) Detergent-solubilized NADPH-cytochrome c (P450) reductase from the higher plant, Catharanthus roseus. J Biol Chem 254:2419-2427
55. McFarlane J, Madyastha KM, Coscia CJ (1975) Regulation of secondary metabolism in higher plants. Effect of alkaloids on a cytochrome P450 dependent monooxygenase. Biochem Biophys Res Commun 66:1263-1269
56. Mahroug S, Burlat V, St-Pierre B (2005) Cellular and sub-cellular organisation of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Phytochem Rev this issue
57. Maldonado-Mendoza IE, Burnett RJ, Nessler CL (1992) Nucleotide sequence of a cDNA encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol 100:1613-1614
58. Meehan TD, Coscia CJ (1973) Hydroxylation of geraniol and nerol by a monooxygenase from Vinca rosea. Biochem Biophys Res Commun 53:1043-1048
59. Meijer AH, Lopez Cardoso MI, Voskuilen JTH, de Waal A, Verpoorte R, Hoge JHC (1993a) Isolation and characterization of a cDNA clone from Catharanthus roseus encoding NADPH: cytochrome P450 reductase, an essential enzyme for reactions catalysed by cytochrome P450 monooxygenases in plants. Plant J 4:47-60
60. Meijer AH, de Waal A, Verpoorte R (1993b) Purification of the cytochrome P450 enzyme geraniol 10-hydroxylase from cell cultures of Catharanthus roseus. J Chromatogr 635:237-249
61. Mérillon JM, Doireau P, Guillot A, Chénieux JC, Rideau M (1986) Indole alkaloid accumulation and tryptophan decarboxylase activity in Catharanthus roseus cells cultured in three different media. Plant Cell Rep 5:23-26
62. Mérillon JM, Ouelhazi L, Doireau P, Chénieux JC, Rideau M (1989) Metabolic changes and alkaloid production in habituated and non-habituated cells of Catharanthus roseus grown in hormone-free medium. Comparing hormone-deprived non-habituated cells with habituated cells. J Plant Physiol 134:54-60
63. Mincheva Z, Courtois M, Crèche J, Rideau M, Viaud-Massuard MC (2004) One pot synthesis of functionalized 4,5-dihydroisoxazole derivatives via nitrile oxides, and biological evaluation with plant cells. Bioorg Med Chem 12:191-197
64. Moreno PRH, van der Heijden R, Verpoorte R (1993a) Effect of terpenoid precursor feeding and elicitation on formation of indole alkaloids in cell suspension cultures of Catharanthus roseus. Plant Cell Rep 12:702-705
65. Moreno PRH, Schlatmann JE, van der Heijden R, van Gulik WM, ten Hoopen HJ, Verpoorte R, Heijnen JJ (1993b) Induction of ajmalicine formation and related enzyme activities in Catharanthus roseus cells: effect of inoculum density. Appl Microbiol Biotech 39:42-47
66. Moreno PRH, Poulsen C, van der Heijden R, Verpoorte R (1996) Effects of elicitation on different metabolic pathways in Catharanthus roseus (L.) G. Don cell suspension cultures. Enzyme Microb Technol 18:99-107
67. Morgan JA, Shanks JV (2000) Determination of metabolic rate-limitations by precursor feeding in Catharanthus roseus hairy root cultures. J Biotechnol 79:137-145
68. Nagata N, Suzuki M, Yoshida S, Muranaka T (2002) Mevalonic acid partially restores chloroplast and etioplast development in Arabidopsis lacking the non-mevalonate pathway. Planta 216:345-350
69. Nakamura A, Shimada H, Masuda T, Ohta H, Takamiya KI (2001) Two distinct isopentenyl diphosphate isomerases in cytosol and plastid are differentially induced by environmental stresses in tobacco. FEBS Lett 506:61-64
70. Page JE, Hause G, Raschke M, Gao W, Schmidt J, Zenk MH, Kutchan TM (2004) Functional analysis of the final steps of the 1-deoxy-d-xylulose (DXP) pathway to isoprenoids in plants using virus-induced gene silencing. Plant Physiol 134:1401-1413
71. Papon N, Bremer J, Vansiri A, Andreu F, Rideau M, Crèche J (2005) Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells. Planta Med 71:572-574
72. Proteau PJ (2004) 1-deoxy-d-xylulose 5-phosphate reductoisomerase: an overview. Bioorg Chem 32:483-493
73. Querol J, Campos N, Imperial S, Boronat A, Rodríguez- Concepción M (2002) Functional analysis of the Arabidopsis thaliana GCPE protein involved in plastid isoprenoid biosynthesis. FEBS Lett 514:343-346
74. Ramos-Valdivia AC (1996) Characterization of isopentenyl diphosphate isomerase. A regulatory enzyme in Cinchona isoprenoid biosynthesis, PhD Thesis, Leiden University, The Netherlands, 145 pp
75. Ramos-Valdivia AC, van der Heijden R, Verpoorte R (1998) Isopentenyl diphophate isomerase and prenyltransferase activities in rubiaceous and apocynaceous cultures. Phytochemistry 48:961-969
76. Richard SB, Ferrer JL, Bowman ME, Lillo AM, Tetzlaff CN, Cane DE, Noel JP (2002) Structure and mechanism of 2-C-methyl-d-erythritol 2,4-cyclodiphosphate synthase. An enzyme in the mevalonate-independent isoprenoid biosynthetic pathway. J Biol Chem 277:8667-8672
77. Riou C, Tourte Y, Lacroute F, Karst F (1994) Isolation and characterization of a cDNA encoding Arabidopsis thaliana mevalonate kinase by genetic complementation in yeast. Gene 148:293-297
78. Rodríguez-Concepción M, Ahumada I, Diez-Juez E, Sauret-Gueto S, Lois LM, Gallego F, Carratero-Paulet L, Campos N, Boronat A (2001) 1-deoxy-xylulose 5-phosphate reductoisomerase and plastid isoprenoid biosynthesis during tomato fruit ripening. Plant J 27:213-222
79. Rodríguez-Concepción M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130:1079-1089
80. Rodríguez-Concepción M, Querol J, Lois LM, Imperial S, Boronat A (2003) Bioinformatic and molecular analysis of hydroxymethylbutenyl diphosphate synthase (GCPE) gene expression during carotenoid accumulation in ripening tomato fruit. Planta 217:476-482
81. Rodríguez-Concepción M, Forés O, Martinez-Garcia JF, Gonzalez V, Phillips MA, Ferrer A, Boronat A (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis development. Plant Cell 16:144-156
82. Rohmer M (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat Prod Rep 16:565-574
83. Sanchez-Iturbe P, Galaz-Avalos RM, Loyola-Vargas VM (2005) Determination and partial purification of a monoterpene cyclase from Catharanthus roseus hairy roots. Phyton 55-69
84. Schiel O, Witte L, Berlin J (1987) Geraniol-10-hydroxylase activity and its relation to monoterpene indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus. Z Naturforsch 42:1075-1081
85. Schuhr CA, Radykewicz T, Sagner S, Latzel C, Zenk MH, Arigoni D, Bacher A, Rohdich F, Eisenreich W (2003) Quantitative assessment of cross talk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy. Phytochem Rev 2:3-16
86. Schulte AE, van der Heijden R, Verpoorte R (1999) Purification and characterization of phosphomevalonate kinase from Catharanthus roseus. Phytochemistry 52:975-983
87. Schulte AE, van der Heijden R, Verpoorte R (2000a) Purification and characterization of mevalonate kinase from suspension-cultured cells of Catharanthus roseus (L.) G. Don. Arch Biochem Biophys 378:287-298
88. Schulte AE, Llamas Duran EM, van der Heijden R, Verpoorte R (2000b) Mevalonate kinase activity in Catharanthus roseus plants and suspension cultured cells. Plant Sci 150:59-69
89. Scott AI, Mizukami H, Lee SL (1979) Characterization of a 5-methyltryptophan resistant strain of Catharanthus roseus cultured cells. Phytochemistry 18:795-798
90. Seemann M, Wegner P, Schünemann V, Tse Sum Bui B, Wolff M, Marquet A, Trautwein AX, Rohmer M (2005) Isoprenoid biosynthesis in chloroplasts via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (GcpE) from Arabidopsis thaliana is a [4Fe-4S] protein. J Biol Inorg Chem 10:131-137
91. Soler E, Clastre M, Bantignies B, Marigo G, Ambid C (1993) Uptake of isopentenyl diphosphate by plastids isolated from Vitis vinifera L. cell suspensions. Planta 191:324-329
92. Tholl D, Kish CM, Orlova I, Sherman D, Gershenzon J, Pichersky E, Dudareva N (2004) Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16:977-992
93. Uesato S, Matsuda S, Inouye H (1984) Mechanism for iridane skeleton formation from acyclic monoterpenes in the biosynthesis of secologanin and vindoline in Catharanthus roseus and Lonicera morrowii. Chem Pharm Bull 23:1671-1674
94. Uesato S, Ogawa Y, Inouye H, Saiki K, Zenk MH (1986a) Synthesis of iridodial by cell free extracts from Rauwolfia serpentina. Tetrahedron Lett 27:2893-2896
95. Uesato S, Miyauchi M, Itoh H, Inouye H (1986b) Biosynthesis of iridoid glucosides in Galium mollugo, G. spurium, var echinospermum and Deutzia crenata. Intermediacy of deoxyloganic acid, loganin and iridodial glucoside. Phytochemistry 25:2515-2521
96. Uesato S, Ikeda H, Fujita T, Inouye H, Zenk MH (1987) Elucidation of iridodial formation mechanism. Partial purification and characterisation of the novel monoterpene cyclase from Rauwolfia serpentina cell suspension cultures. Tetrahedron Lett 28:4431-4434
97. Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295-297
98. Van der Heijden R, Verpoorte R (1995) Metabolic enzymes of 3-hydroxy-3-methylglutaryl-coenzyme A in Catharanthus roseus. Plant Cell Tiss Org Cult 43:85-88
99. Van der Heijden R, Verpoorte R, Duine JA (1994) Biosynthesis of 3S-hydroxy-3-methylglutaryl-coenzyme A in Catharanthus roseus: acetoacetyl-CoA thiolase and HMG-CoA synthase show similar chromatographic behaviour. Plant Physiol Biochem 32:807-812
100. Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R (2004) The Catharanthus roseus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11:607-628
101. Veau B, Courtois M, Oudin A, Chénieux JC, Rideau M, Clastre M (2000) Cloning and expression of cDNA encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochim Biophys Acta 1517:159-163
102. Vetter H-P, Mangold U, Schroeder G, Marner F-J, Werck-Reichhart D, Schroerder J (1992) Molecular analysis and heterologous expression of an inducible cytochrome P-450 protein from periwinkle (Catharanthus roseus L.). Plant Physiol 100:998-1007
103. Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243-254
104. Whitmer S, van der Heijden R, Verpoorte R (2002a) Effect of precursor feeding on alkaloid accumulation by a tryptophan decarboxylase over-expressing transgenic cell line T22 of Catharanthus roseus. J Biotechnol 96:193-203
105. Whitmer S, van der Heijden R, Verpoorte R (2002b) Effect of precursor feeding on alkaloid accumulation by a strictosidine synthase over-expressing transgenic cell line S1 of Catharanthus roseus. Plant Cell Tiss Org Cult 69:85-93
106. Wolfertz M, Sharkey TD, Boland W, Kühnemann F (2004) Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis. Plant Physiol 135:1939-1945
107. Wolff M, Seemann M, Tse Sum Bui B, Frapart Y, Tritsch D, Estrabot AG, Rodríguez-Concepción M, Boronat A, Marquet A, Rohmer M (2003) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe-4S] protein. FEBS Lett 541:115-120
108. Yang T, Li J, Wang HX, Zeng Y (2005) A geraniol-synthase gene from Cinnamomum tenuipilum. Phytochemistry 66:285-293
109. Zhao J, Hu Q, Guo Y-Q, Zhu W-H (2001) Effects of stress factors, bioregulators, and synthetic precursors on indole alkaloid production in compact callus clusters cultures of Catharanthus roseus. Appl Microbiol Biotechnol 55:693-698
110. Zenk MH, El-Saghi H, Arens H, Stockkigt J, Weiler EW, Deus B (1977) Formation of the indole alkaloids serpentine and ajmalicine in cell suspension cultures of Catharanthus roseus. In: Barz W, Reinhard E, Zenk MH (eds) Plant tissue culture and its biotechnological application. Springer Verlag, Berlin, New York, pp 27-43