Deciphering the evolution, cell biology and regulation of monoterpene indole alkaloids

Advances in Botanical Research

Volumn 68, Issue , 2013, Pages 73-109

  St Pierre, Benoit ^a   Besseau, Sébastien ^a   Clastre, Marc ^a   Courdavault, Vincent ^a   Courtois, Martine ^a   Crèche, Joel ^a   Ducos, Eric ^a   de Bernonville, Thomas Dugé ^a   Dutilleul, Christelle ^a   Glévarec, Gaëlle ^a   Imbault, Nadine ^a   Lanoue, Arnaud ^a   Oudin, Audrey ^a   Papon, Nicolas ^a   Pichon, Olivier ^a   Giglioli Guivarc'h, Nathalie ^a  

^a UNIVERSITÉ DE TOURS   (France)

Author keywords

Catharanthus; Enzyme subcellular localisation; Evolution; Metabolism regulation; Monoterpene indole alkaloids; Pathway architecture; Phytohormone; Secondary metabolism

Indexed keywords

EID: 84881004454     PISSN: 00652296     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-408061-4.00003-1     Document Type: Chapter

References (126)

1. Aerts R., Gisi D., De Carolis E., De Luca V., Baumann T.W. Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings. The Plant Journal 1994, 5:635-643.
2. Amini A., Andreu F., Glévarec G., Rideau M., Crèche J. Down-regulation of the CrHPT1 histidine phosphotransfer protein prevents cytokinin-mediated up-regulation of CrDXR, and CrG10H transcript levels in periwinkle cell cultures. Molecular Biology Reports 2012, 39:8491-8496.
3. Amini A., Glévarec G., Andreu F., Rideau M., Crèche J. Low levels of gibberellic acid control the biosynthesis of Ajmalicine in Catharanthus roseus cell suspension cultures. Planta Medica 2009, 75:187-191.
4. APG III,THE ANGIOSPERM PHYLOGENY GROUP An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 2009, 161:105-121.
5. Arvy M.-P., Imbault N., Naudascher F., Thiersault M., Doireau P. 2,4-D and alkaloid accumulation in periwinkle cell suspensions. Biochimie 1994, 76:410-416.
6. Berlin J., Rügenhagen C., Kuzovkina I.N., Fecker L.F., Sasse F. Are tissue cultures of Peganum harmala a useful model system for studying how to manipulate the formation of secondary metabolites?. Plant Cell, Tissue and Organ Culture 1994, 38:289-297.
7. Burlat V., Oudin A., Courtois M., Rideau M., St-Pierre B. 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. The Plant Journal 2004, 38:131-141.
8. Campos-Tamayo F., Hernandez-Dominguez E., Vazquez-Flota F.A. Vindoline formation in shoot cultures of Catharanthus roseus is synchronously activated with morphogenesis through the last biosynthetic step. Annals of Botany 2008, 102:409-415.
9. Chahed K., Oudin A., Guivarc'h N., Hamdi S., Chénieux J.C., Rideau M., et al. 1-Deoxy-D-xylulose 5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant Physiology and Biochemistry 2000, 38:559-566.
10. Chakravorty D., Botella J.R. Over-expression of a truncated Arabidopsis thaliana heterotrimeric G protein γ subunit results in a phenotype similar to α and β subunit knockouts. Gene 2007, 393:163-170.
11. Chockalingam S., Sundari M.S.N., Thenmozhi S. Impact of the extract of Catharanthus roseus on feeding and enzymatic digestive activities of Spodoptera litura. Journal of Environmental Biology 1989, 10:303-307.
12. Contin A., van der Heijden R., Lefebre A.W., Verpoorte R. The iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture. FEBS Letters 1998, 4:413-416.
13. Costa M.M., Hilliou F., Duarte P., Pereira L.G., Almeida I., Leech M., et al. Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiology 2008, 146:403-417.
14. Courdavault V., Burlat V., St-Pierre B., Giglioli-Guivarc'h N. Characterisation of CaaX-prenyltransferases in Catharanthus roseus: Relationships with the expression of genes involved in the early stages of monoterpenoid biosynthetic pathway. Plant Science 2005, 168:1097-1107.
15. Courdavault V., Burlat V., St-Pierre B., Giglioli-Guivarc'h N. 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 Reports 2009, 28:83-93.
16. Courdavault V., Clastre M., Simkin A.D., Giglioli-Guivarc'h N. Prenylated proteins are required for methyl-jasmonate-induced monoterpenoid indole alkaloids biosynthesis in Catharanthus roseus. Isoprenoid synthesis in plants and microorganisms 2013, 285-296. Springer, New York. T.J. Bach, M. Rhomer (Eds.).
17. Courdavault V., Thiersault M., Courtois M., Gantet P., Oudin A., Doireau P., et al. CaaX-prenyltransferases are essential for expression of genes involved in the early stages of monoterpenoid biosynthetic pathway in Catharanthus roseus cells. Plant Molecular Biology 2005, 57:855-870.
18. De Luca V., Cutler A.J. Subcellular localization of enzymes involved in indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiology 1987, 85:1099-1102.
19. De Luca V., Balsevich J., Tyler R.T., Eilert U., Panchuk B.D., Kurz W.G.W. Biosynthesis of indole alkaloids: Developmental regulation of the biosynthetic pathway from tabersonine to vindoline in Catharanthus roseus. Journal of Plant Physiology 1986, 125:147-156.
20. De Luca V., St-Pierre B. The cell and developmental biology of alkaloid biosynthesis. Trends in Plant Sciences 2000, 5:168-173.
21. Décendit A., Liu D., Ouelhazi L., Doireau P., Mérillon J.M., Rideau M. Cytokinin-enhanced accumulation of indole alkaloids in Catharanthus roseus cell cultures. The factors affecting the cytokinin response. Plant Cell Reports 1992, 11:400-403.
22. De-Eknamkul W., Suttipanta N., Kutchan T.M. Purification and characterization of deacetylipecoside synthase from Alangium lamarckii Thw. Phytochemistry 2000, 55:177-181.
23. Devoto A., Turner J.G. Jasmonate-regulated Arabidopsis stress signalling network. Physiologia Plantarum 2005, 123:161-172.
24. DiCosmo F., Quesnel A., Misawa M., Tallevi S.G. Increased synthesis of ajmalicine and catharanthine by cell suspension cultures of Catharanthus roseus in response to fungal culture-filtrates. Applied Biochemistry and Biotechnology 1987, 14:101-106.
25. Dinda B., Debnath S., Harigaya Y. Naturally occurring iridoids. A review, part 1. Chemical and Pharmaceutical Bulletin 2007, 55:159-222.
26. Dinda B., Debnath S., Harigaya Y. Naturally occurring secoiridoids and bioactivity of naturally occurring iridoids and secoiridoids-A review, part 2. Chemical and Pharmaceutical Bulletin 2007, 55:689-728.
27. Eilert U., Constabel F., Kurz W.G.W. Elicitor-stimulation of monoterpene indole alkaloids formation in suspension cultures of Catharanthus roseus. Journal of Plant Physiology 1986, 126:11-22.
28. Eilert U., Nesbitt L.R., Constabel F. Laticifers and latex in fruits of periwinkle, Catharanthus roseus. Canadian Journal of Botany 1985, 63:1540-1546.
29. El-Sayed M., Verpoorte R. Methyljasmonate accelerates catabolism of monoterpenoid indole alkaloids in Catharanthus roseus during leaf processing. Fitoterapia 2005, 76:83-90.
30. Facchini P.J., St-Pierre B. Synthesis and trafficking of alkaloid biosynthetic enzymes. Current Opinion in Plant Biology 2005, 8:657-666.
31. Gantet P., Imbault N., Thiersault M., Doireau P. Necessity of a functional octadecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant & Cell Physiology 1998, 39:220-225.
32. Geerlings A., Ibanñez M.M.-L., Memelink J., van der Heijden R., Verpoorte R. Molecular cloning and analysis of strictosidine β-D-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Journal of Biological Chemistry 2000, 275:3051-3056.
33. Gelb M.H., Brunsveld L., Hrycyna C.A., Michaelis S., Tamanoi F., Van Voorhis W.C., et al. Therapeutic intervention based on protein prenylation and associated modifications. Nature Chemical Biology 2006, 2:518-528.
34. Gerasimenko I., Sheludko Y., Ma X., Stöckigt J. Heterologous expression of a Rauvolfia cDNA encoding strictosidine glucosidase, a biosynthetic key to over 2000 monoterpenoid indole alkaloids. European Journal of Biochemistry 2002, 269:2204-2213.
35. Gerber E., Hemmerlin A., Hartmann M., Heintz D., Hartmann M.A., Mutterer J., et al. The plastidial 2-C-methyl-d-erythritol 4-phosphate pathway provides the isoprenyl moiety for protein geranylgeranylation in tobacco BY-2 cells. The Plant Cell 2009, 21:285-300.
36. Geu-Flores F., Sherden N.H., Courdavault V., Burlat V., Glenn W.S., Wu C., et al. An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 2012, 492:138-142.
37. Giddings L.A., Liscombe D.K., Hamilton J.P., Childs K.L., DellaPenna D., Buell C.R., et al. A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. Journal of Biological Chemistry 2011, 286:16751-16757.
38. Giglioli-Guivarch N., Courdavault V., Oudin A., Crèche J., Crèche J., St-Pierre B. Madagascar periwinkle, an attractive model for studying the control of the biosynthesis of terpenoid derivative compounds. Floriculture, ornamental and plant biotechnology: Advances and topical issues 2006, Vol. 2. Global Science Books, Ikenobe, Japan. 1st ed. J.A. Texeira da Silva (Ed.).
39. Ginis O., Oudin A., Guirimand G., Chebbi M., Courdavault V., Glévarec G., et al. A type-B response regulator drives the expression of the hydroxymethylbutenyl diphosphate synthase gene in periwinkle. Journal of Plant Physiology 2012, 169:1571-1574.
40. Grosse W., Klapheck S. Enzymic studies on the biosynthesis of serotonin and the regulation in walnuts (Juglans regia L.). Zeitschrift für Pflanzenphysiologie 1979, 93:359-363.
41. Guirimand G., Burlat V., Oudin A., Lanoue A., St-Pierre B., Courdavault V. Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and itsapplication to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Reports 2009, 28:1215-1234.
42. Guirimand G., Courdavault V., Lanoue A., Mahroug S., Guihur A., Blanc N., et al. Strictosidine activation in Apocynaceae: Towards a "nuclear time bomb?". BMC Plant Biology 2010, 10:182.
43. Guirimand G., Courdavault V., St-Pierre B., Burlat V. Biosynthesis and regulation of alkaloids. Plant developmental biology-Biotechnological perspectives 2010, Vol. 2:139-160. Springer-Verlag, Berlin, Heidelberg. E.-C. Pua, M.R. Davey (Eds.).
44. Guirimand G., Ginis O., Guihur A., Poutrain P., Hericourt F., Oudin A., et al. The subcellular organization of strictosidine biosynthesis in Catharanthus roseus epidermis highlights several transtonoplast translocations of intermediate metabolites. FEBS Journal 2011, 278:749-763.
45. Guirimand G., Guihur A., Phillips M.A., Oudin A., Glévarec G., Melin C., et al. A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus. Plant Molecular Biology 2012, 79:443-459.
46. Guirimand G., Guihur A., Poutrain P., Hericourt F., Mahroug S., St-Pierre B., et al. Spatial organization of the vindoline biosynthetic pathway in Catharanthus roseus. Journal of Plant Physiology 2011, 168:519-628.
47. Hedhili S., Courdavault V., Giglioli-Guivarc'h N., Gantet P. Regulation of the terpene moiety biosynthesis of Catharanthus roseus terpene indole alkaloids. Phytochemistry Reviews 2007, 6:341-351.
48. Hicks M.A., Barber A.E., Giddings L.A., Caldwell J., O'Connor S.E., Babbittet P.C. The evolution of function in strictosidine synthase-like proteins. Proteins: Structure, Function and Bioinformatics 2011, 79:3082-3098.
49. Howe G.A., Jander G. Plant immunity to insect herbivores. Annual Review of Plant Biology 2008, 59:41-66.
50. Hwang I., Chen H.C., Sheen J. Two-component signal transduction pathways in Arabidopsis. Plant Physiology 2002, 129:500-515.
51. Imbault N., Thiersault M., Dupéron P., Benabdelmouna A., Doireau P. Pravastatin: A tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspension. Physiologia Plantarum 1996, 98:803-809.
52. Irmler S., Schroder G., St-Pierre B., Crouch N.P., Hotze M., Schmidt J., et al. Indole alkaloid biosynthesis in Catharanthus roseus: New enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase. The Plant Journal 2000, 24:797-804.
53. Janssens S.B., Knox E.B., Huysmans S., Smets E.F., Merckx V.S.F.T. Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene: Results of a global climate change. Molecular Phylogenetics and Evolution 2009, 52:806-824.
54. Jensen S.R. Systematic implications of the distribution of iridoids and other chemical compounds in the Loganiaceae and other families of the Asteridae. Annals of the Missouri Botanical Garden 1992, 79:284-302.
55. Jensen S.R., Schripsema J. Chemotaxonomy and pharmacology of Gentianaceae. Gentianaceae: Systematics and natural history 2002, 573-632. Cambridge University Press, Cambridge. L. Struwe, V.A. Albert (Eds.).
56. Kibble N.A.J., Sohani M.M., Shirley N., Byrt C., Roessner U., Bacic A., et al. Phylogenetic analysis and functional characterisation of strictosidine synthase-like genes in Arabidopsis thaliana. Functional Plant Biology 2009, 36:1098-1109.
57. Kissen R., Rossiter J.T., Bones A.M. The 'mustard oil bomb': Not so easy to assemble?! Localization, expression and distribution of the components of the myrosinase enzyme system. Phytochemistry Reviews 2009, 8:69-86.
58. Kliebenstein D.J., Kroymann J., Mitchell-Olds T. The glucosinolate-myrosinase system in an ecological and evolutionary context. Current Opinion in Plant Biology 2005, 8:264-271.
59. Konno K., Hirayama C., Yasui H., Nakamura M. Enzymatic activation of oleuropein: A protein crosslinker used as a chemical defense in the privet tree. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:9159-9164.
60. Konno K., Okada S., Hirayama C. Selective secretion of free glycine, a neutralizer against a plant defense chemical, in the digestive juice of the privet moth larvae. Journal of Insect Physiology 2001, 47:1451-1457.
61. Kutchan T.M. A role for intra- and intercellular translocation in natural product biosynthesis. Current Opinion in Plant Biology 2005, 8:292-300.
62. Laflamme P., St-Pierre B., De Luca V. Molecular and biochemical analysis of a Madagascar periwinkle root-specific minovincinine-19-hydroxy-O-acetyltransferase. Plant Physiology 2001, 125:189-198.
63. Larsson S. The "new" chemosystematics: Phylogeny and phytochemistry. Phytochemistry 2007, 68:2903-2907.
64. Levac D., Murata J., Kim W.S., De Luca V. Application of carborundum abrasion for investigating the leaf epidermis: Molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase. The Plant Journal 2008, 53:225-236.
65. Liscombe D.K., MacLeod B.P., Loukanina N., Nandi O.I., Facchini P.J. Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 2005, 66:2501-2520.
66. Lorence A., Nessler C.L. Camptothecin, over four decades of surprising findings. Phytochemistry 2004, 65:2735-2749.
67. Luijendijk T.J.C., van der Meijden E., Verpoorte R. Involvement of strictosidine as a defensive chemical in Catharanthus roseus. Journal of Chemical Ecology 1996, 22:1355-1366.
68. Ma X.Y., Panjikar S., Koepke J., Loris E., Stöckigt J. The structure of Rauvolfia serpentina strictosidine synthase is a novel six-bladed β-propeller fold in plant proteins. The Plant Cell 2006, 18:907-920.
69. Mahroug S., Burlat V., St-Pierre B. Cellular and sub-cellular organization of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Phytochemistry Reviews 2007, 6:363-381.
70. Mahroug S., Courdavault V., Thiersault M., St-Pierre B., Burlat V. Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs. Planta 2006, 223:1191-1200.
71. Mano Y., Nemoto K. The pathway of auxin biosynthesis in plants. Journal of Experimental Botany 2012, 63:2853-2872.
72. McKnight T.D., Bergey D.R., Burnett R.J., Nessler C.L. Expression of enzymatically active and correctly targeted strictosidine synthase in transgenic tobacco plants. Planta 1991, 185:148-152.
73. Meisner J., Weissenberg M., Palevitch D., Aharonson N. Phagodeterrency induced by leaves and leaf extracts of Catharanthus roseus in the larva of Spodoptera littoralis (Lepidoptera, Noctuidae). Journal of Economic Entomology 1981, 74:131-135.
74. Memelink J., Verpoorte R., Kijne J.W. ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends in Plant Science 2001, 6:212-219.
75. Menke F.L., Champion A., Kijne J.W., Memelink J. 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 Journal 1999, 18:4455-4463.
76. Menke F.L., Parchmann S., Mueller M.J., Kijne J.W., Memelink J. Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthclic genes in Catharanthus roseus. Plant Physiology 1999, 119:1289-1296.
77. Mersey B.G., Cutler A.J. Differential distribution of specific indole alkaloids in leaves of Catharanthus roseus. Canadian Journal of Botany 1986, 64:1039-1045.
78. Morant A.V., Jorgensen K., Jorgensen C., Paquette S.M., Sanchez-Perez R., Moller B.L., et al. β-glucosidases as detonators of plant chemical defense. Phytochemistry 2008, 69:1795-1813.
79. Murata J., De Luca V. The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. The Plant Cell 2008, 20:524-542.
80. Murata J., Roepke J., Gordon H., De Luca V. 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. The Plant Journal 2005, 44:581-594.
81. Nelson D., Werck-Reichhart D. A P450-centric view of plant evolution. The Plant Journal 2011, 66:194-211.
82. Nomura T., Quesada A.L., Kutchan T.M. The new β-D-glucosidase in terpenoid-isoquinoline alkaloid biosynthesis in Psychotria ipecacuanha. Journal of Biological Chemistry 2008, 283:34650-34659.
83. Nour-Eldin H.H., Halkier B.A. The emerging field of transport engineering of plant specialized metabolites. Current Opinion in Biotechnology 2013, 24:263-270.
84. Ober D., Hartmann T. Homospermidine synthase, the first pathway-specific enzyme of pyrrolizidine alkaloid biosynthesis, evolved from deoxyhypusine synthase. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:14777-14782.
85. Oudin A., Courtois M., Rideau M., Clastre M. The iridoid pathway in Catharanthus roseus alkaloid biosynthesis. Phytochemistry Reviews 2007, 6:259-276.
86. Oudin A., Mahroug S., Courdavault V., Hervouet N., Zelwer C., Rodríguez-Concepción M., et al. Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Molecular Biology 2007, 65:13-30.
87. Ouwerkerk P.B.F., Hallard D., Verpoorte R., Memelink J. Identification of UV-B light-responsive regions in the promoter of the tryptophan decarboxylase gene from Catharanthus roseus. Plant Molecular Biology 1999, 41:491-503.
88. Pan Q., Chen Y., Wang Q., Yuan F., Xing S., Tian Y. Effect of plant growth regulators on the biosynthesis of vinblastine, vindoline and catharanthine in Catharanthus roseus. Plant Growth Regulation 2010, 60:133-141.
89. Papon N., Bremer J., Vansiri A., Andreu F., Rideau M., Crèche J. Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells. Planta Medica 2005, 71:572-574.
90. Pasqua G., Monacelli B., Valletta A. Cellular localisation of the anti-cancer drug camptothecin in Camptotheca acuminata Decne (Nyssaceae). European Journal of Histochemistry 2004, 48:321-328.
91. 2+-release components act in opposite ways in the regulation of the auxin- dependent MIA biosynthesis in Catharanthus roseus cells. Journal of Experimental Botany 2009, 60:1387-1398.
92. Reimann A., Nurhayati N., Backenköhler A., Ober D. Repeated evolution of the pyrrolizidine alkaloid-mediated defense system in separate angiosperm lineages. The Plant Cell 2004, 16:2772-2784.
93. Rodriguez S., Compagnon V., Crouch N.P., St-Pierre B., De Luca V. Jasmonate-induced epoxidation of tabersonine by a cytochrome P-450 in hairy root cultures of Catharanthus roseus. Phytochemistry 2003, 64:401-409.
94. Rodríguez-Concepción M., Yalovsky S., Gruissem W. Protein prenylation in plants: Old friends and new targets. Plant Molecular Biology 1999, 39:865-870.
95. Roepke J., Salim V., Wu M., Thamm A.M.K., Murata J., Ploss K., et al. Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:15287-15292.
96. Samanani N., Liscombe D.K., Facchini P.J. Molecular cloning and characterization of norcoclaurine synthase, an enzyme catalyzing the first committed step in benzylisoquinoline biosynthesis. The Plant Journal 2004, 40:302-313.
97. Schafer W.R., Rine J. Protein prenylation: Genes, enzymes, targets and functions. Annual Review of Genetics 1992, 26:209-237.
98. Schattat M., Barton K., Baudisch B., Klösgen R.B., Mathur J. Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiology 2011, 155:1667-1677.
99. Simkin A.J., Miettinen K., Claudel P., Burlat V., Guirimand G., Courdavault V., et al. Characterization of the plastidial geraniol synthase from Madagascar periwinkle which initiates the monoterpenoid branch of the alkaloid pathway in internal phloem associated parenchyma. Phytochemistry 2013, 85:36-43.
100. Singla B., Chugh A., Khurana J.P., Khurana P. An early auxinresponsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. Journal of Experimental Botany 2006, 57:4059-4070.
101. Smith J.I., Smart N.J., Kurz W.G.W., Misawa M. Stimulation of indole alkaloid production in cell suspension cultures of Catharanthus roseus by abscisic acid. Planta Medica 1987, 53:470-474.
102. Stöckigt J., Barleben L., Panjikar S., Loris E.A. 3D-Structure and function of strictosidine synthase-the key enzyme of monoterpenoid indole alkaloid biosynthesis. Plant Physiology and Biochemistry 2008, 46:340-355.
103. Stöckigt J., Panjikar S. Structural biology in plant natural product biosynthesis-Architecture of enzymes from monoterpenoid indole and tropane alkaloid biosynthesis. Natural Product Reports 2007, 24:1382-1400.
104. St-Pierre B., De Luca V. A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiology 1995, 109:131-139.
105. St-Pierre B., Laflamme P., Alarco A.M., De Luca V. The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. The Plant Journal 1998, 14:703-713.
106. St-Pierre B., Vázquez-Flota F.A., De Luca V. Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. The Plant Cell 1999, 11:887-900.
107. Szabó L.F. Rigorous biogenetic network for a group of indole alkaloids derived from strictosidine. Molecules 2008, 13:1875-1896.
108. COI1 complex during jasmonate signalling. Nature 2007, 448:661-665.
109. To J.P., Kieber J.J. Cytokinin signaling: Two-components and more. Trends in Plant Science 2008, 13:85-92.
110. Trusov Y., Rookes J.E., Chakravorty D., Armour D., Schenk P.M., Botella J.R. Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiology 2006, 140:210-220.
111. Valletta A., Trainotti L., Santamaria A.R., Pasqua G. Cell-specific expression of tryptophan decarboxylase and 10-hydroxygeraniol oxidoreductase, key genes involved in camptothecin biosynthesis in Camptotheca acuminata Decne (Nyssaceae). BMC Plant Biology 2010, 10:69.
112. van der Fits L., Memelink J. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 2000, 289:295-297.
113. van der Heijden R., Jabos D.J., Snoeijer W., Hallard D., Verpoorte R. The Catharanthus alkaloids: Pharmacognosy and biotechnology. Current Medicinal Chemistry 2004, 11:607-628.
114. Vázquez-Flota F., Carrillo-Pech M., Minero-García Y., Miranda-Ham M.L. Alkaloid metabolism in wounded Catharanthus roseus seedlings. Plant Physiology and Biochemistry 2004, 42:623-628.
115. Vazquez-Flota F.A., De Carolis E.D., Alarco A.M., De Luca V. 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 Molecular Biology 1997, 34:935-948.
116. Vazquez-Flota F., De Luca V. Jasmonate modulates development and light regulated alkaloid biosynthesis in Catharanthus roseus. Phytochemistry 1998, 49:395-402.
117. Vazquez-Flota F.A., St-Pierre B., De Luca V. Light activation of vindoline biosynthesis does not require cytomorphogenesis in Catharanthus roseus seedlings. Phytochemistry 2000, 55:531-536.
118. Veau B., Courtois M., Oudin A., Chenieux J.C., Rideau M., Clastre M. Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochimica et Biophysica Acta 2000, 1517:159-163.
119. Wikström N., Savolainen V., Chase M.W. Evolution of the angiosperms: Calibrating the family tree. Proceedings of the Royal Society B Biological Sciences 2001, 268:2211-2220.
120. Yahia A., Kevers C., Gaspar T., Chénieux J.C., Rideau M., Crèche J. Cytokinins and ethylene stimulate indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms. Plant Sciences 1998, 133:9-15.
121. Yazaki K. Transporters of secondary metabolites. Current Opinion in Plant Biology 2005, 8:301-307.
122. Yazaki K., Sugiyama A., Morita M., Shitan N. Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochemistry Reviews 2008, 7:513-524.
123. Yoder L.R., Mahlberg P.G. Reactions of alkaloid and histochemical indicators in laticifers and specialized parenchyma cells of Catharanthus roseus (Apocynaceae). American Journal of Botany 1976, 63:1167-1173.
124. Zhang H., Hedhili S., Montiel G., Zhang Y., Chatel G., Pré M., et al. The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. The Plant Journal 2011, 67:61-71.
125. Zhao Y. Auxin biosynthesis: A simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Molecular Plant 2012, 5:334-338.
126. Ziegler J., Facchini P. Alkaloid biosynthesis: Metabolism and trafficking. Annual Review of Plant Biology 2008, 59:735-769.