Catharanthus terpenoid indole alkaloids: Biosynthesis and regulation

Phytochemistry Reviews

Volumn 6, Issue 2-3, 2007, Pages 277-305

  El Sayed, Magdi ^a,b   Verpoorte, Rob ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b ASWAN UNIVERSITY   (Egypt)

Author keywords

Biosynthesis; Catharanthus; Indole alkaloids; Indole pathway; MEP pathway; Regulation; Terpenoids

Indexed keywords

2 C METHYL DEXTRO ERYTHRITOL 4 PHOSPHATE; 4,21 DEHYDROEISSOSCHIZINE; AJMALICINE; AKUAMMIDINE; ALSTONINE; ANHYDROVINBLASTINE; CATHARANTHINE; CATHARANTHUS ROSEUS EXTRACT; CATHENAMINE; ENZYME; EPICATHENAMINE; ERYTHRITOL; IMINIUM; INDOLE ALKALOID; MEVALONIC ACID; PERIVINE; SECODINE; SECOLOGANIN; SERPENTINE; STEMMADENINE; STRICTOSIDINE; TABERSONINE; TERPENE DERIVATIVE; TETRAHYDROALSTONINE; TRYPTAMINE; UNCLASSIFIED DRUG; VINBLASTINE; VINCRISTINE; VINDOLINE; VINDOLININE; VINLEUROSINE;

AMINO ACID SYNTHESIS; BIOSYNTHESIS; CATALYSIS; CATHARANTHUS ROSEUS; DIMERIZATION; ENZYME REGULATION; FUNGUS; GENE OVEREXPRESSION; GROWTH REGULATION; METABOLIC ENGINEERING; MOLECULAR CLONING; NONHUMAN; PLANT CELL CULTURE; PLANT GENETICS; PLANT GROWTH; PLANT METABOLISM; PRECURSOR; PRIORITY JOURNAL; PRODUCTIVITY; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW;

CATHARANTHUS; CATHARANTHUS ROSEUS;

EID: 34249875679     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-006-9047-8     Document Type: Review

References (195)

1. Aerts RJ, Gisi D, De Carolis E, De Luca V, Baumann TW (1994) Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus roseus and Cinchona seedlings. Plant J 5:635-643
2. Aerts RJ, Schafer A, Hesse M, Baumann TW, Slusarenko A (1996) Signalling molecules and the synthesis of alkaloids in Catharanthus roseus seedlings. Phytochemistry 42:417-422
3. Albrecht M, Sandmann G (1994) Light-stimulated carotenoid biosynthesis during transformation of maize etioplast is regulated by increased activity of isopentenyl pyrophosphate isomerase. Plant Physiol 105:529-534
4. 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
5. 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
6. Ayora-Talavera T, Chappell J, Lozoya-Gloria E, Loyola-Vargas VM (2002) Overexpression in Catharanthus roseus hairy roots of a truncated hamster 3-hydroxy-3-methylglutaryl-CoA reductase gene. Appl Biochem Biotechnol 97:135-145
7. Bach TJ (1995) Some new aspects of isoprenoid biosynthesis in plants-a review. Lipids 30:191-202
8. Bach TJ, Raudot V, Vollack KU, Weber T, Zeiler S (1994) Further studies on the enzymatic conversion of acetyl-coenzyme A into 3-hydroxy-3- methylglutaryl-coenzyme A in radish. Plant Physiol Biochem 32:775-783
9. Balsevich J, De Luca V, Kurz WGW (1986) Altered alkaloid pattern in dark grown seedlings of Catharanthus roseus. The isolation and characterization of 4-desacetoxyvindoline: a novel indole alkaloid and proposed precursor of vindoline. Heterocycles 24:2415-2421
10. Battersby AR, Hall ES (1969) The intermediacy of geissoschizine in indole alkaloid biosynthesis: rearrangement to the Strychnos skeleton. Chem Commun 14:793-794
11. Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascade. Plant Cell 12:1103-1115
12. Bongaerts RJM (1998) The chorismate branching point in Catharanthus roseus: aspects of anthranilate synthase regulation in relation to indole alkaloid biosynthesis. PhD thesis, Leiden University, The Netherlands
13. Brown RT, Hill JS, Smith GF, Stapleford HSJ (1971) On the rearrangement of catharanthine, stemmadenine and tabersonine in acetic acid. Tetrahedron 27:5217-5228
14. Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (2004) Co-expression of the 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
15. Canel C, Lopez-Cradoso MI, Whitmer S, van der Fits L, Pasquali G, van der Heijden R, Hoge JHC, Verpoorte R (1998) Effects of overexpression of strictosidine synthase and tryptophan decarboxylase on alkaloid production by cell cultures of Catharanthus roseus. Planta 205:414-419
16. Chahed K, Oudin A, Guivarc'h N, Hamdi S, Chenieux JC, Rideau M, Clastre M (2000) 1-Deoxy-d-xylulose-5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant Physiol Biochem 38:559-566
17. 2+ fluxes during elicitation of the oxidative burst in aequonin-transformed tobacco cells. J Biol Chem 272:28274-28280
18. Chappell J (1995) The biochemistry and molecular biology of isoprenoid metabolism. Plant Physiol 107:1-6
19. Collu G (1999) Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in the biosynthesis of terpenoid indole alkaloids in higher plants: an enzymological and molecular study. PhD thesis, Leiden University
20. 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
21. 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
22. Contin A (1999) The biosynthesis of secologanin in Catharanthus roseus cell suspension cultures. PhD thesis, Leiden University, The Netherlands
23. Contin A, van der Heijden R, Lefeber A, 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
24. Contin A, Collu G, van der Heijden R, Verpoorte R (1999) The effects of phenobarbital and ketoconazole on the alkaloid biosynthesis in Catharanthus roseus cell suspension cultures. Plant Physiol Biochem 37:139-144
25. Davies WJ, Jones HG (1991) Abscisic acid physiology and biochemistry. Bioscientific Publishers, Oxford, UK
26. De Carolis E, De Luca V (1993) Purification, characterization and kinetic analysis of a 2-oxoglutarate-dependent dioxygenase involved in vindoline biosynthesis from Catharanthus roseus. J Biol Chem 268:5504-5511
27. De Carolis E, Chan F, Balsevich J, De Luca V (1990) Isolation and characterization of a 2-oxoglutarate dependent dioxygenase involved in the second-to-last step in vindoline biosynthesis. Plant Physiol 94:1323-1329
28. Decendit A, Liu D, Ouelhazi L, Doireau P, Mèrillon JM, Rideau M (1992) Cytokinin-enhanced accumulation of indole alkaloids in Catharanthus roseus cell cultures-the factors affecting the cytokinin response. Plant Cell Rep 11:400-403
29. Decendit A, Petit G, Andreu F, Doireau P, Mèrillon JM, Rideau M (1993) Putative sites of cytokinin action during their enhancing effect on indole alkaloid accumulation in periwinkle cell suspensions. Plant Cell Rep 12:710-712
30. De Luca V (1993) Enzymology of indole alkaloid biosynthesis. In: Lea PJ (ed) Methods in plant biochemistry, enzymes of secondary metabolism. Academic, London, pp 345-368
31. De Luca V, Cutler AJ (1987) Subcellular localization of enzymes involved in indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 85:1099-1102
32. De Luca V, Balsevich J, Tyler RT, Eilert U, Panchuk BD, Kurz WGW (1986) Biosynthesis of indole alkaloids: development regulation of the biosynthetic pathway from tabersonine to vindoline in Catharanthus roseus. J Plant Physiol 125:147-156
33. De Luca V, Balsevich J, Tyler RT, Kurz WGW (1987) Characterization of a novel N-methyltransferase (NMT) from Catharanthus roseus. Plant Cell Rep 6:458-461
34. De Luca V, Marineau C, Brisson N (1989) Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal DOPA decarboxylase. Proc Natl Acad Sci USA 86:2582-2586
35. Dethier M, De Luca V (1993) Partial purification of a N-methyltransferase involved in vindoline in Catharanthus roseus. Phytochemistry 32:673-678
36. Deus-Neumann B, Zenk MH (1984) Instability of indole alkaloid production in Catharanthus roseus cell suspension cultures. Planta Med 50:427-431
37. De Waal A, Meijer AH, Verpoorte R (1995) Strictosidine synthase from Catharanthus roseus: purification and characterization of multiple forms. Biochem J 306(2):571-580
38. Diez E, Montamat F, Delrot S, Boronat A (1997) Expression of Arabidopsis thaliana 3-hydroxy-3-methylglutaryl-coenzyme A synthase in Escherichia coli. In: Abstract book, 3rd Terpnet meeting, Université de Poitier, France, 29-30 May
39. Dubey VS, Bhalla R, Luthra R (2003) An overview of non-mevalonate pathway for terpenoid biosynthesis in plants. J Biosci 28:101-110
40. Duvold T, Bravo JM, Pale-Grosdemange C, Rohmer M (1997a) Biosynthesis of 2-C-methyl-d-erythritol, a putative C-5 intermediate in the mevalonate independent pathway for isoprenoid biosynthesis. Tetrahedron Lett 38:4769-4772
41. Duvold T, Cali P, Bravo JM, Rohmer M (1997b) Incorporation of 2-C-methyl-d-erythritol, a putative isoprenoid precursor in the mevalonate-independent pathway, into ubiquinone and menaquinone of Escherichia coli. Tetrahedron Lett 38:6181-6184
42. Eilert U, Kurz WG, Constabel F (1987) In: Green CE (ed) Plant cell and tissue culture. A. R. Liss, New York, p 213
43. Eisenreich W, Menhard B, Hylands PJ, Zenk MH, Bacher A (1996) Studies on the biosynthesis of taxol: the taxane carbon skeleton is not mevalonoid origin. Proc Natl Acad Sci USA 93:6431-6436
44. Eisenreich W, Sagner S, Zenk MH, Bacher A (1997) Monoterpenoid essential oils are not of mevalonoid origin. Tetrahedron Lett 38:3889-3892
45. El-Sayed M, Verpoorte R (2002) Effect of phytohormones on growth and alkaloid accumulation by a Catharanthus roseus cell suspension cultures fed with alkaloid precursors tryptamine and loganin. Plant Cell Tissue Organ Cult 68:265-270
46. El-Sayed M, Choi YH, Frédérich M, Roytrakul S, Verpoorte R (2004) Alkaloid accumulation in Catharanthus roseus cell suspension cultures fed with stemmadenine. Biotechnol Lett 26:793-798
47. Enjuto M, Balcells L, Campos N, Caelles C, Arró M, Boronat A (1994) Arabidopsis thaliana contains two differentially expressed 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes, which encode microsomal forms of the enzyme. Proc Natl Acad Sci USA 91:927-931
48. Facchini PJ, DiCosmo F (1991) Secondary metabolites biosynthesis in cultured cells of Catharanthus roseus (L.) Don immobilized by adhesion to glass fibers. Appl Microbiol Biotechnol 35:382-392
49. Fernandez JA, Owen TG, Kurz WG, De Luca V (1989) Immunological detection and quantitation of tryptophan decarboxylase in developing Catharanthus roseus seedlings. Plant Physiol 91:79-84
50. Garnier F, Carpin S, Label P, Crèche J, Rideau M, Hamdi S (1996) Effect of cytokinin on alkaloid accumulation in periwinkle callus cultures transformed with a light-inducible ipt gene. Plant Sci 120:47-55
51. Gary JC (1987) Control of isoprenoid biosynthesis in higher plants. Adv Bot Res 14:25-90
52. Geerlings A, 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
53. Goddijn OJM (1992) Regulation of terpenoid indole alkaloid biosynthesis in Catharanthus roseus. PhD thesis, Leiden University, The Netherlands
54. Goddijn OJM, De Kam RJ, Zanetti A, Schilperoort RA, Hoge JHC (1992) Auxin rapidly down-regulates transcription of the tryptophan decarboxylase gene from Catharanthus roseus. Plant Mol Biol 18:113-120
55. Goddijn OJM, Pennings EJM, van der Helm P, Verpoorte R, Hoge JHC (1995) Overexpression of a tryptophan decarboxylase cDNA in Catharanthus roseus crown gall calluses results in increased tryptamine levels but not in increased terpenoid indole alkaloid production. Transgenic Res 4:315-323
56. Goodbody AE, Endo T, Vukovic J, Kutney JP, Choi LSL, Misawa M (1988) Enzymatic coupling of catharanthine and vindoline to form 3′,4′- anhydrovinblastine by horseradish peroxidase. Planta Med 54:136-140
57. Green TR, Dennis DT, West CA (1975) Compartmentation of isopentenyl pyrophosphate isomerase and pyrenyltransferase in developing castor bean endosperm. Biochem Biophys Res Commun 64:976-982
58. Grolle S, Bringer-Meyer S, Sahm H (2000) Isolation of the dxr gene of Zymomonas mobilis and characterization of the 1-deoxy-d-xylulose-5-phosphate reductoisomerase. FEMS Microbiol Lett 191:131-137
59. Guarnaccia R, Botta L, Coscia CJ (1974) Biosynthesis of acidic iridoid monoterpene glucosides in Vinca rosea. J Am Chem Soc 96:7079-7084
60. Hallard D (2000) Transgenic plant cells for the production of indole alkaloids. PhD thesis, University of Leiden, The Netherlands
61. Hallard D, van der Heijden R, Verpoorte R, Lopes Cardoso M, Pasquali G, Memelink J, Hoge JHC (1997) Suspension cultured transgenic cells of Nicotiana tabacum expressing tryptophan decarboxylase and strictosidine synthase cDNA from Catharanthus roseus produce strictosidine upon secologanin feeding. Plant Cell Rep 17:50-54
62. Hampton RY, Rine J (1994) Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum in yeast. J Cell Biol 125:299-312
63. Hemscheidt T, Zenk MH (1980) Glucosidases involved in indole alkaloid biosynthesis of Catharanthus roseus cell cultures. FEBS Lett 110:187-191
64. Hemscheidt T, Zenk MH (1985) Partial purification and characterization of a NADPH dependent tetrahydroalstonine synthase from Catharanthus roseus cell suspension cultures. Plant Cell Rep 4:216-219
65. Hilliou F, Costa M, Almeida I, Lopes Cardoso I, Leech M, Ros Barcelo A, Sottomayor M (2002) Cloning of a peroxidase enzyme involved in the biosynthesis of pharmaceutically active terpenoid indole alkaloids in Catharanthus roseus (L.) G. Don. In: Acosta M, Rodriguez-Lopez JN, Pedreno MA (eds) Proceedings of the VI international plant peroxidase symposium, University of Murcia and University of A Coruna, pp 152-158
66. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY (2004a) Expression of a feedback-resistant anthranilate synthase in Catharanthus roseus hairy roots provides evidence for tight regulation of terpenoid indole alkaloid levels. Biotechnol Bioeng 86:718-727
67. Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY (2004b) Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab Eng 6:268-276
68. Irmler S, Schröder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strak 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
69. Jacobs D (2003) Proteome analysis of the medicinal plant Catharanthus roseus. PhD thesis, University of Leiden, The Netherlands
70. Jacobs DI, Gaspari M, van der Greef J, van der Heijden R, Verpoorte R (2005) Proteome analysis of Catharanthus roseus cultured cells for the identification of proteins involved in alkaloid biosynthesis and finding of novel sequences. Planta 221:690-704
71. Jossang A, Fodor P, Bodo B (1998) A new structural class of bisindole alkaloids from the seeds of Catharanthus roseus: vingramine and methylvingramine. J Org Chem 63:7162-7167
72. Katayama S, Adachi N, Takao K, Nagakawa T, Matsuda H, Kawamukai M (1995) Molecular cloning and sequencing of the hcs gene which encodes 3-hydroxy-3-methylglutaryl-coenzyme A synthase of Schizosaccharomyces pombe. Yeast 11:1533-1537
73. Knobloch KH, Berlin J (1983) Influence of phosphate on formation of indole alkaloids and phenolic compounds in cell suspension cultures of Catharanthus roseus. I. Comparison of enzyme activities and product accumulation. Plant Cell Tissue Organ Cult 2:233-240
74. Knobloch KH, Hansen B, Berlin J (1981) Medium induced formation of indole alkaloids and concomitant changes of interrelated enzyme activities in cell suspension cultures of Catharanthus roseus. Z Naturforsch 36c:40-43
75. Korth KL, Stermer BA, Bhattacharyya MK, Dixon RA (1997) HMG-CoA reductase gene families that differentially accumulate transcripts in potato tubers are developmentally expressed in floral tissues. Plant Mol Biol 33:545-551
76. Kutchan TM (1993) Strictosidine: from alkaloid to enzyme to gene. Phytochemistry 32:493-506
77. Kutney PJ, Hibino T, Jahngen E, Okutani T, Ratcliffe AH, Treasurywala AM, Wunderly SL (1976) Total synthesis of indole and dihydroindole alkaloids. IX. Studies on the synthesis of bisindole alkaloids in the vinblastine-vincristine series. The biogenetic approach. Helv Chim Acta 59:2858-2882
78. Lange BM, Croteau R (1999) Isopentenyl diphosphate biosynthesis via a mevalonate-independent pathway: isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. Proc Natl Acad Sci USA 96:13714-13719
79. Lange BM, Wildung MR, McCaskill D, Croteau R (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci USA 95:2100-2014
80. Langlois N, Gueritte F, Langlois Y, Potier P (1976) Application of a modification of the Polonovski reaction to the synthesis of vinblastine-type alkaloids. J Am Chem Soc 98:7017-7024
81. Leivar P, González VM, Castel S, Trelease RN, López- Iglesias C, Arró M, Boronat A, Campos N, Ferrer A, Fernàndez- Busquets X (2005) Subcellular localization of Arabidopsis 3-hydroxy-3- methylglutaryl-coenzyme A reductase. Plant Physiol 137:57-69
82. Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47-65
83. Lois LM, Campos N, Putra SR, Danielsen K, Rohmer M, Boronat A (1998) Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of 1-deoxyxylulose-5- phosphate, a common precursor of isoprenoid, thiamin, and pyridoxol biosynthesis. Proc Natl Acad Sci USA 95:2105-2110
84. Lopes Cardoso MI (1995) Analysis and modification of the expression of genes involved in plant secondary metabolism: genes encoding early steps in terpenoid indole biosynthesis in Catharanthus roseus. PhD thesis, Catholic University, Portugal
85. Lopes Cardoso MI, Meijer AH, Rueb S, Queiroz Machado J, Memelink J, Hoge JHC (1997) A promoter region that controls basal and elicitor-inducible expression levels of the NADPH: cytochrome P450 reductase gene (Cpr) from Catharanthus roseus binds nuclear factor GT-1. Mol Gen Genet 256:674-681
86. Loyola-Vargas V, Mendez-Zeel M, Monforte-Gonzalez M, Miranda-Ham ML (1992) Serpentine accumulation during greening in normal and tumor tissues of Catharanthus roseus. J Plant Physiol 140:213-217
87. Luijendijk T (1995) Strictosidine glucosidase in indole alkaloid producing plants; characteristics and physiological implications. PhD thesis, Leiden University, The Netherlands
88. Luijendijk T, Stevens LH, Verpoorte R (1998) Purification and characterization of strictosidine β-d-glucosidase from Catharanthus roseus cell suspension cultures. Plant Physiol Biochem 36:419-425
89. Madyastha KM, Coscia CJ (1979) Enzymology of indole alkaloid biosynthesis. Recent Adv Phytochem 13:85-129
90. Madyastha KM, Guarnaccia R, Baxter C, Coscia CJ (1973) Monoterpene biosynthesis VII: S-adenosyl-l-methionine: loganic acid methyltransferase, a carboxyl-alkylating enzyme from Vinca rosea. J Biol Chem 248:2497-2501
91. Madyastha KM, Meehan TD, Coscia CJ (1976) Characterization of a cytochrome P-450 dependent monoterpene hydroxylase from the higher plant Vinca rosea. Biochemistry 15:1097-1102
92. Madyastha KM, Ridgway JE, Dwyer JG, Coscia CJ (1977) Subcellular localization of a cytochrome P-450 monooxygenase in vesicles of the higher plant Catharanthus roseus. J Cell Biol 72:302-313
93. Maldonada-Mendosa IE, Burnett RJ, Nessler CL (1992) Nucleotide sequence of a cDNA encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase from Catharanthus roseus. Plant Physiol 100:1613-1614
94. Maldonada-Mendosa IE, Burnett RJ, Lopez-Meyer M, Nessler CL (1994) Regulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase by wounding and methyljasmonate. Plant Cell Tissue Organ Cult 38:351-356
95. Mangold U, Eichel J, Batschauer A, Lanz T, Kaiser T, Spangenberg G, Werck-Reichhart D, Schröder J (1994) Gene and cDNA for plant cytochrome p450 proteins (CYP72 family) from Catharanthus roseus, and transgenic expression of the gene and a cDNA in tobacco and Arabidopsis thaliana. Plant Sci 96:129-136
96. 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
97. McKaskill D, Croteau R (1995) Monoterpene and sesquiterpene biosynthesis in glandular trichomes of peppermint (Mentha × piperita) rely exclusively on plastid-derived iospentenyl diphosphate. Planta 197:49-56
98. McKnight TD, Roessner CA, Devagupta R, Scott AI, Nessler CL (1990) Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus. Nucleic Acids Res 18:4939
99. McKnight TD, Bergey DR, Burnett RJ, Nessler CL (1991) Expression of enzymatically active and correctly targeted strictosidine synthase in transgenic tobacco plants. Planta 185:148-152
100. Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467-472
101. Meijer AH, de Waal A, Verpoorte R (1993a) Purification of the cytochrome P-450 enzyme geraniol 10-hydroxylase from cell cultures of Catharanthus roseus. J Chromatogr 635:237-249
102. Meijer AH, Lopes Cardoso MI, Voskuilen JT, de Waal A, Verpoorte R, Hoge JHC (1993b) Isolation and characterization of a cDNA clone from Catharanthus roseus encoding NADPH: cytochrome P450 reductase, an enzyme essential for reactions catalyzed by cytochrome P450 mono-oxygenases in plants. Plant J 4:47-60
103. Memelink J, Verpoorte R, Kijne JW (2001) ORCAnisation of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212-219
104. Menke FLH, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455-4463
105. Merillon JM, Doireau P, Guillot A, Chenieux JC, Rideau M (1986) Indole alkaloid accumulation and tryptophan decarboxylase activity in Catharanthus roseus cells cultures in three different media. Plant Cell Rep 5:23-26
106. Mizukami H, Nördlov H, Lee SI, Scott AI (1979) Purification and characterization of strictosidine synthase (an enzyme condensing tryptamine and secologanin) from Catharanthus roseus cultured cells. Biochemistry 18:3760-3763
107. Mizutani M, Ward E, Ohta D (1998) Cytochrome P450 superfamily in Arabidopsis thaliana: isolation of cDNAs, differential expression and RFLP mapping of multiple cytochrome P450. Plant Mol Biol 37:39-52
108. Montamat F, Guilloton M, Karst F, Delrot S (1995) Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3- methylglutaryl-coenzyme A synthase. Gene 167:197-201
109. Moreno PRH, van der Heijden R, Verpoorte R (1993) 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
110. Moreno PRH, van der Heijden R, Verpoorte R (1995) Cell and tissue cultures of Catharanthus roseus: a literature survey. II. Updating from 1988 to 1993. Plant Cell Tissue Organ Cult 42:1-25
111. Moreno PRH, Poulsen C, van der Heijden R, Verpoorte R (1996) Effects of elicitation on different secondary metabolic pathways in Catharanthus roseus cell suspension cultures. Enzyme Microb Technol 18:99-107
112. Morgan JA, Shanks JV (1999) Inhibitor studies of tabersonine metabolism in C. roseus hairy roots. Phytochemistry 51:61-68
113. Morgan JA, Shanks JV (2000) Determination of metabolic rate-limitations by precursor feeding in Catharanthus roseus hairy root cultures. J Biotechnol 79:137-145
114. Murata J, 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
115. Nebert DW (1979) Multiple forms of inducible drug-metabolizing enzymes: a reasonable mechanism by which any organism can cope with adversity. Mol Cell Biochem 27:27
116. Newman JD, Chappell J (1999) Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. Crit Rev Biochem Mol Biol 34:95-106
117. Noe W, Berlin J (1984) Tryptophan decarboxylase from Catharanthus roseus cell suspension cultures: purification, molecular and kinetic data of the homogenous protein. Plant Mol Biol 3:281-288
118. Ouwerkerk PBF, Memelink J (1999) Elicitor-responsive promoter regions in the tryptophan decarboxylase gene from Catharanthus roseus. Plant Mol Biol 39:129-136
119. Pasquali G (1994) Regulation of the terpenoid indole alkaloid biosynthetic gene strictosidine synthase from Catharanthus roseus. PhD thesis, Leiden University
120. Pasquali G, Goddijn OJM, De Waal A, Verpoorte R, Schilperoort RA, Hoge JHC, Memelink J (1992) Coordinated regulation of two indole alkaloid biosynthesis genes from Catharanthus roseus by auxin and elicitors. Plant Mol Biol 18:1121-1131
121. Pennings EJ, Groen B, Duine JA, Verpoorte R (1989a) Tryptophan decarboxylase from Catharanthus roseus is a pyridoxo-quinoprotein. FEBS Lett 255:97-100
122. Pennings EJ, Verpoorte R, Goddijn OJM, Hoge JHC (1989b) Purification of tryptophan decarboxylase from cell cultures of Catharanthus roseus. J Chromatogr 483:311-318
123. Pennings EJ, van den Bosch RA, van der Heiden R, Stevens LH, Duine JA, Verpoorte R (1989c) Assay of strictosidine synthase from plant cell cultures by high-performance liquid chromatography. Anal Biochem 176:412-415
124. Piñas A, Ahumada J, Gonzalez V, Vollack KU, Bach TJ, Boronat A (1997) Cloning and characterization of cDNA clones encoding acetoacetyl-CoA thiolase from Arabidopsis thaliana. In: Abstract book, 3rd Terpnet meeting, Université de Poitier, France, May 29-30
125. Poulsen C, Verpoorte R (1991) Roles of chorismate mutase, isochorismate synthase and anthranilate synthase in plants. Phytochemistry 30:377-386
126. Poulsen C, Bongaerts R, Verpoorte R (1993) Purification and characterization of anthranilate synthase from Catharanthus roseus. Eur J Biochem 212:431-440
127. Power R, Kurz WGW, De Luca V (1990) Purification and characterization of acetylcoenzyme A: deacetylvindoline 4-O-acetyltransferase from Catharanthus roseus. Arch Biochem Biophys 279:370-376
128. Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91-102
129. Ramos-Valdivia AC, van der Heijden R, Verpoorte R (1997) Isopentenyl diphosphate isomerase: a core enzyme in isoprenoid biosynthesis. A review of its biochemistry and function. Nat Prod Rep 14:591-603
130. Ramos-Valdivia AC, van der Heijden R, Verpoorte R (1998) Isopentenyl diphosphate isomerase and prenyltransferase activities in rubiaceous and apocynaceous cultures. Phytochemistry 48:961-969
131. Reymond P, Farmer E (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404-411
132. Rijhwani SK, Shanks JV (1998) Effect of elicitor dosage and exposure time on biosynthesis of indole alkaloids by Catharanthus roseus hairy root cultures. Biotechnol Prog 14:442-449
133. Rodriguez-Concepcion 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
134. Rohdich F, Wungsintaweekul J, Luttgen H, Fischer M, Eisenreich W, Schuhr CA, Fellermeier M, Schramek N, Zenk M, Bacher A (2000) Biosynthesis of terpenoids: 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase from tomato. Proc Natl Acad Sci USA 97:8251-8256
135. Rohdich F, Kis K, Bacher A, Eisenreich W (2001) The non-mevalonate pathway of isoprenoids: genes, enzymes and intermediates. Curr Opin Chem Biol 5:535-540
136. 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
137. Rüffer M, Kan-Fan C, Husson HP, Stöchigt J, Zenk MH (1979) 4,1-Dehydrogeissoschizine, an intermediate in heteroyohimbine alkaloid biosynthesis. J Chem Soc Chem Commun 1016-1018
138. Sagner S, Eisenreich W, Fellermeier M, Latzel C, Bacher A, Zenk MH (1998) Biosynthesis of 2-C-methyl-d-erythritol in plants by rearrangement of the terpenoid precursor 1-deoxy-d-xylulose 5-phosphate. Tetrahedron Lett 39:2091-2094
139. 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 42c:1075-1081
140. Scheel D (1998) Resistance response physiology and signal transduction. Curr Opin Plant Biol 1(4):305-310
141. 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
142. Schulte AE (1998) Regulation of mevalonate metabolism in Catharanthus roseus. PhD thesis, Leiden University, The Netherlands
143. Schulte AE, van der Heijden R, Verpoorte R (1999) Purification and characterization of phosphomevalonate kinase from Catharanthus roseus. Phytochemistry 52:975-983
144. Schulte AE, van der Heijden R, Verpoorte R (2000) Purification and characterization of mevalonate kinase from Catharanthus roseus (L.) G. Don. Arch Biochem Biophys 378:287-298
145. Schwender J, Müller C, Zeidler J, Lichtenthaler HK (1999) Cloning and heterologous expression of a cDNA encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase of Arabidopsis thaliana. FEBS Lett 455:140-144
146. Scott AI, Lee SL, Wan W (1977) Indole alkaloid biosynthesis: partial purification of ajmalicine synthase from Catharanthus roseus. Biochem Biophys Res Commun 75:1004-1009
147. Shanks JV, Bhadra R (1997) Characteristics of selected hairy root lines of Catharanthus roseus. In: Doran PM (ed) Hairy roots. Harwood, Reading, UK, pp 51-63
148. Sierra M (1991) Aspects of indole alkaloid accumulation in Tabernaemontana tissue cultures: differentiation, peroxidases and stability. PhD thesis, Leiden University, The Netherlands
149. Smith JI, Smart NJ, Kurz WGW, Misawa M (1987) Stimulation of indole alkaloid production in cell suspension cultures of Catharanthus roseus by abscisic acid. Planta Med 53:470-474
150. Sommer S, Severin K, Camara B, Heide L (1995) Intracellular localization of geranylpyrophosphate synthase from cell cultures of Lithospermum erythrorhizon. Phytochemistry 38:623-627
151. Sottomayor M, de Pinto MC, Salema R, DiCosmo F, Pedreno MA, Ros Barcelo A (1996) The vacuolar localization of a basic peroxidase isoenzyme responsible for the synthesis of α-3′, 4′-anhydrovinblastine in Catharanthus roseus (L.) G. Don leaves. Plant Cell Environ 19:761-767
152. Sottomayor M, Lopez-Serrano M, DiCosmo F, 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
153. Sprenger GA (1996) Carbohydrate metabolism in Zymomonas mobilis: a catabolic highway with some scenic routes. FEMS Microbiol Lett 145:301-307
154. Sprenger GA, Schorken U, Wiegert T, Grolle S, de Graaf AA, Taylor SV, Begley TP, Bringer-Meyer S, Sahm H (1997) Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-d-xylulose. Proc Natl Acad Sci USA 94:12857-12862
155. St-Pierre B, 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
156. St-Pierre B, Laflamme P, Alarco AM, De Luca V (1998) The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. Plant J 14:703-713
157. St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:887-900
158. Stermer BA, Bianchini GM, Korth KL (1994) Regulation of HMG-CoA reductase activity in plants: review. J Lipid Res 35:1133-1140
159. Stevens LH (1994) Formation and conversion of strictosidine in the biosynthesis of monoterpenoid indole and quinoline alkaloids. PhD thesis, Leiden University, The Netherlands
160. Stevens LH, Blom TJM, Verpoorte R (1993) Subcellular localization of tryptophan decarboxylase, strictosidine synthase and strictosidine β-d-glucosidase in suspension cultured cells of Catharanthus roseus and Tabernaemontana divaricata. Plant Cell Rep 12:573-576
161. Stöckigt J (1980) In: Phillipson JD, Zenk MH (eds) Indole and biogenetically related alkaloids. Academic, London, p 113
162. Takahashi S, Kuzuyama T, Watanabe H, Seto H (1998) A 1-deoxy-d-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-d-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc Natl Acad Sci USA 95:9879-9884
163. Treimer JF, Zenk MH (1979) Purification and properties of strictosidine synthase, the key enzyme in indole alkaloid formation. Eur J Biochem 101:225-233
164. Uesato S, Ogawa Y, Inouye H, Saiki K, Zenk MH (1986) Synthesis of iridodial by cell free extracts from Rauwolfia serpentina cell suspension cultures. Tetrahedron Lett 27:2893-2896
165. Uesato S, Ikeda H, Fujita T, Inouye H, Zenk MH (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
166. Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295-297
167. Van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43-53
168. Van der Heijden R, Verpoorte R (1995) Metabolic enzymes of 3-hydroxy-3-methylglutaryl-coenzyme A in Catharanthus roseus. Plant Cell Tissue Organ Cult 43:85-88
169. Van der Heijden R, Boer-Hlupa V, Verpoorte R, Duine JA (1994) Enzymes involved in the metabolism of 3-hydroxy-3-methylglutaryl-coenzyme A in Catharanthus roseus. Plant Cell Tissue Organ Cult 38:345-348
170. Vasquez-Flota FA, De Luca V (1998) Jasmonate modulates development- and light-regulated alkaloid biosynthesis in Catharanthus roseus. Phytochemistry 49:395-402
171. Vasquez-Flota FA, De Carolis ED, Alarco AM, De Luca V (1997) Molecular cloning and characterization of desacetoxyvindoline-4-hydroxylase, a 2-oxoglutarate dependent-dioxygenase involved in the biosynthesis of vindoline in Catharanthus roseus (L.) G. Don. Plant Mol Biol 34:935-948
172. Vasquez-Flota FA, St-Pierre B, De Luca V (2000) Light activation of vindoline biosynthesis does not require cytomorphogenesis in Catharanthus roseus seedlings. Phytochemistry 55:531-536
173. Veau B, Courtois M, Oudin A, Chenieux JC, Rideau M, Clastre M (2000) Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochem Biophys Acta 1517:159-163
174. Verpoorte R (1998) Exploration of nature's chemodiversity: the role of secondary metabolites as lead for drug development. Drug Dev Today 3:232-238
175. Verpoorte R, Alfermann AW (2000) Metabolic engineering of plant secondary metabolism. Kluwer Academic Publishers, Dordrecht
176. Verpoorte R, van der Heijden R, Moreno PRH (1997) Biosynthesis of terpenoid indole alkaloids in Catharanthus roseus cells. In: Cordell GA (ed) The alkaloids, vol 49. Academic, San Diego, pp 221-299
177. Verpoorte R, van der Heijden R, Memelink J (1998) Plant biotechnology and the production of alkaloids: prospects of metabolic engineering. In: Cordell GA (ed) The alkaloids, vol 50. Academic, San Diego, pp 453-508
178. Verpoorte R, van der Heijden R, Memelink J (2000) Engineering the plant cell factory for secondary metabolite production. Transgenic Res 9:323-343
179. Verpoorte R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1:13-25
180. Vetter HP, Mangold U, Schröder G, Marner FJ, Werck-Reichhart D, Schröder J (1992) Molecular analysis and heterologous expression of an inducible cytochrome P450 protein from periwinkle (Catharanthus roseus L.). Plant Physiol 100:998-1007
181. Vollack KU, Bach TJ (1995) In: Kader JC, Mazliak P (eds) Plant lipid metabolism. Kluwer Academic Publishers, Dordrecht, p 335
182. Weber T, Bach TJ (1994) Conversion of acetyl-coenzyme A into 3-hydroxy-3-methylglutaryl-coenzyme A in radish seedlings; evidence of a single monomeric protein catalyzing a FeII/quinone-stimulated double condensation reaction. Biochim Biophys Acta 1211:85-96
183. Weissenborn DL, Denbow CJ, Laine M, Lang SS, Yang Z, Yu X, Cramer CL (1995) HMG-CoA reductase and terpenoid phytoalexines: molecular specialization within a complex pathway. Physiol Plant 93:393-400
184. Whitmer S (1999) Aspects of terpenoid indole alkaloid formation by transgenic cell lines of Catharanthus roseus over-expressing tryptophan decarboxylase and strictosidine synthase. PhD thesis, Leiden University
185. Whitmer S, Canel C, Hallard D, Goncalves C, Verpoorte R (1998) Influence of precursor availability on alkaloid accumulation by transgenic cell line of Catharanthus roseus. Plant Physiol 116:853-857
186. Whitmer S, van der Heijden R, Verpoorte R (2002a) Effect of precursor feeding on alkaloid accumulation by a strictosidine synthase over-expressing transgenic cell line S1 of Catharanthus roseus. Plant Cell Tissue Organ Cult 69:85-93
187. Whitmer S, van der Heijden R, Verpoorte R (2002b) Effect of precursor feeding on alkaloid accumulation by a tryptophan decarboxylase overexpressing transgenic cell line T22 of Catharanthus roseus. J Biotechnol 96:193-203
188. Yahia A, Kevers C, Gaspar T, Chènieux J, Rideau M, Crèche J (1998) Cytokinins and ethylene stimulate indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms. Plant Sci 133:9-15
189. Yamamoto H, Katano N, Ooi A, Inoue K (2000) Secologanin synthase which catalyzes the oxidative cleavage of loganin into secologanin is a cytochrome P450. Phytochemistry 53:7-12
190. Zhao J, Zhu W, Hu Q, He XW (2000a) Improved indole alkaloid production in Catharanthus roseus suspension cultures by various chemicals. Biotechnol Lett 22:1221-1226
191. Zhao J, Zhu W, Hu Q (2000b) Promotion of indole alkaloid production in Catharanthus roseus cell cultures by rare earth elements. Biotechnol Lett 22:825-828
192. Zhao J, Zhu W, Hu Q (2001a) Effects of light and plant growth regulators on the biosynthesis of vindoline and other indole alkaloids in Catharanthus roseus callus cultures. Plant Growth Regul 33:43-49
193. Zhao J, Zhu W, Hu Q (2001b) Enhanced catharanthine production in catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Technol. May 7; 28(7-8):673-681
194. Zhao J, Zhu W, Hu Q (2001c) Selection of fungal elicitors to increase indole alkaloid accumulation in catharanthus roseus suspension cell culture. Enzyme Microb Technol. May 7; 28(7-8):666-672
195. Zheng Z, Wu M (2004) Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Sci 166:507-514