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Plant Growth Regulation

, Volume 68, Issue 2, pp 111–127 | Cite as

Catharanthus roseus alkaloids: application of biotechnology for improving yield

  • Abdul MujibEmail author
  • Abdul Ilah
  • Junaid Aslam
  • Samar Fatima
  • Zahid Hameed Siddiqui
  • Mehpara Maqsood
Review paper

Abstract

Catharanthus roseus (L.) G. Don. is a well known medicinal plant. It produces several phyto-compounds many of which show anticancerous properties. The yields of these compounds are however, very low. In this present article, the current development of secondary metabolite synthesis in C. roseus involving biotechnology has been reviewed keeping in mind the various basic factors that influence yield. The importance of cell culture, the role of culturing conditions and other approaches aiming at higher production of alkaloids have been discussed. The genes encoding important enzymes, proteomics, expressed sequence tag and transcription factors in relation to alkaloid yield have also been summarized in order to understand the regulatory mechanisms of C. roseus.

Keywords

Catharanthus roseus Indole alkaloids Biotechnology In vitro culture conditions 

Abbreviations

2, 4-D

2, 4-Dichlorophenoxyaceticacid

BA/BAP

6-Benzyladenine

DMSO

Dimethylsulfoxide

GA3

Gibberellic acid

HPLC

High performance liquid chromatography

KN

Kinetin

MS

Murashige and Skoog

NAA

α-Naphthalene acetic acid

PGR

Plant growth regulator

SE

Somatic embryos

TDC

Tryptophan decarboxylase

SSS

Strictosidine synthetase

Notes

Acknowledgments

The first author is highly thankful to Central Council for Research in Unani Medicine (CCRUM) and Department of Botany, Hamdard University (Jamia Hamdard), New Delhi, for providing financial assistance and other facilities. The help rendered by present and past research students is also acknowledged. We wish to thank anonymous reviewers for their comments on manuscript and critical reading.

References

  1. Akcam E, Yurekli AK (1995) Effect of different nutrient media and explant sources on callus induction of Catharanthus roseus L.(G). Don plants. Turk J Bot 19:569–572Google Scholar
  2. Akimoto C, Aoyagi H, Tanaka H (1999) Endogenous elicitor-like effect of alginate on physiological activities of plant cells. Appl Microbiol Biotechnol 52:429–436Google Scholar
  3. Amini A, Glévarec G, Andreu F, Rideau M, Crèche J (2009) Low levels of gibberellic acid control the biosynthesis of ajmalicine in Catharanthus roseus cell suspension cultures. Planta Med 75:187–191PubMedGoogle Scholar
  4. Aoyagi H, Akimoto-Tomiyama C, Tanaka H (2006) Preparation of mixed alginate elicitors with high activity for the efficient production of 5′-phosphodiesterase by Catharanthus roseus cells. Biotechnol Lett 28:1567–1571PubMedGoogle Scholar
  5. Bachiri Y, Gazeau C, Hansz J, Morisset C, Dereuddre J (1995) Successful cryopreservation of suspension cells by encapsulation dehydration. Plant Cell Tissue Organ Cult 43:241–248Google Scholar
  6. Bailey CM, Nicholson H (1990) Optimal temperature control for structured model of plant cell culture. Biotechnol Bioeng 35:252–258PubMedGoogle Scholar
  7. Batra J, Dutta A, Singh D, Kumar S, Sen J (2004) Growth and terpenoid indole alkaloid production in Catharanthus roseus hairy root clones in relation to left- and right-termini-linked Ri T-DNA gene integration. Plant Cell Rep 23:148–154PubMedGoogle Scholar
  8. Begum F, Nageswara Rao SS, Rao K, Prameela Devi Y, Giri A, Giri CC (2009) Increased vincristine production from Agrobacterium tumefaciens C58 induced shooty teratomas of Catharanthus roseus G. Don. Nat Prod Res 23:973–981PubMedGoogle Scholar
  9. Benjamin BD, Siphahimalani AT, Helen MR (1990) Growth and alkaloid production of different cell lines of Catharanthus roseus (L). Don. Ind J Exp Biol 28:516–518Google Scholar
  10. Bergland T, Kalbin G, Strid A, Rydstrom J, Ohlsson AB (1996) UV-B and oxidative stress induced increase in nicotinamide and trigonelline and inhibition of defensive metabolism induction by poly(ADP-ribose) polymerase inhibitor in plant tissue. FEBS Lett 380:188–193Google Scholar
  11. Binder BY, Peebles CA, Shanks JV, San KY (2009) The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol Prog 25:861–865PubMedGoogle Scholar
  12. Campos-Tamayo F, Hernández-Domínguez E, Vázquez-Flota F (2008) Vindoline formation in shoot cultures of Catharanthus roseus is synchronously activated with morphogenesis through the last biosynthetic step. Ann Bot 102:409–415PubMedGoogle Scholar
  13. Carturan G, Dal Monte R, Pressi G, Secondin S, Verza P (1998) Production of valuable drugs from plant cells immobilized by hybrid Sol-Gel SiO2. J Sol Gel Sci Tech 13:273–276Google Scholar
  14. Chung IM, Hong SB, Peebles CA, Kim JA, San KY (2007) Effect of the engineered indole pathway on accumulation of phenolic compounds in Catharanthus roseus hairy roots. Biotechnol Prog 23:327–332PubMedGoogle Scholar
  15. Cloutier M, Bouchard-Marchand E, Perrier M, Jolicoeur MA (2008) Predictive nutritional model for plant cells and hairy roots. Biotechnol Prog 99:189–200Google Scholar
  16. Datta A, Srivastava PS (1997) Variation in vinblastine production by Catharanthus roseus during in vivo and in vitro differentiation. Phytochemistry 46:135–137Google Scholar
  17. 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 11:400–403Google Scholar
  18. Dutta A, Batra J, Pandey-Rai S, Singh D, Kumar S, Sen J (2005) Expression of terpenoid indole alkaloid biosynthetic pathway genes corresponds to accumulation of related alkaloids in Catharanthus roseus (L.) G. Don. Planta 220:376–383PubMedGoogle Scholar
  19. Dutta A, Sen J, Deswal R (2007) Down regulation of terpenoid indole alkaloid biosynthetic pathway by low temperature and cloning of a AP2 type C-repeat binding factor (CBF) from Catharanthus roseus (L). G. Don. Plant Cell Rep 26:1869–1878PubMedGoogle Scholar
  20. Ebel J, Scheel D (1997) Signals in host-parasite interactions. In: Carroll GC, Tudzynski P (eds) The mycota plant relationships, part A, vol V. Springer, Berlin, pp 85–105Google Scholar
  21. Favretto D, Piovan A, Filippini R, Caniato R (2001) Monitoring the production yields of vincristine and vinblastine in Catharanthus roseus from somatic embryogenesis. Semiquantitative determination by flow-injection electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 5:364–369Google Scholar
  22. Fiore CM, Trabace T, Sunseri F (1997) High frequency of plant regeneration in sunflower from cotyledons via somatic embryogenesis. Plant Cell Rep 16:295–298Google Scholar
  23. Garnier F, Carpin S, Label P, Creche J, Rideau M, Hamdi S (1996) Effect of cytokinin on alkaloid accumulation in periwinkle callus cultures transformed with a light inducible ipt gene. Plant Sci Limerick 120:47–55Google Scholar
  24. Giddings LA, Liscombe DK, Hamilton JP, Childs KL, Dellapenna D, Buell CR, O’Connor SE (2011) A stereoselective hydroxylation step of alkaloid biosynthesis by a unique cytochrome P450 in Catharanthus roseus. J Biol Chem 286:16751–16757PubMedGoogle Scholar
  25. Goddijn OJM, Pennings EJM, Helm PV, Schilperoort RA, Verpoorte R, Hoge JHC, Vander- Helm P (1995) Overexpression of a tryptophan decarboxylase cDNA in Catharanthus roseus crown gall calluses results in increased tryptamide levels but not in increased terpenoid indole alkaloid production. Trans Res 4:315–323Google Scholar
  26. Hernández-Domínguez E, Campos-Tamayo F, Carrillo-Pech M, Vázquez-Flota F (2006) Catharanthus roseus shoot cultures for the production of monoterpenoid indole alkaloids. Methods Mol Biol 318:349–355PubMedGoogle Scholar
  27. Hirata K, Horiuchi M, Asada M, Ando T, Miyamota K, Miura Y (1992) Stimulation of dimeric alkaloid production by near-ultraviolet light in multiple shoot cultures of Catharanthus roseus. Ferment Bioeng 74:222–225Google Scholar
  28. Hoopen HJG, Gulik T, Van WM, Schlatmann JE, Moreno PRH, Vinki JL, Heijnen JJ, Heijnen R, Verpoorte R, Ten Hoopen HJG, Gulik V (1994) Ajmalicine production by cell cultures of Catharanthus roseus: from shake flask to bioreactor. Plant Cell Tissue Organ Cult 38:85–91Google Scholar
  29. Ilah A, Mujib A, Aslam J, Fatima S, Abdin MZ (2009) Somatic embryogenesis and two embryo specific proteins (38 and 33 kD) in Catharanthus roseus L. (G.) Don. Biologia 64:299–304Google Scholar
  30. Jacobs DI, Gaspari M, van der Greef J, van der Heijden R, Verpoorte R (2005) Proteome analysis of the medicinal plant Catharanthus roseus. Planta 221:690–704PubMedGoogle Scholar
  31. Junaid A, Bhatt MA, Mujib A, Sharma MP (2006) Somatic embryo proliferation, maturation and germination in Catharanthus roseus. Plant Cell Tissue Organ Cult 84:325–332Google Scholar
  32. Junaid A, Mujib A, Sharma MP, Tang W (2007) Growth regulators affect primary and secondary somatic embryogenesis in Madagaskar periwinkle (Catharanthus roseus (L) G. Don) at morphological and biochemical levels. Plant Growth Regul 51:271–281Google Scholar
  33. Junaid A, Mujib A, Samar F, Sharma MP (2008) Cultural conditions affect somatic embryogenesis in Catharanthus roseus L (G.) Don. Plant Biotechnol Rep 2:179–189Google Scholar
  34. Junaid A, Mujib A, Sharma MP (2009) Screening of vincristine yield in ex vitro and in vitro somatic embryos derived plantlets of Catharanthus roseus L. (G) Don. Sci Hortic 119:325–329Google Scholar
  35. Kargi F, Ganapathi B (1991) Effects of precursor stimulating agents on formation of indole formation by C. roseus in a biofilm reactor. Enzyme Microb Technol 13:643–647Google Scholar
  36. Kargi F, Potts P (1991) Effect of various stress factors on indole alkaloid formation by C. roseus (periwinkle) cells. Enzyme Microb Technol 13:760–763Google Scholar
  37. Kevei E, Nagy F (2003) Phytochrome controlled signaling cascades in higher plants. Physiol Planta 117:305–313Google Scholar
  38. Kim S, Song NH, Jung KH, Kwak SS, Liu JR (1994) High frequency plant regeneration from anther-derived cell suspension cultures via somatic embryogenesis in Catharanthus roseus. Plant Cell Rep 13:319–322Google Scholar
  39. Kuboyama T, Yokoshima S, Tokuyama H, Fukuyama T (2004) Stereocontrolled total synthesis of (+) vincristine. PNAS 101:11966–11970PubMedGoogle Scholar
  40. Kulkarni RN, Baskaran K (2008) Inheritance of pollen-less anthers and “thrum” and “pin” flowers in periwinkle. J Hered 99:426–431PubMedGoogle Scholar
  41. Lee CW, Shuler ML (2000) The effect of inoculum density and conditioned medium on the production of ajmalicine and catharanthine from immobilized Catharanthus roseus cells. Biotechnol Bioeng 67:61–71PubMedGoogle Scholar
  42. Lee-Parsons CW, Ertürk S, Tengtrakool J (2004) Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnol Lett 26:1595–1599PubMedGoogle Scholar
  43. 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 53:225–236PubMedGoogle Scholar
  44. Liscombe DK, Usera AR, O’Connor SE (2010) Homolog of tocopherol C methyltransferases catalyzes N methylation in anticancer alkaloid biosynthesis. Proc Natl Acad Sci USA 107:18793–18798PubMedGoogle Scholar
  45. Liu D, Andreau F, Merillon JM, Chenieux JC, Rideau M (1990) Stimulation de l’accumulation alcaloidique par la zeatine dans une suspension cellulaire de Catharanthus roseus. G. Don autotrophe aux cytokinines. Colloq De I’INRA 51:291–293Google Scholar
  46. Loyola-Vargas VM, Mende-Zeel M, Monforte-Gonzales M, Miranda-Ham ML (1992) Serpentine accumulation during greening in normal and tumor tissues of Catharanthus roseus. J Plant Physiol 140:213–217Google Scholar
  47. Magnotta M, Murata J, Chen J, De Luca V (2006) Identification of a low vindoline accumulating cultivar of Catharanthus roseus (L.) G. Don by alkaloid and enzymatic profiling. Phytochemistry 67:1758–1764PubMedGoogle Scholar
  48. Magnotta M, Murata J, Chen J, De Luca V (2007) Expression of deacetylvindoline-4-O-acetyltransferase in Catharanthus roseus hairy roots. Phytochemistry 68:1922–1931PubMedGoogle Scholar
  49. Mannonen L, Toivonen L, Kauppinen VC (1990) Effects of long term preservation on growth and productivity of Panax ginseng and Catharanthus roseus cell culture. Plant Cell Rep 9:173–177Google Scholar
  50. Marfori EC, Alejar AA (1993) Alkaloid yield variation in callus cultures derived from different plant parts of the white and rosy purple periwinkle, Catharanthus roseus (L). Don. Philipp J Biotechnol 4:1–8Google Scholar
  51. Meijer AH, Verpoorte R, Hoge JHC (1993) Regulation of enzymes and genes involved in terpenoids indole alkaloid biosynthesis in Catharanthus roseus. J Plant Res 3:145–164Google Scholar
  52. Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219PubMedGoogle Scholar
  53. Menke FLH, Parchmann S, Mueller MJ, Kijne JW, Memelink J (1999) Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. Plant Physiol 119:1289–1296PubMedGoogle Scholar
  54. Montiel G, Breton C, Thiersault M, Burlat V, Jay-Allemand C, Gantet P (2007) Transcription factor Agamous-like 12 from Arabidopsis promotes tissue-like organization and alkaloid biosynthesis in Catharanthus roseus suspension cells. Metab Eng 9:125–132PubMedGoogle Scholar
  55. Moreno PRH, Van der Heijden R, Verpoorte R (1993) Effect of terpenoid precursor feeding and elicitation on formation of indole alkaloids in cell suspension cultures of Catharanthus roseus. Plant Cell Rep 12:702–705Google Scholar
  56. Moreno PRH, Van der Heijden R, Verpoorte R (1995) Cell and tissue cultures of Catharanthus roseus; a literature survey II. Updating from 1988–1993. Plant Cell Tissue Organ Cult 42:1–25Google Scholar
  57. Moreno-Valenzuela OA, Monforte-Gonzalez M, Munoz-Sanchex JA, Mendez-Zeel M, Loyola Vargas VM, Hernandez-Sotomayor MT (1999) Effect of macerozyme on secondary metabolism plant product production and phospholipase C activity in Catharanthus roseus hairy roots. J Plant Physiol 155:447–452Google Scholar
  58. Moreno-Valenzuela OA, Minero-García Y, Chan W, Mayer-Geraldo E, Carbajal E, Loyola-Vargas VM (2003) Increase in the indole alkaloid production and its excretion into the culture medium by calcium antagonists in Catharanthus roseus hairy roots. Biotechnol Lett 25:1345–1349PubMedGoogle Scholar
  59. Morgan JA, Shanks JV (2000) Effects of precursor feeding on alkaloid production in C. roseus hairy root cultures. J Biotechnol 79:137–145PubMedGoogle Scholar
  60. Morgan JA, Barney CS, Penn AH, Shanks JV (2000) Effects of buffered media upon growth and alkaloid production of Catharanthus roseus hairy roots. Appl Microbiol Biotechnol 53:262–265PubMedGoogle Scholar
  61. Mujib A, Samaj J (2006) Somatic embryogenesis. Springer, BerlinGoogle Scholar
  62. Mujib A, Das S, Dey S, Bhattacharya B (1995) Influence of agitation in in vitro cultivation of Catharanthus roseus (L). G. Don multiple shoot. Phytomorphology 45:239–245Google Scholar
  63. Murata J, Bienzle D, Brandle JE, Sensen CW, De Luca V (2006) Expressed sequence tags from Madagascar periwinkle (Catharanthus roseus). FEBS Lett 580:4501–4507PubMedGoogle Scholar
  64. Mustafa NR, Kim HK, Choi YH, Erkelens C, Lefeber AW, Spijksma G, van der Heijden R, Verpoorte R (2009) Biosynthesis of salicylic acid in fungus elicited Catharanthus roseus cells. Phytochemistry 70:532–539PubMedGoogle Scholar
  65. Nato A, Fresnau C, Moursalinowa N, De Buyser J, Lavergne D, Henry Y (2000) Expression of auxin and light regulated arrestin like proteins, G proteins and nucleoside diphosphate kinase during development of wheat somatic embryos. Plant Physiol Biochem 38:483–490Google Scholar
  66. Naudascher F, Doireau P, Thiersault M, Guillot A, Merillon JM, Chenieux JC (1990) Influence de la disponibilite en precurseurs I’accumulation alcaloidique dans les cellules de Catharanthus roseus Cultivees in vitro comparison entre suspensions en phase de croissance et suspensions en phase stationaire. Les Colloq. de I’INRA 51:307–309Google Scholar
  67. Ning LL, Han J, Zhang XY, Guo HZ, Bi KS, Guo DA (2004) Biotransformation of triptolide and triptonide by cell suspension cultures of Catharanthus roseus. J Asian Nat Prod Res 6:93–97PubMedGoogle Scholar
  68. Nuutila AM (1994) Bioreactor studies on hairy root cultures of Catharanthus roseus. Composition of three bioreactor types. Biotechnol Tech 8:61–66Google Scholar
  69. Palazón J, Cusidó RM, Gonzalo J, Bonill M, Morales C, Piñol MT (1998) Relation between the amount of rol C gene product and indole alkaloid accumulation in Catharanthus roseus transformed root cultures. J Plant Physiol 153:712–771Google Scholar
  70. Paynee GF, Paynee NN, Shuler ML (1988) Bioreactor considerations for secondary metabolite production from plant cell tissue culture; indole alkaloid from Catharanthus roseus. Biotechnol Bioeng 31:905–912Google Scholar
  71. Peebles CA, Gibson SI, Shanks JV, San KY (2007) Characterization of an ethanol-inducible promoter system in Catharanthus roseus hairy roots. Biotechnol Prog 23:1258–1260PubMedGoogle Scholar
  72. Pietrosiuk A, Furmanowa M, Lata B (2007) Catharanthus roseus: micropropagation and in vitro techniques. Phytochem Rev 6:459–473Google Scholar
  73. Pomahacová B, Dusek J, Dusková J, Yazaki K, Roytrakul S, Verpoorte R (2009) Improved accumulation of ajmalicine and tetrahydroalstonine in Catharanthus cells expressing an ABC transporter. J Plant Physiol 166:1405–1412PubMedGoogle Scholar
  74. Ramani S, Chelliah J (2007) UV-B-induced signaling events leading to enhanced-production of catharanthine in Catharanthus roseus cell suspension cultures. BMC Plant Biol 7(7):61PubMedGoogle Scholar
  75. Ramani S, Jayabaskaran C (2008) Enhanced catharanthine and vindoline production in suspension cultures of Catharanthus roseus by ultraviolet-B light. J Mol Signal 25(3):9Google Scholar
  76. 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 14:442–449PubMedGoogle Scholar
  77. Ruiz-May E, Galaz-Avalos RM, Loyola-Vargas VM (2009) Differential secretion and accumulation of terpene indole alkaloids in hairy roots of Catharanthus roseus treated with methyl jasmonate. Mol Biotechnol 41:278–285PubMedGoogle Scholar
  78. Runguphan W, O’Connor SE (2009) Metabolic reprogramming of periwinkle plant culture. Nat Chem Biol 5:151–153PubMedGoogle Scholar
  79. Runguphan W, Qu X, O’Connor SE (2010) Intregration carbon-halogen bond formation into medicinal plant metabolism. Nature 468:461–464PubMedGoogle Scholar
  80. Saenz L, Santamaria JM, Villanueva MA, Loyola-Vargas VM, Ovopera C (1993) Change in alkaloid content of C. roseus as a result of water stress and treatment with abscissic acid. J Plant Physiol 142:244–247Google Scholar
  81. Sakano K, Kiyota S, Yazaki Y (1997) Acidification and alkalinization of culture medium by Catharanthus roseus cells is anoxic production of lactate a cause of cytoplasmic acidification? Plant Cell Physiol 38:1053–1059Google Scholar
  82. Samar F, Mujib A, Nasim SA, Siddiqui ZH (2009) Cryopreservation of embryogenic cell suspensions of Catharanthus roseus L. (G) Don. Plant Cell Tissue Organ Cult 98:1–9Google Scholar
  83. Satdive RK, Fulzele DP, Eapen S (2003) Studies on production of ajmalicine in shake flasks by multiple shoot cultures of Catharanthus roseus. Biotechnol Prog 19:1071–1075PubMedGoogle Scholar
  84. Schlatmann JE, Ten Hoopen HJG, Heijnen JJ (1992) Optimization of the medium composition for alkaloid production by Catharanthus roseus using statistical experimental designs. Med Fac Landbouw Univ Gent 57:1567–1569Google Scholar
  85. Schlatmann JE, Moreno PRH, Ten Hoopen HJG, Verpoorte R, Heijnen JJ (1994) Effect of oxygen and nutrient limitation on ajmalicine production and related enzyme activities in high density cultures of Catharanthus roseus. Biotechnol Bioeng 44:461–468PubMedGoogle Scholar
  86. Seitz HU, Eilert U, De Luca V, Kurz WGW (1989) Elicitor mediated induction of phenylalanine ammonia lyase and tryptophan decarboxylase; accumulation of phenols and indole alkaloids in cell suspension cultures of Catharanthus roseus. Plant Cell Tissue Organ Cult 18:71–78Google Scholar
  87. Shimoda K, Kwon S, Utsuki A, Ohiwa S, Katsuragi H, Yonemoto N, Hamada H, Hamada H (2007) Glycosylation of capsaicin and 8-nordihydrocapsaicin by cultured cells of Catharanthus roseus. Phytochemistry 68:1391–1396PubMedGoogle Scholar
  88. Sun M, Zeng JJ (2005) A study on the hairy root culture and antitumor alkaloids production of Catharanthus roseus. Zhongguo Zhong Yao Za Zhi 30:741–743PubMedGoogle Scholar
  89. Thorpe TA (1995) In vitro embryogenesis in plants. Kluwer/Dordrecht, NetherlandsGoogle Scholar
  90. Toivonen L, Laakso S, Rosenqvist H (1992) The effect of temperature on growth, indole alkaloid accumulation and lipid composition Catharanthus roseus cell suspension cultures. Plant Cell Rep 11:390–394Google Scholar
  91. Torne JM, Moysset L, Santos M, Simon E (2001) Effects of light quality on somatic embryogenesis in Araujia sercifera. Physiol Plant 111:405–411PubMedGoogle Scholar
  92. Valluri JV (2009) Bioreactor production of secondary metabolites from cell cultures of periwinkle and sandalwood. Methods Mol Biol 547:325–335PubMedGoogle Scholar
  93. Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297PubMedGoogle Scholar
  94. Van der Heijden R, Verpoorte R, Ten Hoopen HJG (1989) Cell and tissue cultures of Catharanthus roseus (L). G. Don: a literature survey. Plant Cell Tissue Organ Cult 18:231–280Google Scholar
  95. Van der Heijden R, De Boer-Hlupa V, Verpoorte R, Duine JA (1994) Enzymes involved in the metabolism of 3-hydroxy-3-methylglutaryl coenzyme A in Catharanthus roseus. Plant Cell Tissue Organ Cult 38:345–349Google Scholar
  96. Van der Heijden R, Jacobs DT, Snoeijer W, Hallard D, Verpoorte R (2004) The Catharanthus alkaloids: pharamacognosy and biochemistry. Curr Med Chem 11:607–628Google Scholar
  97. Van Gulik WM, Ten Hoopen HJG, Heijnen JJ (1993) A structured model describing carbon and phosphate limited growth of Catharanthus roseus plant cell suspensions in batch and chemostat cultures. Biotechnol Bioeng 41:771–780PubMedGoogle Scholar
  98. Vazquez-Flota G, Moreno-Valenzuela ML, Miranda Ham ML, Coello ML, Coello J, Loyola-Vargas VM (1994) Catharanthine and ajmalicine in Catharanthus roseus hairy root cultures. Medium optimization and elicitation. Plant Cell Tissue Organ Cult 38:273–279Google Scholar
  99. Vázquez-Flota F, Hernández-Domínguez E, de Lourdes Miranda-Ham M, Monforte-González M (2009) A differential response to chemical elicitors in Catharanthus roseus in vitro cultures. Biotechnol Lett 31:591–595PubMedGoogle Scholar
  100. Wang JY, Liu ZP, Liu L, Liu C (2008) Effects of NaCl on the growth and alkaloid content of Catharanthus roseus seedlings. Ying Yong Sheng Tai Xue Bao 19:2143–2148PubMedGoogle Scholar
  101. Whitmer S, Canel C, Hallard D, Goncalves C, Verpoorte R (1998) Influence of precursor availability on alkaloid accumulation by transgenic cell line of Catharanthus roseus. Plant Physiol 116:853–857PubMedGoogle Scholar
  102. Whitmer S, Van der Heijden R, Verpoorte R (2000) 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 69:85–93Google Scholar
  103. Xu M, Dong J (2005) Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells. Appl Microbiol Biotechnol 67:40–44PubMedGoogle Scholar
  104. Yang L, Dai J, Sakai J, Ando M (2005) Biotransformation of alpha-santonin by cell suspension cultures of five plants. Biotechnol Lett 27:793–797PubMedGoogle Scholar
  105. Zhao J, Hu Q, Guo YQ, Zhu WH (2001a) Effects of stress factors, bioregulators, and synthetic precursors on indole alkaloid production in compact callus clusters cultures of Catharanthus roseus. Appl Microbiol Biotechnol 55:693–698PubMedGoogle Scholar
  106. Zhao J, Zhu WH, Hu Q (2001b) Effects of light and plant growth regulators on the biosynthesis of vindoline and other indole alkaloids in Catharanthus roseus callus cultures. Plant Growth Reg 33:43–49Google Scholar
  107. Zhao J, Zhu WH, Hu Q (2001c) Enhanced Catharanthine production in Catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Technol 28:673–681PubMedGoogle Scholar
  108. Zhao ML, Shao JR, Tang YX (2009) Production and metabolic engineering of terpenoid indole alkaloids in cell cultures of the medicinal plant Catharanthus roseus (L.) G. Don (Madagascar periwinkle). Biotechnol Appl Biochem 52:313–323Google Scholar
  109. Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis metabolism and trafficking. Annu Rev Plant Biol 59:735–769PubMedGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Abdul Mujib
    • 1
    Email author
  • Abdul Ilah
    • 1
  • Junaid Aslam
    • 1
  • Samar Fatima
    • 1
  • Zahid Hameed Siddiqui
    • 1
  • Mehpara Maqsood
    • 1
  1. 1.Cellular Differentiation and Molecular Genetics Section, Department of BotanyHamdard UniversityNew DelhiIndia

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