Molecular regulation of terpenoid indole alkaloids pathway in the medicinal plant, Catharanthus roseus

Journal of Medicinal Plants Research

Volumn 5, Issue 5, 2011, Pages 663-676

  Zhou, Mei Liang ^a,b   Hou, Hong Li ^c   Zhu, Xue Mei ^a   Shao, Ji Rong ^a   Wu, Yan Min ^b   Tang, Yi Xiong ^b  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c Shenzhen Imported Center for Quality Crop Seed   (China)

Author keywords

Compartmentalization; Indole alkaloid; Jasmonate; Nitric oxide; Phytohormone; Prenylated proteins

Indexed keywords

AJMALICINE; ALKALOID DERIVATIVE; ANHYDROVINBLASTINE; BERBERINE; CATHARANTHINE; ETHYLENE; INDOLE ALKALOID; ISOQUINOLINE; JASMONIC ACID; NITRIC OXIDE; PLANT MEDICINAL PRODUCT; STRICTOSIDINE; TERPENE; TERPENOID DERIVATIVE; TERPENOID INDOLE ALKALOID DERIVATIVE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; VINBLASTINE; VINCRISTINE; VINDOLINE;

BIOSYNTHESIS; CATHARANTHUS ROSEUS; DRUG SYNTHESIS; GROWTH REGULATION; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT GROWTH; PLANT LEAF; PLANT METABOLISM; PLANT STEM; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PRENYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

CATHARANTHUS ROSEUS;

EID: 79955368579     PISSN: 19960875     EISSN: 19960875     Source Type: Journal    
DOI: None     Document Type: Review

References (103)

1. Alcantara J, Bird DA, Franceschi VR, Facchini J (2005). Sanguinarine biosynthesis is associated with the endoplasmic reticulum in cultured opium poppy cells after elicitor treatment. Plant Physiol., 138: 173-183.
2. Allen GJ, Murata Y, Chu SP, Nafisi M, Schoeder JI (2002). Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell, 14: 1649-1662.
3. Amini A, Glévarec G, Andreu F, Rideau M, Crèche J (2009). Low levels of gibberellic acid control the biosynthesis of Ajmalicine in Catharanthus roseus cell suspension cultures. Planta Med., 75: 187-191.
4. Barbora P, Jaroslav D, Jiřina D, Kazufumi Y, Sittiruk R, Verpoorte R (2009). Improved accumulation of ajmalicine and tetrahydroalstonine in Catharanthus cells expressing an ABC transporter. J. Plant Physiol., 166: 1405-1412.
5. Benjamins R, Scheres B (2008). Auxin: The looping star in plant development. Annu. Rev. Plant Biol., 59: 443-465.
6. Besson-Bard A, Pugin A, Wendehenne D (2008). New insights into nitric oxide signaling in plants. Annu. Rev. Plant Physiol., 59: 21-39.
7. Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006). ABA induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J., 45: 113-122.
8. Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (2004). Coexpression 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 mono-terpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J., 38: 131-141.
9. Casey PJ (1995). Protein lipidation in cell signaling. Science, 268: 221-225.
10. Chatel G, Montiel G, Metal P (2003). CrMYC1, a Catharanthus roseus elicitor-and jasmonate-responsive bHLH transcription factor that binds the G-box element of the strictosidine synthase gene promoter. J. Exp. Bot., 54: 2587-2588.
11. Chini A, Fonseca S, Fernández G, Adiel B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448: 666-671.
12. 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.
13. Courdavault V, Burlat V, St-Pierre B, 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 C. roseus. Plant Cell Rep., 28: 83-93.
14. 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 C. roseus cells. Plant Mol. Biol., 57: 855-870.
15. Costa MMR, Hilliou F, Duarte P, Pereira LG, Almeida I, Leech M, Memelink J, Barceló AR, Sottomayor M (2008). Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in C. roseus. Plant Physiol., 146: 403-417.
16. De Carolis E, Chan F, Balsevich J, De Luca V (1990). Isolation and characterization of a 2-oxoglu-tarate-dependent dioxygenase involved in the second-to-last step in vindoline biosynthesis. Plant Physiol., 94: 1323-1329.
17. Decendit A, Liu D, Ouelhazi L, Doireau P, Mérillon 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.
18. Decendit A, Petit G, Andreu F, Doireau P, Mérillon 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.
19. Devoto A, Turner JG (2005). Jasmonate-regulated Arabidopsis stress signalling network. Physiol Plantarum., 123: 161-172.
20. Dutta A, Sen J, Deswal R (2007). Downregulation of terpenoid indole alkaloid biosynthetic pathway by low temperature and cloning of a AP2 type C-repeat binding factor (CBF) from C. roseus (L). G. Don. Plant Cell Rep., 26: 1869-1878.
21. Elizabeta H, Freddy CT, Vázquez-Flota F (2004). Vindoline synthesis in in vitro shoot cultures of C. roseus. Biotechnol. Lett., 26: 671-674.
22. 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.
23. El-Sayed M, Verpoorte R (2004). Growth, metabolic profiling and enzymes activities of Catharan thus roseus seedlings treated with plant growth regulators. Plant Growth Regul., 44: 53-58.
24. Gagne J, Smalle J, Gingerich D, Walker J, Yoo S, Yanagisawa S, Vierstra R (2004). Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad. Sci. U.S.A., 101: 6803-6808.
25. Geerlings A, Martinez-Lozano IM, 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.
26. Gen-ichiro A, Stefan G, Massimo M, Simone B, Birgit S, Margit L, Axel M, Wilhelm B (2008). Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta, 227: 453-464.
27. Goddijn OJM, De Kam RJ, Zanetti A, Schilperoort RA, Hoge JHC (1992). Auxin rapidly down-regulates transcription of the tryptophan decarboxylase gene from C. roseus. Plant Mol. Biol., 18: 1113-1120.
28. Goossens A, Hakkinen ST, Laakso I, Oksman-Caldentey KM, Inze D (2003). Secretion of secondary metabolites by ATP-binding cassette transporters in plant cell suspension cultures. Plant Physiol., 131: 1161-1164.
29. 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 applicat-ion to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep., 28: 1215-1234.
30. Guo H, Ecker J (2003). Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell., 115: 667-677.
31. Hedhili S, Courdavault V, Giglioli-Guivarc'h N, Gantet P (2007). Regulation of the terpene moiety biosynthesis of Catharanthus roseus terpene indole alkaloids. Phytochem. Rev., 6: 341-351.
32. Howe GA, Jander G (2008). Plant immunity to insect herbivores. Annu. Rev. Plant Biol., 59: 41-66.
33. Hua J, Meyerowitz E (1998). Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell, 94: 261-271.
34. 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. Plantarum, 98: 803-809.
35. 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.
36. Jin HB, Liu DH, Zuo KJ, Gong YF, Miao ZQ, Chen YH, Ren WW, Sun XF, Tang KX (2007). Molecular cloning and characterization of Crmdr1, a novel MDR-type ABC transporter gene from Catharanthus roseus. DNA Sequence, 18: 316-325.
37. Jordan MA, Thrower D, Wilson L (1991). Mechanism of Inhibition of Cell Proliferation by Vinca Alkaloids. Cancer Res., 51: 2212-2222.
38. Kende H (1993). Ethylene biosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol., 44: 283-307.
39. Kendrick MD, Chang C (2008). Ethylene signaling: new levels of complexity and regulation. Curr. Opin. Plant Biol., 11: 479-485.
40. Kutchan TM (2005). A role for intra-and intercellular translocation in natural product biosynthesis. Curr. Opin. Plant Biol., 8: 292-300.
41. Laflamme P, St-Pierre B, De Luca V (2001). Molecular and biochemical analysis of a Madag-ascar periwinkle rootspecific minovincinine-19-hydroxy-O-acetyltransferase. Plant Physiol., 125: 189-198.
42. Lange BM, Rujan T, Martin W, Croteau R (2000). Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. U.S.A., 97: 13172-13177.
43. Lee-Parsons CWT, Ertürk S (2005). Ajmalicine production in methyl jasmonate-induced Cathar-anthus roseus cell cultures depends on Ca2+ level. Plant Cell Rep., 24: 677-682.
44. Lee-Parsons CWT, Ertürk S, Tengtrakool J (2004). Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnol. Lett., 26: 1595-1599.
45. Madyastha KM, Ridgway JE, Dwyer JG, Coscia CJ (1977). Subcellular localization of a cytochrome P-450-dependent monooxygenase in vesicles of the higher plant Catharanthus roseus. J. Cell Biol., 72: 303-313.
46. Mahroug S, Burlat V, St-Pierre B (2007). Cellular and sub-cellular organisation of the mono-terpenoid indole alkaloid pathway in Catharanthus roseus. Phytochem. Rev., 6: 363-381.
47. Maldonado-Mendoza IE, Burnett RJ, Lbpez-Meyer M, Nessler CL (1994). Regulation of 3-hydroxy-3-methylglutaryi-coenzyme A reductase by wounding and methyl jasmonate. Plant Cell Tissue Organ Cult., 38: 351-356.
48. 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.
49. Memelink J, Verpoorte R, Kijne W (2001). ORCAnization of jasmonateresponsive gene expression in alkaloid metabolism. Trends Plant Sci., 6: 212-219.
50. 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 elicitorinducible AP2-domain transcription factor, ORCA2. EMBO J., 18: 4455-4463.
51. Moreno-Valenzuela OA, Minero-García Y, Brito-Argaez L, Carbajal-Mora E, Echeverría O, Vázquez-Nin G, Loyola-Vargas VM (2003). Immunocytolocalization of tryptophan decarboxy-lase in C. roseus hairy roots. Mol. Biotechnol., 23: 11-18.
52. 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.
53. Ng CK, McAinsh MR (2003). Encoding specificity in plant calcium signaling: hot-spotting the ups and downs and waves. Ann. Bot., 92: 477-485.
54. Oksman-Caldentey KM, Inzé D (2004). Plant cell factories in the postgenomic era: new ways to produce designer secondary metabolites. Trends Plant Sci., 9: 433-440.
55. Otani M, Shitan N, Sakai K, Martinoia E, Sato F, Yazaki K (2005). Characterization of Vacuolar Transport of the Endogenous Alkaloid Berberine in Coptis japonica. Plant Physiol., 138: 1939-1946.
56. Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodriguez-Concepcion M, St-Pierre B, Burlat V (2007). 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.
57. Ouelhazi L, Filali M, Décendit A, Chénieux JC, Rideau M (1993). Differential protein accumulation in zeatin-and 2,4-D-treated cells of Catharanthus roseus. Correlation with indole alkaloid biosynthesis. Plant Physiol. Biochem., 31: 421-431.
58. Ouwerkerk PBF, Memelink J (1999). A G-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.
59. Pan QF, Chen Y, Wang Q, Yuan F, Xing SH, Tian YS, Zhao JY, Sun XF, Tang KX (2010). Effect of plant growth regulators on the biosynthesis of vinblastine, vindoline and catharanthine in Catharanthus roseus. Plant Growth Regul., 60: 133-141.
60. Papon N, Bremer J, Vansiri A, Andreu F, Rideau M, Creche J (2005). Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathways in Catharanthus roseus suspension cells. Planta Med., 71: 572-574.
61. Papon N, Senoussi MM, Andreu F, Rideau M, Chenieux JC, Creche J (2004). Cloning of a gene encoding a putative ethylene receptor in Catharanthus roseus and its expression in plant and cell cultures. Biol. Plantarum, 48: 345-350.
62. Pasquali G, Goddijn OJM, De Waal A, Verpoorte R, Schilperoort RA, Hoge JHC, Memelink J (1992). Coordinated regulation of two indole alkaloid biosynthetic genes from Catharanthus roseus by auxin and elicitors. Plant Mol. Biol., 18: 1121-1131.
63. Pauw B, Hilliou FAO, Martin VS, Chatel G, de Wolf CJF, Champion A, Martial P, van Duijn B, Kijne JW, 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.
64. Pieterse CMJ, Antonio LR, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol., 5: 308-316.
65. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003). EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F Box proteins: EBF1 and EBF2. Cell, 115: 679-689.
66. Poutrain P, Mazars C, Thiersault M, Rideau M, Pichon O (2009). Two distinct intracellular Ca2+-release components act in opposite ways in the regulation of the auxin-dependent MIA biosynthesis in Catharanthus roseus cells. J. Exp. Bot., 60: 1387-1398.
67. Pré M, Atallah M, Champion A, De Vos M, Pieterse CMJ, Memelink J (2008). The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol., 147: 1347-1357.
68. Qiao WH, Fan LM (2008). Nitric oxide signaling in plant responses to abiotic stresses. J. Integr. Plant Biol., 50: 1238-1246.
69. Quint M, Gray WM (2006) Auxin signaling. Curr. Opin. Plant Biol., 9: 448-453.
70. Rodriguez S, Compagnon V, Crouch NP, St-Pierre B, De Luca V (2003). Jasmonate-induced epoxidation of tabersonine by cytochrome P-450 in hairy root cultures of Catharanthus roseus. Phytochemistry, 64: 401-409.
71. Roytrakul S, Verpoorte R (2007). Role of vacuolar transporter proteins in plant secondary metabolism: Catharanthus roseus cell culture. Phytochem. Rev., 6: 383-396.
72. Schafer WF, Rine J (1992). Protein prenylation: Genes, enzymes, targets and functions. Annu. Rev. Genet., 30: 209-237.
73. Scheiner-Bobis G (2001). Sanguinarine induces K+ outflow from yeast cells expressing mammalian sodium pumps. N-S. Arch. Pharmacol., 7: 1288-1289.
74. Sibéril Y, Benhamron S, Memelink J, Giglioli-Guivarc'h N, Thiersault M, Boisson B, Doireau P, Gantet P (2001). Catharanthus roseus G-box binding factors 1 and 2 act as repressors of stricto-sidine synthase gene expression in cell cultures. Plant Mol. Biol., 45: 477-488.
75. Singh SN, Vats P, Suri S, Shyam R, Kumria MML, Rangganathan S, Sridharan K (2001). Effect of an antidiabetic extract of Catharanthus roseus on enzymatic activities in steptozotocin induced diabetic rats. J. Ethnopharmacol., 76: 269-277.
76. Sirikantaramas S, Yamazaki M, Saito K (2008). Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochem. Rev., 7: 467-477.
77. 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.
78. Sottomayor M, De Pinto MC, Salema R, Dicosmo F, Pedreno MA, Barcelo AR (1996). The vacuolar localization of a basic peroxidase isoenzyme responsible for the synthesis of a-30,40-anhydrovinblastine in Catharanthus roseus (L) G. Don leaves. Plant Cell Environ., 19: 761-767.
79. Stevens LH, Blom TJM, Verpoorte R (1993). Subcellular localization of tryptophan decarboxylase, strictosidine synthase and strictosidine glucosidase in suspension cultured cells of Catharanthus roseus and Tabernaemontana divaricata. Plant Cell Rep., 12: 563-576.
80. Stevens LH, Schripsema J, Pennings EJM, Verpoorte R (1992). Activities of enzymes involved in indole alkaloid biosynthesis in suspension cultures of Catharanthus, Cinchona and Tabernaemontana species. Plant Physiol. Biochem., 30: 675-681.
81. 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.
82. St-Pierre B, Vázquez-Flota FA, De Luca V (1999). Multi-cellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell, 11: 887-900.
83. Stuehr DJ, Santolini J, Wang ZQ, Wei CC, Adak S (2004). Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem., 279: 36167-36170.
84. Suttipanta N, Pattanaik S, Gunjan S, Xie CH, Littleton J, Yuan L (2007). Promoter analysis of the Catharanthus roseus geraniol 10-hydroxylase gene involved in terpenoid indole alkaloid biosynthesis. Biochimica et Biophysica Acta, 1769: 139-148.
85. Tang ZH, Yang L, Zu YG, Guo XR (2009). Variations of vinblastine accumulation and redox state affected by exogenous H2O2 in Catharanthus roseus (L.)G. Don. Plant Growth Regul., 57: 15-20.
86. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature, 448: 661-665.
87. Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Anderson D, Chen JG, Jones AM, Botella JR (2007) Heterotrimeric G protein gamma subunits provide functional selectivity in Gbc dimer signaling in Arabidopsis. Plant Cell, 19: 1235-1250.
88. Van der Fits L, Memelink J (2000). ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289: 295-297.
89. Van der Fits L, Memelink J (2001). The jasmonate-inducible AP2/ERFdomain transcrition factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J., 25: 43-53.
90. Van der Fits L, Zhang H, Menke FLH, Deneka M, Memelink J (2000). A Catharanthus roseus BPF-1 homologue interacts with an elicitorresponsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway. Plant Mol. Biol., 44: 675-685.
91. Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R (2004). The Catharant-hus alkaloids: pharmacognosy and biotechnology. Curr. Med. Chem., 11: 607-628.
92. Vázquez-Flota F, Moreno-Valenzuela O, Miranda-Ham ML, Coello-Coello J, Loyola-Vargas VM (1994). Catharanthine and ajmalicine synthesis in Catharanthus roseus hairy root cultures. Plant Cell Tissue Organ Cult., 38: 273-279.
93. 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. Biochimica et Biophysica Acta, 1517: 159-163.
94. Verpoorte R, Choi YH, Mustafa NR, Kim HK (2008). Metabolomics: back to basics. Phytochem. Rev., 7: 525-537.
95. Weiss D, Baumert A, Vogel M, Roos W (2006). Sanguinarine reductase, a key enzyme of benzophenanthridine detoxification. Plant Cell Environ., 29: 291-302.
96. Willem FB, Stijn LD, Miguel FC De Bolle, Bruno PAC (2006). The role of ethylene in host-pathogen interactions. Annu. Rev. Phytopathol., 44: 393-416.
97. Xu MJ, Dong JF (2005). Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells. Appl. Microbiol. Biotechnol., 67: 40-44.
98. Xu MJ, Dong JF (2007a). Enhancing terpeniod indole alkaloid production by inducible expression of mammalian Bax in Catharanthus roseus cells. Sci. China Ser. C Life Sci., 50: 234-241.
99. Xu MJ, Dong JF (2007b). Involvement of nitric oxide signaling in mammalian Bax-induced terpenoid indole alkaloid production of Catharanthus roseus cells. Sci. China Ser. C Life Sci., 50: 799-807.
100. Yazaki K (2006). ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett., 580: 1183-1191.
101. Zhao J, Zhu WH, Hu Q (2001). 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.
102. Zhou ML, Shao JR, Tang YX (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.
103. Zhou ML, Zhu XM, Shao JR, Wu YM, Tang YX (2010). Transcriptional response of the catharanthine biosynthesis pathway to methyl jasmonate/nitric oxide elicitation in Catharanthus roseus hairy root culture. Appl. Microbiol. Biotechnol., 88: 737-750.