Skip to main content

Molecular Network of Monoterpene Indole Alkaloids (MIAs) Signaling in Plants with Reference to Catharanthus roseus (L.) G. Don

  • Chapter
  • First Online:
Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2

Abstract

Terpenoids are the most functionally and structurally varied group of plant metabolites. These are synthesized in all organisms but are especially abundant and diverse in plants. Despite their diversity of functions and structures, all terpenoids are derived from the common five-carbon (C5) building unit, isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP) through MEP pathway in all living organisms. The MEP pathway synthesizes IPP and DMAPP in plastids in plants and more complex terpenoids are usually formed by “head-to-tail” or “head-to-head” addition of isoprene units. Monoterpene indole alkaloids (MIAs) are one of important class of terpenoids which are C10 terpenoids, consisting of two isoprene units and are the components of more than 2000 defined compounds. These are a large group of plant-derived natural products with a range of pharmacological properties. These MIAs are potent drugs, such as anticancer, antimalarial, and antiarrhythmic agents. These MIAs have been found in eight different plant families, being most common in Apocynaceae, Rubiaceae, and Loganiaceae. Madagascar periwinkle, Catharanthus roseus, the best-characterized MIA-producing plant species, is the source of the valuable MIAs. It has approximately 130 alkaloids of indole group, out of which 25 are dimeric in nature. Some of these compounds have important medicinal properties such as anticancerous property (vincristine and vinblastine) and antiarrhythmic property (ajmalicine and serpentine). In the present chapter, molecular network of monoterpene indole alkaloids (MIAs) signaling in plants with reference to Catharanthus roseus (L.) G. Don has been reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Araki N, Kusumi K, Masamoto K, Niwa Y, Iba K (2000) Temperature-sensitive Arabidopsis mutant defective in 1-deoxy-D-xylulose 5-phosphate synthase within the plastid non-mevalonate pathway of isoprenoid biosynthesis. Physiol Plant 108:19–24

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bach TJ (1995) Some aspects of isoprenoid biosynthesis in plants- A review. Lipids 30:191–202

    Google Scholar 

  • Back K, Chappell J (1996) Identifying functional domains within terpene cyclases using a domain-swapping strategy. Proc Natl Acad Sci U S A 93(13):6841–6845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascade. Plant Cell 12:1103–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besseau S, Kellner F, Lanoue A, Thamm AMK, Salim V, Schneider B, Geu-Flores F, Hofer R, Guirimand G, Guihur A, Oudin A, Glevarec G, Foureau E, Papon N, Clastre M, Giglioli-Guivarch N, St-Pierre B, Werck-Reichhart D, Burlat V, De Luca V, O’Connor SE, Courdavault V (2013) A Pair of Tabersonine 16-Hydroxylases initiates the synthesis of vindoline in an organ-dependent manner in Catharanthus roseus. Plant Physiol 163(4): 1792–1803

    Google Scholar 

  • Binder BYK, Christie AM, Jacqueline P, Shanks V, San KY (2009) The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol Prog 25:861–865

    Article  CAS  PubMed  Google Scholar 

  • Blom TJM, Sierra M, van Vliet TB, Franke-van Dijk MEI, de Koning P, van Iren F, Verpoorte R, Libbenga KR (1991) Uptake and accumulation of ajmalicine into isolated vacuoles of cultured cells of Catharanthus roseus (L.) G. Don and its conversion into serpentine. Planta 183:170–177

    Article  CAS  PubMed  Google Scholar 

  • Bohlmann J, Lins T, Martin W, Eilert U (1996) Anthranilate synthase from Ruta graveolens. Duplicated ASα genes encode tryptophan-sensitive and tryptophan-insensitive isoenzymes specific to amino acid and alkaloid biosynthesis. Plant Physiol 111:507–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M (2001) Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 3:289–300

    Article  CAS  PubMed  Google Scholar 

  • Botella-Pavia P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188–199

    Article  CAS  PubMed  Google Scholar 

  • Bouvier F, Suire C, d’Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24:241–252

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Caelles C, Ferrer A, Balcells L, Hegardt FG, Boronat A (1989) Isolation and structural characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Mol Biol 13:627–638

    Article  CAS  PubMed  Google Scholar 

  • Carretero-Paulet L, Ahumada I, Cunillera N, Rodríguez-Concepción M, Ferrer A, Boronat A, Campos N (2002) Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-d-erythritol 4-phosphate pathway. Plant Physiol 129:1581–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chahed K, Oudin A, Guivarch 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

    Article  CAS  Google Scholar 

  • Choi YH, Tapias EC, Kim HK, Alfons WML, Erkelens C, Jacobus TJ, Berzin J, Zel J, Verpoorte R (2004) Metabolic discrimination of Catharanthus roseus leaves infected by phytoplasma using 1H-NMR spectroscopy and multivariate data analysis. Plant Physiol 135:2398–2410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Contin A, Van der Heijden R, Lefeber AWM, 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

    Article  CAS  PubMed  Google Scholar 

  • Contin A, Collu G, van der Heijden R, Verpoorte R (1999) The effects of phenobarbital and ketonazole on the alkaloid biosynthesis in Catharanthus roseus cell suspension cultures. Plant Physiol Biochem 37:139–144

    Article  CAS  Google Scholar 

  • Cordier H, Karst F, Berges T (1999) Heterologous expression in Saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol Biol 39:953–967

    Article  CAS  PubMed  Google Scholar 

  • Cordoba E, Salmi M, Leon P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60:2933–2943

    Article  CAS  PubMed  Google Scholar 

  • Costa MMR, Hilliou F, Duarte P, Pereira LG, Almeida I, Leech M, Memelink J, Barcelo AR, Sottomayor M (2008) Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus. Plant Physiol 146(2):403–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham FX, Lafond TP, Gantt E (2000) Evidence of a role for LytB in the non mevalonate pathway of isoprenoid biosynthesis. J Bacteriol 182:5841–5848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabricant DS, Farnsworth NR (2001) The value of plants used in traditional medicine for drug discovery. Environ Health Perspect 109(1):69–75, PMCID: PMC1240543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies WJ, Jones HG (1991) Abscisic acid physiology and biochemistry. Bioscientific Publishers, Oxford

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • De Luca V, Laflamme P (2001) The expanding universe of alkaloid biosynthesis. Curr Opin Plant Biol 4:225–233

    Article  PubMed  Google Scholar 

  • De Luca V, Balsevich J, Tyler RT, Eilert U, Panchuk BD, Kurz WGW (1986) Biosynthesis of indole alkaloids: developmental regulation of the biosynthetic pathway from tabersonine to vindoline in Catharanthus roseus. J Plant Physiol 125:147–156

    Google Scholar 

  • De Luca V, Marineau C, Brisson N (1989) Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases. Proc Natl Acad Sci U S A 86(8):2582–2586

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Decendit A, Liu D, Ouelhazi L, Doireau P, Merillon 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

    Article  CAS  PubMed  Google Scholar 

  • Decendit A, Petit G, Andreu F, Doireau P, Merillon 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

    Article  CAS  PubMed  Google Scholar 

  • Dethier M, De Luca V (1993) Partial purification of an N-methyltransferase involved in vindoline biosynthesis in Catharanthus roseus. Phytochemistry 32: 673–678

    Google Scholar 

  • Dewick PM (2002) Medicinal natural products: a biosynthetic approach, 2nd edn. Wiley, Chichester, pp 291–403

    Google Scholar 

  • Dumontet C, Sikic BI (1999) Mechanisms of action of and resistance to anti tubulin agents: microtubule dynamics, drug transport, and cell death. J Clin Oncol 17:1061–1070

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6:277–305

    Article  CAS  Google Scholar 

  • El-Sayed M, Choi YH, Frederich M, Roytrakul S, Verpoorte R (2004) Alkaloid accumulation in Catharanthus roseus cell suspension cultures fed with stemmadenine. Biotechnol Lett 26:793–798

    Google Scholar 

  • Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27

    Article  CAS  PubMed  Google Scholar 

  • Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52:29–66

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fahn W, Gundlach H, Deus-Neumann B, Stockigt J (1985) Late enzymes of vindoline biosynthesis: acetyl-CoA:17-O-deacetylvindoline 17-O-acetyl- transferase. Plant Cell Rep 4:337–340

    Article  CAS  PubMed  Google Scholar 

  • Gantet P, Memelink J (2002) Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. Trends Pharmacol Sci 23:563–569

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Goddijn OJ, Lohman FP, de Kam RJ, Schilperoort RA, Hoge JH (1994) Nucleotide sequence of the tryptophan decarboxylase gene of Catharanthus roseus and expression of tdc-gusA gene fusions in Nicotiana tabacum. Mol Gen Genet 242(2):217–225

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 application to the subcellular localization of hydroxyl methylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep 28:1215–1234

    Article  CAS  PubMed  Google Scholar 

  • Guirimand G, Guihur A, Ginis O, Poutrain P, Héricourt F, Oudin A, Lanoue A, St-Pierre B, Burlat V, Courdavault V (2011) The subcellular organization of strictosidine biosynthesis in Catharanthus roseus epidermis highlights several trans-tonoplast translocations of intermediate metabolites. FEBS Lett 278:749–763

    Article  CAS  Google Scholar 

  • Guirimand G, Guihur A, Phillips MA, Oudin A, Glévarec G, Mahroug S, Melin C, Papon N, Clastre M, Giglioli-Guivarc’h N, St-Pierre B, Rodríguez- Concepción M, Burlat V, Courdavault V (2012) Triple subcellular targeting of isopentenyl diphosphate isomerases encoded by a single gene. Plant Signal Behav 7(11):1495–1497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta P, Goel R, Pathak S, Srivastava A, Singh SP, Sangwan RS, Asif MH, Trivedi PK (2013) De Novo assembly, functional annotation and comparative analysis of Withania somnifera leaf and root transcriptomes to identify putative genes involved in the withanolides biosynthesis. PLoS One 8(5):e62714, PMCID: PMC3648579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallahan DL, West JM, Wallsgrove RM, Smiley DW, Dawson GW, Pickett JA, Hamilton JG (1995) Purification and characterization of an acyclic monoterpene primary alcohol: NADP+ oxidoreductase from catmint (Nepeta racemosa). Arch Biochem Biophys 318:105–112

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Hong SB, Hughes EH, Shanks JV, San K-Y, Gibson SI (2003) Role of the non-mevalonate pathway in indole alkaloid production by Catharanthus roseus hairy roots. Biotechnol Prog 19(3):1105–1108 (PMID: 12790690)

    Google Scholar 

  • Hsiao YY, Jeng MF, Tsai WC, Chuang YC, Li CY, Wu TS, Kuoh CS, Chen WH, Chen HH (2008) A novel homodimeric geranyl diphosphate synthase from the orchid Phalaenopsis bellina lacking a DD(X) 2–4 motif. Plant J 55:719–733

    Article  CAS  PubMed  Google Scholar 

  • Hughes EH, Hong SB, Gibson SI, Shanks JV, San KY (2004) Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine. Metab Eng 6:268–276

    Article  CAS  PubMed  Google Scholar 

  • Ikeda H, Esaki N, Nakai S, Hashimoto K, Uesato S, Soda K, Fujita T (1991) Acyclic monoterpene primary alcohol: NADP+ oxidoreductase of Rauwolfia serpentine cells: the key enzyme in biosynthesis of monoterpene alcohols. J Biochem 109:341–347

    CAS  PubMed  Google Scholar 

  • Irmler S, Schroder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strack D, Matern U, Schroder 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

    Article  CAS  PubMed  Google Scholar 

  • Istvan ES, Deisenhofer J (2000) The structure of the catalytic portion of human HMG-CoA reductase. Biochim Biophys Acta 1529:9–18

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kruczynsky A, Hill BT (2001) Vinflunine, the latest Vinca alkaloid in clinical development. A review of its preclinical anticancer properties. Crit Rev Oncol Hematol 40:159–173

    Article  Google Scholar 

  • Kutchan TM (2005) A role for intra- and intercellular translocation in natural product biosynthesis. Curr Opin Plant Biol 8:292–300

    Article  CAS  PubMed  Google Scholar 

  • Kutchan TM (1998) Molecular genetics of plant alkaloid biosynthesis. In The Alkaloids. (Cordell G ed.) San Diego: Academic Press 50: 257–316

    Google Scholar 

  • 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(8):2858–2882

    Article  CAS  PubMed  Google Scholar 

  • Kuzuyama T, Takagi M, Takahashi S, Seto H (2000) Cloning and characterization of 1-deoxy-D-xylulose 5-phosphate synthase from Streptomyces sp. strain CL190, which uses both the mevalonate and non mevalonate pathways for isopentenyl diphosphate biosynthesis. J Bacteriol 182:891–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laflamme P, St-Pierre B, De Luca V (2001) Molecular and biochemical analysis of a Madagascar periwinkle rootspecific minovincinine-19- hydroxy-O-acetyltransferase. Plant Physiol 125:189–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Learned RM, Connolly EL (1997) Light modulates the spatial patterns of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene expression in Arabidopsis thaliana. Plant J 11:499–511

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Poulter CD (2006) Escherichia coli type I isopentenyl diphosphate isomerase: structural and catalytic roles for divalent metals. J Am Chem Soc 128(35):11545–11550

    Article  CAS  PubMed  Google Scholar 

  • Lee M, Martin MN, Hudson AO, Lee J, Muhitch MJ, Leustek T (2005) Methionine and threonine synthesis are limited by homoserine availability and not the activity of homoserine kinase in Arabidopsis thaliana. Plant J 41:685–696

    Article  CAS  PubMed  Google Scholar 

  • Levac D, Murata J, Kim WS, De Luca V (2008) Application of carborundum abrasion for investigating leaf epidermis: Molecular cloning of Catharanthus roseus 16-hydroxytabersonine-16-O-methyltransferase. Plant J 53: 225–236

    Google Scholar 

  • Li QR, Di Fiore S, Fischer R, Wang M (2003) Expression of tryptophan decarboxylase in chloroplasts of transgenic tobacco plants. Bot Bull Acad Sinica 44:193–198

    CAS  Google Scholar 

  • Lichtenthaler HK, Rohmer M, Schwender J (1997) Two independent biochemical pathways for isopentenyl diphosphate (IPP) and isoprenoid biosynthesis in higher plants. Physiol Plant 101:643–652

    Article  CAS  Google Scholar 

  • Lois LM, Rodríguez-Concepcion M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J 22:503–513

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Loyola-Vargas VM, Mendiz MZ, Miriam MG, De L, Mirinda-Ham M (1992) Serpentine accumulation during greening in normal and tumor tissues of Catharanthus roseus. Plant Physiol 140:213–217

    Article  CAS  Google Scholar 

  • Lu H, Gorman E, McKnight TD (2005) Molecular characterisation of two anthranilate synthase alpha subunit genes in Camptotheca acuminata. Planta 221:352–360

    Article  CAS  PubMed  Google Scholar 

  • Luijendijk T (1995) Strictosidine glucosidase in indole alkaloid producing plants; characteristics and physiological implications. PhD thesis, Leiden University, The Netherlands

    Google Scholar 

  • Luijendijk T, Stevens LH, Verpoorte R (1998) Purification and characterization of strictosidine b-D-glucosidase from Catharanthus roseus cell suspension cultures. Plant Physiol Biochem 36:419–425

    Article  CAS  Google Scholar 

  • Madyastha KM, Coscia CJ (1979) Detergent-solubilized NADPH-cytochrome c (P450) reductase from the higher plant, Catharanthus roseus. J Biol Chem 254:2419–2427

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Maldonado-Mendoza IE, Vincent RM, Nessler CL (1997) Molecular characterization of three differentially expressed members of the Camptotheca acuminata 3-hydroxy-3-methylglutaryl CoA reductase (HMGR) gene family. Plant Mol Biol 34:781–790

    Article  CAS  PubMed  Google Scholar 

  • Matthews PD, Wurtzel ET (2000) Metabolic engineering of carotenoid accumulation in Escherichia coli by modulation of the isoprenoid precursor pool with expression of deoxyxylulose phosphate synthase. Appl Microbiol Biotechnol 53:396–400

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Meehan TD, Coscia CJ (1973) Hydroxylation of geraniol and nerol by a monooxygenase from Vinca rosea. Biochem Biophys Res Commun 53:1043–1048

    Google Scholar 

  • Meijer AH, Verpoorte R, Hoge JHC (1993) Regulation of enzymes and genes involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J Plant Res 3:145–164

    Google Scholar 

  • Memelink J, Verpoorte R, Kijne JW (2001) ORC anisation of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219

    Article  CAS  PubMed  Google Scholar 

  • Misra N, Gupta AK (2006) Effect of salinity and different nitrogen sources on the activity of antioxidant enzymes and indole alkaloid content in Catharanthus roseus seedlings. J Plant Physiol 163:11–18

    Article  CAS  PubMed  Google Scholar 

  • Misra N, Luthra R, Kumar S (2006) Bioconversion of Ajmalicine to Serpentine in Catharanthus roseus roots. J Plant Sci 1:340–347

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Morant M, Bak S, Moller BL, Werck-Reichhart D (2003) Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr Opin Biotechnol 14:151–162

    Article  CAS  PubMed  Google Scholar 

  • Moreno PRH, Poulsen C, Heijden R, Verpoorte R (1996) Effects of elicitation on different metabolic pathways in Catharanthus roseus (L.) G. Don cell suspension cultures. Enzyme Microb Technol 18:99–107

    Article  CAS  Google Scholar 

  • Moreno PRH, Van der Heijden R, Verpoorte R (1993) Effect of terpenoid precursor feeding and elicitation of formation of indole alkaloids in cell suspension cultures of Catharanthus roseus. Plant Cell Rep 12:702–705

    Google Scholar 

  • Moreno-Valenzuela OA, Minero-Garcia Y, Chan W, Mayer-Geraldo E, Carbajal E, Loyola-Vargas VM (2003) Increase in the indole alkaloid production and its excretion into culture medium by calcium antagonistic in Catharanthus roseus hairy roots. Biotechnol Lett 25:1345–1349

    Article  CAS  PubMed  Google Scholar 

  • Morgan JA, Shanks JV (1999) Inhibitor studies of tabersonine metabolism in C. roseus hairy roots. Phytochemistry 51:61–68

    Article  CAS  PubMed  Google Scholar 

  • Morgan JA, Shanks JV (2000) Determination of metabolic rate-limitations by precursor feeding in Catharanthus roseus hairy root cultures. J Biotechnol 79:137–145

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee A, Basu S, Sarkar N, Ghosh A (2001) Advances in cancer therapy with plant based natural products. Curr Med Chem 8:1467–1486

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20:524–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nejat N, Vadamalai G, Dickinson M (2012) Expression patterns of genes involved in the defense and stress response of Spiroplasma citri infected Madagascar Periwinkle Catharanthus roseus. Int J Mol Sci 13:2301–2313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niyogi KK, Fink GR (1992) Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell 4(6):721–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogura K, Koyama T (1998) Enzymatic aspects of isoprenoid chain elongation. Chem Rev 98:1263–1276

    Article  CAS  PubMed  Google Scholar 

  • Osman MEH, Soad SE, Abo El-Soud K, Hasan AM (2008) Response of Catharanthus roseus shoots to salinity and drought in relation to vincristrine alkaloid content. Asian J Plant Sci 6:1223–1228

    Google Scholar 

  • Oudin A, Courtois M, Rideau M, Clastre M (2007) The iridoid pathway in Catharanthus roseus alkaloid biosynthesis. Phytochem Rev 6:259–276

    Article  CAS  Google Scholar 

  • Page JE, Hause G, Raschke M, Gao W, Schmidt J, Zenk MH, Kutchan TM (2004) Functional analysis of the final steps of the 1-deoxy-D-xylulose (DXP) pathway to isoprenoids in plants using virus-induced gene silencing. Plant Physiol 134:1401–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 pathway in Catharanthus roseus suspension cells. Planta Med 71:572–574

    Article  CAS  PubMed  Google Scholar 

  • Pasquali G (1994) Regulation of the terpenoid indole alkaloid biosynthetic gene strictosidine synthase from Catharanthus roseus. PhD thesis, Leiden University

    Google Scholar 

  • Peebles CA, Hughes EH, Shanks JV, San KY (2009) Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time. Metab Eng 11:76–86

    Article  CAS  PubMed  Google Scholar 

  • Phillips MA, D’Auria JC, Gershenzon J, Pichersky E (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 20:677–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Poulsen C, Bongaerts R, Verpoorte R (1993) Purification and characterization of anthranilate synthase from Catharanthus roseus. Eur J Biochem 212:431–440

    Article  CAS  PubMed  Google Scholar 

  • Powers R, Kurz WGW, De Luca V (1990) Purification and characterization of acetyl-CoA: deacetylvindoline 4-O-acetyltransferase from Catharanthus roseus. Arch Biochem Biophys 279:370–376

    Article  Google Scholar 

  • Proteau PJ (2004) 1-Deoxy-D-xylulose 5-phosphate reductoisomerase: an overview. Bioorg Chem 32:483–493

    Article  CAS  PubMed  Google Scholar 

  • Querol J, Campos N, Imperial S, Boronat A, Rodríguez-Concepción M (2002) Functional analysis of the Arabidopsis thaliana GCPE protein involved in plastid isoprenoid biosynthesis. FEBS Lett 514:343–346

    Article  CAS  PubMed  Google Scholar 

  • Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91–102

    Article  CAS  PubMed  Google Scholar 

  • Rai A, Smita SS, Singh AK, Shanker K, Nagegowda DA (2013) Heteromeric and homomeric geranyl diphosphate synthases from Catharanthus roseus and their role in monoterpene indole alkaloid biosynthesis. Mol Plant 6(5):1531–1549

    Article  CAS  PubMed  Google Scholar 

  • Rai V, Tandon PK, Khatoon S (2014) Effect of chromium on antioxidant potential of Catharanthus roseus varieties and production of their anticancer alkaloids: vincristine and vinblastine. Biomed Res Int 2014, Article ID 934182

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Richard SB, Ferrer JL, Bowman ME, Lillo AM, Tetzlaff CN, Cane DE, Noel JP (2002) Structure and mechanism of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase—an enzyme in the mevalonate-independent isoprenoid biosynthetic pathway. J Biol Chem 277:8667–8672

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Concepcion M, Fores O, Martinez-Garcia JF, Gonzalez V, Phillips MA, Ferrer A, Boronat A (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16:144–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohdich F, Wungsintaweekul J, Eisenreich W, Richter G, Schuhr CA, Hecht S, Zenk MH, Bacher A (2000) Biosynthesis of terpenoids: 4-diphosphocytidyl-2-C-methyl-D-erythritol synthase of Arabidopsis thaliana. Proc Natl Acad Sci U S A 97:6451–6456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosco A, Pauli HH, Priesner W, Kutchan TM (1997) Cloning and heterologous expression of NADPH-cytochrome P450 reductases from the Papaveraceae. Arch Biochem Biophys 348:369–377

    Article  CAS  PubMed  Google Scholar 

  • Ross IA (2003) Catharanthus roseus. Medicinal plants of the World, vol 1. Humana Press, Totowa, pp 175–196

    Google Scholar 

  • Sanchez-Iturbe P, Galaz-Avalos RM, Loyola-Vargas VM (2005) Determination and partial purification of a monoterpene cyclase from Catharanthus roseus hairy roots. Phyton 55–69

    Google Scholar 

  • Scheel D (1998) Resistance response physiology and signal transduction. Curr Opin Plant Biol 1(4):305–310

    Article  CAS  PubMed  Google Scholar 

  • Schiel O, Witte L, Berlin J (1987) Geraniol-10-hydroxylase activity and its relation to monoterpene indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus. Z Naturforsch 42:1075–1081

    CAS  Google Scholar 

  • Schmeller T, Wink M (1998) Utilization of alkaloids in modern medicine. In: Roberts MF, Wink M (eds) Alkaloids: biochemistry, ecology and medicinal applications. Plenum, New York, pp 435–459

    Chapter  Google Scholar 

  • Schmidt A, Gershenzon J (2008) Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69:49–57

    Article  CAS  PubMed  Google Scholar 

  • Schmidt A, Wachtler B, Temp U, Krekling T, Seguin A, Gershenzon J (2010) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Picea abies. Plant Physiol 152:639–655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroder G, Unterbusch E, Kaltenbach M, Schmidt J, Strack D, De Luca V, Schroder J, (1999) Light induced cytochrome P450-dependent enzyme in indole alkaloid biosynthesis: tabersonine 16-hydroxylase. FEBS Lett 458: 97–102

    Google Scholar 

  • Schulte AE, Vander Heijden R, Verpoorte R (2000) Purification and characterization of mevalonate kinase from suspension-cultured cells of Catharanthus roseus (L.) G. Don. Arch Biochem Biophys 378(2):287–298

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Seigler DS (1998) Plants with saponins and cardiac glycosides. www.lifwe.vinc.edu/plantbio/363/saponinslides

  • Shanks JV, Bhadra R (1997) Characteristics of selected hairy root lines of Catharanthus roseus. In: Doran PM (ed) Hairy roots. Harwood, Reading, pp 51–63

    Google Scholar 

  • Sharma NK, Pan JJ, Poulter CD (2010) Type II isopentenyl diphosphate isomerase: probing the mechanism with alkyne/allene diphosphate substrate analogues. Biochemistry 49(29):6228–6233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shet MS, Sathasivan K, Arlotto MA, Mehdy MC, Estabrook RW (1993) Purification, characterization, and cDNA cloning of an NADPH-cytochrome P450 reductase from mung bean. Proc Natl Acad Sci U S A 90:2890–2894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sottomayor M, Lopez-Serrano M, Di Cosmo 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

    Article  CAS  PubMed  Google Scholar 

  • Stevens LH (1994) Formation and conversion of strictosidine in the biosynthesis of monoterpenoid indole and quinoline alkaloids. PhD thesis, Leiden University, The Netherlands

    Google Scholar 

  • 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

    Article  Google Scholar 

  • St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseusalkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:887–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tapsell LC, Hemphill I, Cobiac L (2006) Health benefits of herbs and spices: the past, the present, the future. Med J Aust 185:4–24

    Google Scholar 

  • Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0143, PMCID: PMC3268506

    Article  PubMed  PubMed Central  Google Scholar 

  • Treimer JF, Zenk MH (1979) Purification and properties of strictosidine synthase, the key enzyme in indole alkaloid formation. Eur J Biochem 101:225–233

    Article  CAS  PubMed  Google Scholar 

  • Uesato S, Matsuda S, Iida A, Inouye H, Zenk MH (1984) Intermediacy of 10-hydroxygeraniol, 10-hydroxynerol and iridodial in the biosynthesis of ajmaline and vomilenine in Rauwolfia serpentina suspension cultures. Chem Pharm Bull 32:3764–3767

    Article  CAS  Google Scholar 

  • Van der Heijden R, De Boer-Hup V, Verpoorte R, Duine JA (1994) Enzymes involved in the metabolism of 3-hydroxy-3- methylglutaryl coenzyme A in Catharanthus roseus. Plant Cell Tiss Org Cult 38:345–349

    Article  Google Scholar 

  • Van der Heijden R, Jacobs DI, Snoeijer W, Hallared D, Verpoorte R (2004) The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11:607–628

    Article  Google Scholar 

  • Vander Fits L, Memelink J (2000) ORCA3, a jasmonate responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297

    Article  CAS  Google Scholar 

  • Vander 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

    Article  CAS  Google Scholar 

  • Vazquez-Flota FA, De Luca V (1998) Developmental and light regulation of desacetoxyvindoline 4-hydroxylase in Catharanthus roseus (L.) G. Don. Plant Physiol 117(4):1351–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vazquez-Flota F, De Carolis E, 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

    Article  CAS  PubMed  Google Scholar 

  • 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. Biochim Biophys Acta 1517:159–163

    Article  CAS  PubMed  Google Scholar 

  • Verpoorte R, Van der Heijden R, Memelink J (2000) Engineering the plant cell factory for secondary metabolite production. Transgenic Res 9:323–343

    Article  CAS  PubMed  Google Scholar 

  • Verpoorte R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1:13–25

    Article  CAS  Google Scholar 

  • 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 Press, San Diego, pp 221–299

    Google Scholar 

  • Vollack KU, Bach TJ (1996) Cloning of a cDNA encoding cytosolic acetoacetyl-coenzyme A thiolase from radish by functional expression in Saccharomyces cerevisiae. Plant Physiol 111:1097–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang G, Dixon RA (2009) Heterodimeric geranyl (geranyl) diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis. Proc Natl Acad Sci U S A 106:9914–9919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang DH, Du F, Liu HY, Liang ZS (2010) Drought stress increases iridoid glycosides biosynthesis in the roots of Scrophularia ningpoensis seedlings. J Med Plants Res 4(24):2691–2699

    Article  CAS  Google Scholar 

  • Wang Q, Xing S, Pan Q, Yuan F, Zhao J, Tian Y, Chen Y, Wang G, Tang K (2012) Development of efficient Catharanthus roseus regeneration and transformation system using Agrobacterium tumefaciens and hypocotyls as explants. BMC Biotechnol 12:34–46

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Wolff M, Seemann M, Bui BTS, Frapart Y, Tritsch D, Estrabot AG, Rodriguez-Concepcion M, Boronat A, Marquet A, Rohmer M (2003) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a 4Fe-4S protein. FEBS Lett 541:115–120

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Zhao J, Zhu W, Hu Q (2001b) Selection of fungal elicitors to increase indole alkaloid accumulation in Catharanthus roseus suspension cell culture. Enzyme Microb Technol 28(7):666–672

    Google Scholar 

  • Zheng Z, Wu M (2004) Cadmium treatment enhances the production of alkaloid secondary metabolites in Catharanthus roseus. Plant Sci 166:507–514

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shabnam Akhtar .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Akhtar, S., Ahmad, J., Ahmad, A. (2017). Molecular Network of Monoterpene Indole Alkaloids (MIAs) Signaling in Plants with Reference to Catharanthus roseus (L.) G. Don. In: Sarwat, M., Ahmad, A., Abdin, M., Ibrahim, M. (eds) Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-42183-4_2

Download citation

Publish with us

Policies and ethics