Phytochemical genomics of the Madagascar periwinkle: Unravelling the last twists of the alkaloid engine

Phytochemistry

Volumn 113, Issue , 2015, Pages 9-23

  Dugé De Bernonville, Thomas ^a   Clastre, Marc ^a   Besseau, Sébastien ^a   Oudin, Audrey ^a   Burlat, Vincent ^b,c   Glévarec, Gaëlle ^a   Lanoue, Arnaud ^a   Papon, Nicolas ^a   Giglioli Guivarc'H, Nathalie ^a   St Pierre, Benoit ^a   Courdavault, Vincent ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b Centre National de la Recherche Scientifique   (France)

^c CNRS   (France)

Author keywords

Alkaloids; Apocynaceae; Catharanthus roseus; High throughput sequencing; Madagascar periwinkle; Phytochemical genomics; Transcriptomics

Indexed keywords

ANTINEOPLASTIC AGENT; PLANT MEDICINAL PRODUCT; RAUWOLFIA ALKALOID; STRICTOSIDINE; TRANSCRIPTOME; VINBLASTINE; VINCA ALKALOID;

CATHARANTHUS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; GENOMICS; ISOLATION AND PURIFICATION; MADAGASCAR; METABOLISM;

ANTINEOPLASTIC AGENTS; CATHARANTHUS; GENOMICS; MADAGASCAR; MOLECULAR STRUCTURE; PHYTOCHEMICALS; SECOLOGANIN TRYPTAMINE ALKALOIDS; TRANSCRIPTOME; VINBLASTINE; VINCA ALKALOIDS;

EID: 84937909377     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2014.07.023     Document Type: Review

References (105)

1. R.J. Aerts, D. Gisi, E. Carolis, V. Luca, and T.W. Baumann Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings Plant J. 5 1994 635 643
2. K. Asada, V. Salim, S. Masada-Atsumi, E. Edmunds, M. Nagatoshi, K. Terasaka, H. Mizukami, and V. De Luca A 7-deoxyloganetic acid glucosyltransferase contributes a key step in secologanin biosynthesis in Madagascar periwinkle Plant Cell 25 2013 4123 4134
3. D.C. Baulcombe Fast forward genetics based on virus induced gene silencing Curr. Opin. Plant Biol. 2 1999 109 113
4. S. Besseau, F. Kellner, A. Lanoue, A.M. Thamm, V. Salim, B. Schneider, F. Geu-Flores, R. Höfer, G. Guirimand, A. Guihur, A. Oudin, G. Glevarec, E. Foureau, N. Papon, M. Clastre, N. Giglioli-Guivarc'h, B. St-Pierre, D. Werck-Reichhart, V. Burlat, V. De Luca, S.E. O'Connor, and V. Courdavault A pair of tabersonine 16-hydroxylases initiates the synthesis of vindoline in an organ dependent manner in Catharanthus roseus Plant Physiol. 163 2013 1792 1803
5. T.M. Burch-Smith, J.C. Anderson, G.B. Martin, and S.P. Dinesh-Kumar Applications and advantages of virus-induced gene silencing for gene function studies in plants Plant J. 39 2004 734 746
6. T.M. Burch-Smith, M. Schiff, Y. Liun, and S.P. Dinesh-Kumar Efficient virus-induced gene silencing in Arabidopsis Plant Physiol. 142 2006 21 27
7. V. Burlat, A. Oudin, M. Courtois, M. Rideau, and B. St-Pierre 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 2004 131 141
8. K. Chahed, A. Oudin, N. Guivarc'h, S. Hamdi, J.C. Chénieux, M. Rideau, and M. Clastre 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 2000 559 566
9. A. Champagne, H. Rischer, K.M. Oksman-Caldentey, and M. Boutry In-depth proteome mining of cultured Catharanthus roseus cells identifies candidate proteins involved in the synthesis and transport of secondary metabolites Proteomics 12 2012 3536 3547
10. G. Chatel, G. Montiel, M. Pré, J. Memelink, M. Thiersault, B. St-Pierre, P. Doireau, and P. Gantet 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 2003 2587 2588
11. J.C. Chen, C.Z. Jiang, T.E. Gookin, D.A. Hunter, D.G. Clark, and M.S. Reid Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence Plant Mol. Biol. 55 2004 521 530
12. W.-Y. Chen, and C.-P. Lin Characterization of Catharanthus roseus genes regulated differentially by peanut witches' broom phytoplasma infection J. Phytopathol. 159 2011 505 510
13. B. Chevreux, T. Pfisterer, B. Drescher, A.J. Driesel, W.E.G. Müller, T. Wetter, and S. Suhai Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs Genome Res. 14 2004 1147 1159
14. E. Chung, E. Seong, Y.C. Kim, E.J. Chung, S.K. Oh, S. Lee, J.M. Park, Y.H. Joung, and D. Choi A method of high frequency virus-induced gene silencing in chili pepper (Capsicum annuum L. cv. Bukang) Mol. Cells 17 2004 377 380
15. G. Collu, N. Unver, A.M. Peltenburg-Looman, R. van der Heijden, R. Verpoorte, and J. Memelink Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis FEBS Lett. 508 2001 215 220
16. M.M. Costa, F. Hilliou, P. Duarte, L.G. Pereira, I. Almeida, M. Leech, J. Memelink, A.R. Barceló, and M. Sottomayor Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus Plant Physiol. 146 2008 403 417
17. V. Courdavault, N. Papon, M. Clastre, N. Giglioli-Guivarc'h, B. St-Pierre, and V. Burlat A look inside an alkaloid multisite plant: the Catharanthus logistics Curr. Opin. Plant Biol. 19 2014 43 50
18. V. Courdavault, M. Thiersault, M. Courtois, P. Gantet, A. Oudin, P. Doireau, B. St-Pierre, and N. Giglioli-Guivarc'h CaaX-prenyltransferases are essential for expression of genes involved in the early stages of monoterpenoid biosynthetic pathway in Catharanthus roseus cells Plant Mol. Biol. 57 2005 855 870
19. E. De Carolis, F. Chan, J. Balsevich, and V. De Luca Isolation and characterization of a 2-oxoglutarate dependent dioxygenase involved in the second-to-last step in vindoline biosynthesis Plant Physiol. 94 1990 1323 1329
20. V. De Luca, J. Balsevich, R.T. Tyler, and W.G.W. Kurz Characterization of a novel N-methyltransferase (NMT) from Catharanthus roseus plants Plant Cell Rep. 6 1987 458 461
21. V. De Luca, J.A. Alvarez Fernandez, D. Campbell, and W. Kurz Developmental regulation of enzymes of indole alkaloid biosynthesis in Catharanthus roseus Plant Physiol. 86 1988 447 450
22. V. De Luca, C. Marineau, and N. Brisson Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases Proc. Natl. Acad. Sci. U.S.A. 86 1989 2582 2586
23. V. De Luca, V. Salim, D. Levac, S. Masada Atsumi, and F. Yu Discovery and functional analysis of monoterpenoid indole alkaloid pathways in plants Methods Enzymol. 515 2012 207 229
24. V. De Luca, and B. St-Pierre The cell biology of alkaloid biosynthesis: evolution with a twist Trends Plant Sci. 5 2000 168 173
25. M. Dethier, and V. De Luca Partial purification of an N-methyltransferase involved in vindoline biosynthesis in Catharanthus roseus Phytochemistry 32 1993 673 678
26. J. Duffin Poisoning the spindle: serendipity and discovery of the anti-tumor properties of the vinca alkaloids Can. Bull. Med. Hist. 17 2000 155 192
27. P.J. Facchini, J. Bohlmann, P.S. Covello, V. De Luca, R. Mahadevan, J.E. Page, D.K. Ro, C.W. Sensen, R. Storms, and V.J. Martin Synthetic biosystems for the production of high-value plant metabolites Trends Biotechnol. 30 2012 127 131
28. A. Geerlings, M.M. Ibañez, J. Memelink, R. van Der Heijden, and R. Verpoorte Molecular cloning and analysis of strictosidine beta-d-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus J. Biol. Chem. 275 2000 3051 3056
29. F. Geu-Flores, N.H. Sherden, V. Courdavault, V. Burlat, W.S. Glenn, C. Wu, E. Nims, Y. Cui, and S.E. O'Connor An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis Nature 492 2012 138 142
30. L.A. Giddings, D.K. Liscombe, J.P. Hamilton, K.L. Childs, D. DellaPenna, C.R. Buell, and S.E. O'Connor A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus J. Biol. Chem. 286 2011 16751 16757
31. O. Ginis, A. Oudin, G. Guirimand, M. Chebbi, V. Courdavault, G. Glévarec, N. Papon, J. Crèche, and M. Courtois A type-B response regulator drives the expression of the hydroxymethylbutenyl diphosphate synthase gene in periwinkle J. Plant Physiol. 169 2012 1571 1574
32. E. Góngora-Castillo, K.L. Childs, G. Fedewa, J.P. Hamilton, D.K. Liscombe, M. Magallanes-Lundback, K.K. Mandadi, E. Nims, W. Runguphan, B. Vaillancourt, M. Varbanova-Herde, D. DellaPenna, T.D. McKnight, S. O'Connor, and C.R. Buell Development of transcriptomic resources for interrogating the biosynthesis of monoterpene indole alkaloids in medicinal plant species PLoS One 7 2012 e52506
33. M.G. Grabherr, B.J. Haas, M. Yassour, J.Z. Levin, D.A. Thompson, I. Amit, X. Adiconis, L. Fan, R. Raychowdhury, Q. Zeng, Z. Chen, E. Mauceli, N. Hacohen, A. Gnirke, N. Rhind, F. di Palma, B.W. Birren, C. Nusbaum, K. Lindblad-Toh, N. Friedman, and A. Regev Full-length transcriptome assembly from RNA-Seq data without a reference genome Nat. Biotechnol. 29 2011 644 652
34. G. Guimarães, L. Cardoso, H. Oliveira, C. Santos, P. Duarte, and M. Sottomayor Cytogenetic characterization and genome size of the medicinal plant Catharanthus roseus (L.) G. Don AoB Plants 2012 2012 pls002
35. G. Guirimand, V. Burlat, A. Oudin, A. Lanoue, B. St-Pierre, and V. Courdavault Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and its application to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase Plant Cell Rep. 28 2009 1215 1234
36. G. Guirimand, V. Courdavault, A. Lanoue, S. Mahroug, A. Guihur, N. Blanc, N. Giglioli-Guivarc'h, B. St-Pierre, and V. Burlat Strictosidine activation in Apocynaceae: towards a "nuclear time bomb"? BMC Plant Biol. 10 2010 182
37. G. Guirimand, A. Guihur, O. Ginis, P. Poutrain, F. Héricourt, A. Oudin, A. Lanoue, B. St-Pierre, V. Burlat, and V. Courdavault The subcellular organization of strictosidine biosynthesis in Catharanthus roseus epidermis highlights several trans-tonoplast translocations of intermediate metabolites FEBS J. 278 2011 749 763
38. G. Guirimand, A. Guihur, M.A. Phillips, A. Oudin, G. Glévarec, C. Melin, N. Papon, M. Clastre, B. St-Pierre, M. Rodríguez-Concepción, V. Burlat, and V. Courdavault A single gene encodes isopentenyl diphosphate isomerase isoforms targeted to plastids, mitochondria and peroxisomes in Catharanthus roseus Plant Mol. Biol. 79 2012 443 459
39. G. Guirimand, A. Guihur, P. Poutrain, F. Héricourt, S. Mahroug, B. St-Pierre, V. Burlat, and V. Courdavault Spatial organization of the vindoline biosynthetic pathway in Catharanthus roseus J. Plant Physiol. 168 2011 549 557
40. L.C. Hileman, S. Drea, G. de Martino, A. Litt, and V.F. Irish Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (Opium poppy) Plant J. 44 2005 334 341
41. R. Höfer, L. Dong, F. André, J.-F. Ginglinger, R. Lugan, C. Gavira, S. Grec, G. Lang, J. Memelink, S. Van Der Krol, H. Bouwmeester, and D. Werck-Reichhart Geraniol hydroxylase and hydroxygeraniol oxidase activities of the CYP76 family of cytochrome P450 enzymes and potential for engineering the early steps of the (seco)iridoid pathway Metab. Eng. 20 2013 221 232
42. S. Irmler, G. Schröder, B. St-Pierre, N.P. Crouch, M. Hotze, J. Schmidt, D. Strack, U. Matern, and J. Schröder Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase Plant J. 24 2000 797 804
43. D.I. Jacobs, M. Gaspari, J. van der Greef, R. van der Heijden, and R. Verpoorte Proteome analysis of the medicinal plant Catharanthus roseus Planta 221 2005 690 704
44. H. Jia, and Y. Shen Virus-induced gene silencing in strawberry fruit Methods Mol. Biol. 975 2013 211 218
45. T.M. Kutchan, N. Hampp, F. Lottspeich, K. Beyreuther, and M.H. Zenk The cDNA clone for strictosidine synthase from Rauvolfia serpentina. DNA sequence determination and expression in Escherichia coli FEBS Lett. 237 1988 40 44
46. P. Laflamme, B. St-Pierre, and V. De Luca Molecular and biochemical analysis of a Madagascar periwinkle root-specific minovincinine-19-hydroxy-O-acetyltransferase Plant Physiol. 125 2001 189 198
47. D. Leménager, L. Ouelhazi, S. Mahroug, B. Veau, B. St-Pierre, M. Rideau, J. Aguirreolea, V. Burlat, and M. Clastre Purification, molecular cloning, and cell-specific gene expression of the alkaloid-accumulation associated protein CrPS in Catharanthus roseus J. Exp. Bot. 56 2005 1221 1228
48. D. Levac, J. Murata, W.S. Kim, and V. De Luca Application of carborundum abrasion for investigating the leaf epidermis: Molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase Plant J. 53 2008 225 236
49. B. Li, and C.N. Dewey RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome BMC Bioinform. 12 2011 323
50. Y. Li, W. Chen, D. Ma, and Y. Wu CDNA-AFLP analysis revealed genes potentially implicated in Catharanthus roseus flowers during wheat blue dwarf phytoplasma infection Physiol. Mol. Plant Pathol. 84 2013 1 9
51. L. Li, C.J. Stoeckert, and D.S. Roos OrthoMCL: identification of ortholog groups for eukaryotic genomes Genome Res. 13 2003 2178 2189
52. D.K. Liscombe, A.R. Usera, and S.E. O'Connor Homolog of tocopherol C methyltransferases catalyzes N methylation in anticancer alkaloid biosynthesis Proc. Natl. Acad. Sci. U.S.A. 107 2010 18793 18798
53. D.K. Liscombe, and S.E. O'Connor A virus-induced gene silencing approach to understanding alkaloid metabolism in Catharanthus roseus Phytochemistry 72 2011 1969 1977
54. Y. Liu, M. Schiff, and S.P. Dinesh-Kumar Virus-induced gene silencing in tomato Plant J. 31 2002 777 786
55. R. Luo, B. Liu, Y. Xie, Z. Li, W. Huang, J. Yuan, G. He, Y. Chen, Q. Pan, Y. Liu, J. Tang, G. Wu, H. Zhang, Y. Shi, Y. Liu, C. Yu, B. Wang, Y. Lu, C. Han, D.W. Cheung, S.-M. Yiu, S. Peng, Z. Xiaoqian, G. Liu, X. Liao, Y. Li, H. Yang, J. Wang, T.-W. Lam, and J. Wang SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler Gigascience 1 2012 18
56. S.A. Macfarlane Tobraviruses - plant pathogens and tools for biotechnology Mol. Plant Pathol. 11 2010 577 583
57. S. Mahroug, V. Courdavault, M. Thiersault, B. St-Pierre, and V. Burlat Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs Planta 223 2006 1191 1200
58. J.A. Martin, and Z. Wang Next-generation transcriptome assembly Nat. Rev. Genet. 12 2011 671 682
59. T.D. McKnight, C.A. Roessner, R. Devagupta, A.I. Scott, and C.L. Nessler Nucleotide sequence of a cDNA encoding the vacuolar protein strictosidine synthase from Catharanthus roseus Nucleic Acids Res. 18 1990 4939
60. F.L. Menke, A. Champion, J.W. Kijne, and J. Memelink 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 1999 4455 4463
61. K. Miettinen, L. Dong, N. Navrot, T. Schneider, V. Burlat, J. Pollier, L. Woittiez, S. van der Krol, R. Lugan, T. Ilc, R. Verpoorte, K.M. Oksman-Caldentey, E. Martinoia, H. Bouwmeester, A. Goossens, J. Memelink, and D. Werck-Reichhart The seco-iridoid pathway from Catharanthus roseus Nat. Commun. 5 2014 3066
62. J. Murata, D. Bienzle, J.E. Brandle, C.W. Sensen, and V. De Luca Expressed sequence tags from Madagascar periwinkle (Catharanthus roseus) FEBS Lett. 580 2006 4501 4507
63. J. Murata, and V. De Luca 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 2005 581 594
64. J. Murata, J. Roepke, H. Gordon, and V. De Luca The leaf epidermome of Catharanthus roseus reveals its biochemical specialization Plant Cell 20 2008 524 542
65. A. Oudin, M. Courtois, M. Rideau, and M. Clastre The iridoid pathway in Catharanthus roseus alkaloid biosynthesis Phytochem. Rev. 6 2007 259 276
66. A. Oudin, S. Mahroug, V. Courdavault, N. Hervouet, C. Zelwer, M. Rodríguez-Concepción, B. St-Pierre, and V. Burlat Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus Plant Mol. Biol. 65 2007 13 30
67. N. Papon, A. Vansiri, P. Gantet, J.C. Chénieux, M. Rideau, and J. Crèche Histidine-containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in Catharanthus roseus suspension cells FEBS Lett. 558 2004 85 88
68. B. Pauw, F.A.O. Hilliou, V. Sandonis Martin, G. Chatel, C.F.J. de Wolf, A. van Champion, B. Duijn, J.W. Kijne, L. van der Fits, and J. Memelink Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus J. Biol. Chem. 279 2004 52940 52948
69. M. Pré, Y. Sibéril, J. Memelink, A. Champion, P. Doireau, and P. Gantet Isolation by yeast one-hybrid system of cDNAs encoding transcription factors that bind to the G-box element of the strictosidine synthase gene promoter from Catharanthus roseus Int. J. Biochrom. 5 2000 229 244
70. A. Rai, S.S. Smita, A.K. Singh, K. Shanker, and D.A. Nagegowda Heteromeric and homomeric geranyl diphosphate synthases from Catharanthus roseus and their role in monoterpene indole alkaloid biosynthesis Mol. Plant 6 2013 1531 1549
71. F. Ratcliff, B.D. Harrison, and D.C. Baulcombe A similarity between viral defense and gene silencing in plants Science 276 1997 1558 1560
72. F. Ratcliff, A.M. MartIn-Hernandez, and D.C. Baulcombe Tobacco rattle virus as a vector for analysis of gene function by silencing Plant J. 25 2001 237 245
73. H. Rischer, M. Oresic, T. Seppänen-Laakso, M. Katajamaa, F. Lammertyn, W. Ardiles-Diaz, M.C. Van Montagu, D. Inzé, K.M. Oksman-Caldentey, and A. Goossens Gene-to-metabolite networks for terpenoid indole alkaloid biosynthesis in Catharanthus roseus cells Proc. Natl. Acad. Sci. U.S.A. 103 2006 5614 5619
74. J. Roepke, V. Salim, M. Wu, A.M.K. Thamm, J. Murata, K. Ploss, W. Boland, and V. De Luca Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle Proc. Natl. Acad. Sci. U.S.A. 107 2010 15287 15292
75. W. Runguphan, and S.E. O'Connor Metabolic reprogramming of periwinkle plant culture Nat. Chem. Biol. 5 2009 151 153
76. W. Runguphan, J.J. Maresh, and S.E. O'Connor Silencing of tryptamine biosynthesis for production of nonnatural alkaloids in plant culture Proc. Natl. Acad. Sci. U.S.A. 106 2009 13673 13678
77. V. Salim, B. Wiens, S. Masada-Atsumi, F. Yu, and V. De Luca 7-Deoxyloganetic acid synthase catalyzes a key 3 step oxidation to form 7-deoxyloganetic acid in Catharanthus roseus iridoid biosynthesis Phytochemistry 101 2014 23 31
78. V. Salim, F. Yu, J. Altarejos, and V. De Luca Virus-induced gene silencing identifies Catharanthus roseus 7-deoxyloganic acid-7-hydroxylase, a step in iridoid and monoterpene indole alkaloid biosynthesis Plant J. 76 2013 754 765
79. G. Schröder, E. Unterbusch, M. Kaltenbach, J. Schmidt, D. Strack, V. De Luca, and J. Schröder Light-induced cytochrome P450-dependent enzyme in indole alkaloid biosynthesis: tabersonine 16-hydroxylase FEBS Lett. 458 1999 97 102
80. M.H. Schulz, D.R. Zerbino, M. Vingron, and E. Birney Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels Bioinformatics 28 2012 1086 1092
81. V. Sharma, S. Chaudhary, S. Srivastava, R. Pandey, and S. Kumar Characterization of variation and quantitative trait loci related to terpenoid indole alkaloid yield in a recombinant inbred line mapping population of Catharanthus roseus J. Genet. 91 2012 49 69
82. A.K. Shukla, and S.P. Khanuja Catharanthus roseus: The Metabolome That Represents a Unique Reservoir of Medicinally Important Alkaloids Under Precise Genomic Regulation, OMICS Applications in Crop Science 2013 CRC Press 325 384
83. A.K. Shukla, A.K. Shasany, M.M. Gupta, and S.P.S. Khanuja Transcriptome analysis in Catharanthus roseus leaves and roots for comparative terpenoid indole alkaloid profiles J. Exp. Bot. 57 2006 3921 3932
84. Y. Sibéril, S. Benhamron, J. Memelink, N. Giglioli-Guivarc'h, M. Thiersault, B. Boisson, P. Doireau, and P. Gantet Catharanthus roseus G-box binding factors 1 and 2 act as repressors of strictosidine synthase gene expression in cell cultures Plant Mol. Biol. 45 2001 477 488
85. A.J. Simkin, K. Miettinen, P. Claudel, V. Burlat, G. Guirimand, V. Courdavault, N. Papon, S. Meyer, S. Godet, B. St-Pierre, N. Giglioli-Guivarc'h, M.J. Fischer, J. Memelink, and M. Clastre Characterization of the plastidial geraniol synthase from Madagascar periwinkle which initiates the monoterpenoid branch of the alkaloid pathway in internal phloem associated parenchyma Phytochemistry 85 2013 36 43
86. J. Stöckigt, and S. Panjikar Structural biology in plant natural product biosynthesis-architecture of enzymes from monoterpenoid indole and tropane alkaloid biosynthesis Nat. Prod. Rep. 24 2007 1382 1400
87. B. St-Pierre, S. Besseau, M. Clastre, V. Courdavault, M. Courtois, J. Crèche, E. Ducos, T.D. de Bernonville, C. Dutilleul, G. Glévarec, N. Imbault, A. Lanoue, A. Oudin, N. Papon, O. Pichon, and N. Giglioli-Guivarc'h New light on alkaloid biosynthesis and future prospects Adv. Bot. Res. 2013 73 109
88. B. St-Pierre, F.A. Vazquez-Flota, and V. De Luca Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate Plant Cell 11 1999 887 900
89. B. St-Pierre, P. Laflamme, A.M. Alarco, and V. De Luca The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer Plant J. 14 1998 703 713
90. B. St-Pierre, and V. De Luca A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus Plant Physiol. 109 1995 131 139
91. G.H. Svoboda, and D.A. Blake The phytochemistry and pharmacology of Catharanthus roseus (L.) G. Don W.I. Taylor, N.R. Farnsworth, The Catharanthus Alkaloids 1975 Marcel Dekker New York
92. Sung, Y.C., Lin, C.P., Chen, J.C., 2014. Optimization of virus-induced gene silencing in Catharanthus roseus. Plant Pathol. (in press) doi: 10.1111/ppa.12186.
93. N. Suttipanta, S. Pattanaik, M. Kulshrestha, B. Patra, S.K. Singh, and L. Yuan The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus Plant Physiol. 157 2011 2081 2093
94. L. van der Fits, and J. Memelink ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism Science 289 2000 295 297
95. L. van der Fits, H. Zhang, F.L. Menke, M. Deneka, and J. Memelink A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway Plant Mol. Biol. 44 2000 675 685
96. A. Van Moerkercke, M. Fabris, J. Pollier, G.J.E. Baart, S. Rombauts, G. Hasnain, H. Rischer, J. Memelink, K.-M. Oksman-Caldentey, and A. Goossens CathaCyc, a metabolic pathway database built from Catharanthus roseus RNA-Seq data Plant Cell Physiol. 54 2013 673 685
97. F.A. Vazquez-Flota, E.D. De Carolis, A.M. Alarco, and V. De Luca 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 1997 935 948
98. B. Veau, M. Courtois, A. Oudin, J.C. Chénieux, M. Rideau, and M. Clastre Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus Biochim. Biophys. Acta 1517 2000 159 163
99. D. Vom Endt, M. Soares e Silva, J.W. Kijne, G. Pasquali, and J. Memelink Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-Hook DNA-binding proteins Plant Physiol. 144 2007 1680 1689
100. F. Wang, J. Flanagan, N. Su, L.C. Wang, S. Bui, A. Nielson, X. Wu, H.T. Vo, X.J. Ma, and Y. Luo RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues J. Mol. Diagn. 14 2012 22 29
101. Q. Wang, S. Xing, Q. Pan, F. Yuan, J. Zhao, Y. Tian, Y. Chen, G. Wang, and K. Tang Development of efficient Catharanthus roseus regeneration and transformation system using Agrobacterium tumefaciens and hypocotyls as explants BMC Biotechnol. 12 2012 34
102. T. Winzer, V. Gazda, Z. He, F. Kaminski, M. Kern, T.R. Larson, Y. Li, F. Meade, R. Teodor, F.E. Vaistij, C. Walker, T.A. Bowser, and I.A. Graham A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine Science 336 2012 1704 1708
103. M. Xiao, Ye. Zhang, X. Chen, E.-J. Lee, C.J.S. Barber, R. Chakrabarty, I. Desgagné-Penix, T.M. Haslam, Y.-B. Kim, E. Liu, G. MacNevin, S. Masada-Atsumi, D.W. Reed, J.M. Stout, P. Zerbe, Yansheng. Zhang, J. Bohlmann, P.S. Covello, V. De Luca, J.E. Page, D.-K. Ro, V.J.J. Martin, P.J. Facchini, and C.W. Sensen Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest J. Biotechnol. 166 2013 122 134
104. F. Yu, and V. De Luca ATP-binding cassette transporter controls leaf surface secretion of anticancer drug components in Catharanthus roseus Proc. Natl. Acad. Sci. U.S.A. 110 2013 15830 15835
105. F. Yu, A.M.K. Thamm, D. Reed, N. Villa-Ruano, A.L. Quesada, E.L. Gloria, P. Covello, and V. De Luca Functional characterization of amyrin synthase involved in ursolic acid biosynthesis in Catharanthus roseus leaf epidermis Phytochemistry 91 2013 122 127