Acta Physiologiae Plantarum

, Volume 30, Issue 5, pp 581–593 | Cite as

Betalain production in plant in vitro systems

  • Vasil Georgiev
  • Mladenka Ilieva
  • Thomas Bley
  • Atanas Pavlov
Review

Abstract

Betalains have been widely used as natural colorants for many centuries, but their attractiveness for use as colorants of foods (or drugs and cosmetics) has increased recently due to their reportedly high anti-oxidative, free radical scavenging activities and concerns about the use of various synthetic alternatives. The main commercial sources of betalains are powders and concentrates of red beet (Beta vulgaris) or cactus pear (Opuntia ficus-indica) extracts. However, in recent years the technical and commercial feasibility of various in vitro systems to produce them biotechnologically has been explored. These research activities have included assessments of novel approaches for cultivating plant cell or tissue cultures, and diverse bioreactor systems for increasing production levels of secondary metabolites. This paper reviews recent progress in plant in vitro systems for producing betalain pigments. In addition, the factors that could be manipulated, the bioreactor systems that could be used, and the strategies that could be applied to improve betalain production are discussed.

Keywords

Betalains Biological activity Bioreactors Plant in vitro systems Process optimization 

Abbreviations

2,4-D

2,4-Dichlorophenoxyacetic acid

B5

Gamborg’s B5 medium

BAP

6-Benzylaminopurine

DOPA

3,4-dihydroxy-l-phenylalanine

DPPH

1,1-Diphenyl-2-picrylhydrazyl

LDL

Low density lipoproteins

MS

Murashige and Skoog medium

ROS

Reactive oxygen species

References

  1. Akita T, Hina Y, Nishi T (2000) Production of betacyanins by a cell suspension culture of table beet (Beta vulgaris L.). Biosci Biotech Biochem 64:1807–1812CrossRefGoogle Scholar
  2. Akita T, Hina Y, Nishi T (2001) Effect of zinc deficiency on betacyanin production in a cell suspension culture of table beet (Beta vulgaris L.). Biosci Biotech Biochem 65:962–965CrossRefGoogle Scholar
  3. Akita T, Hina Y, Nishi T (2002) New medium composition for high betacyanin production by a cell suspension culture of table beet (Beta vulgaris L.). Biosci Biotech Biochem 66:902–905CrossRefGoogle Scholar
  4. Allegra M, Furtmuller PG, Jantschko W, Zederbauer M, Tesoriere L, Livrea MA, Obinger C (2005) Mechanism of interaction of betanin and indicaxanthin with human myeloperoxidase and hypochlorous acid. Biochem Biophys Res Commun 332:837–844PubMedCrossRefGoogle Scholar
  5. Altamura MM (2004) Agrobacterium rhizogenes rolB and rolD genes: regulation and involvement in plant development. Plant Cell Tiss Org Cult 77:89–101CrossRefGoogle Scholar
  6. Berlin J, Sieg S, Strack D, Bokern M, Harms H (1986) Production of betalains by suspension cultures of Chenopodium rubrum L. Plant Cell Tiss Org Cult 5:163–174CrossRefGoogle Scholar
  7. Bhagyalakshmi N, Thimmaraju R, Narayan MS (2004) Various hexoses and di-hexoses differently influence growth, morphology and pigment synthesis in transformed root cultures of red beet (Beta vulgaris). Plant Cell Tiss Org Cult 78:183–195CrossRefGoogle Scholar
  8. Bhuiyan NH, Adachi T (2003) Stimulation of betacyanin synthesis through exogenous methyl jasmonate and other elicitors in suspension-cultured cells of Portulaca. J Plant Physiol 160:1117–1124PubMedCrossRefGoogle Scholar
  9. Bianco-Colomas J (1980) Qualitative and quantitative aspects of betalains biosynthesis in Amaranthus caudatus L. var pendula seedlings. Planta 149:176–180CrossRefGoogle Scholar
  10. Böhm H, Böhm L, Rink E (1991) Establishment and characterization of a betaxanthin-producing cell culture from Portulaca grandiflora. Plant Cell Tiss Org Cult 26:75–82CrossRefGoogle Scholar
  11. Böhm H, Mäck G (2004) Betaxanthin formation and free amino acids in hairy roots of Beta vulgaris var. lutea depending on nutrient medium and glutamate or glutamine feeding. Phytochemistry 65:1361–1368PubMedCrossRefGoogle Scholar
  12. Bokern M, Heuer S, Wray V, Witte L, Macek T, Vanek T, Strack D (1991) Ferulic acid conjugates and betacyanins from cell cultures of Beta vulgaris. Phytochemistry 30:3261–3265CrossRefGoogle Scholar
  13. Butera D, Tesoriere L, Di Gaudio F, Bongiorno A, Allegra M, Pintaudi AM, Kohen R, Livrea MA (2002) Antioxidant activities of Sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin. J Agric Food Chem 50:6895–6901PubMedCrossRefGoogle Scholar
  14. Cai Y, Sun M, Corke H (2003) Antioxidant activity of betalains from plants of the Amaranthaceae. J Agric Food Chem 51:2288–2294PubMedCrossRefGoogle Scholar
  15. Cai Y, Sun M, Schliemann W, Corke H (2001) Chemical stability and colorant properties of betaxanthin pigments from Celosia argentea. J Agric Food Chem 49:4429–4435PubMedCrossRefGoogle Scholar
  16. Campos D, Noratto G, Chirinos R, Arbizu C, Roca W, Cisneros-Zevallos L (2006) Antioxidant capacity and secondary metabolites in four species of Andean tuber crops: native potato (Solanum sp.), mashua (Tropaeolum tuberosum Ruiz & Pavon), Oca (Oxalis tuberosa Molina) and ulluco (Ullucus tuberosus Caldas). J Sci Food Agric 86:1481–1488CrossRefGoogle Scholar
  17. Cao G, Sofic E, Prior RL (1996) Antioxidant capacity of tea and common vegetables. J Agric Food Chem 44:3426–3430CrossRefGoogle Scholar
  18. Castellar MR, Obon JM, Fernandez-Lopez J (2006) The isolation and properties of a concentrated red–purple betacyanin food colourant from Opuntia stricta fruits. J Sci Food Agric 86:122–128CrossRefGoogle Scholar
  19. Chethana S, Nayak CA, Raghavarao KSMS (2007) Aqueous two phase extraction for purification and concentration of betalains. J Food Eng 81:679–687CrossRefGoogle Scholar
  20. DiIorio A, Cheetham RD, Weathers PJ (1992) Growth of transformed roots in a nutrient mist bioreactor: reactor performance and evaluation. Appl Microbiol Biotechnol 37: 457–462CrossRefGoogle Scholar
  21. DiIorio A, Weathers PJ, Cheetham RD (1993) Non-lethal secondary product release from transformed root cultures of Beta vulgaris. Appl Microbiol Biotechnol 39:174–180CrossRefGoogle Scholar
  22. Downham A, Collins P (2000) Colouring our foods in the last and next millennium. Int J Food Sci Technol 35:2–22Google Scholar
  23. Eibl R, Eibl D (2002) Bioreactors for plant cell and tissue cultures. In: Oksman-Caldentey KM, Barz WH (eds) Plant biotechnology and transgenic plants. Marcel & Dekker, New York, pp 163–200Google Scholar
  24. Escribano J, Pedreño MA, García-Carmona F, Muñoz R (1998) Characterization of the antiradical activity of betalains from Beta vulgaris L. roots. Phytochem Anal 9:124–127CrossRefGoogle Scholar
  25. Esquivel P, Stintzing FC, Carle R (2007) Phenolic compound profiles and their corresponding antioxidant capacity of purple pitaya (Hylocereus sp.) genotypes. Z Naturforsch C 62:636–644PubMedGoogle Scholar
  26. Flores HE, Medina-Bolívar F (1995) Root culture and plant natural products: “Unearthing” the hidden half of plant metabolism. Plant Tiss Cult Biotechnol 1:59–74Google Scholar
  27. Frank T, Stintzing FC, Carle R, Bitsch I, Quaas D, Strass G, Bitsch R, Netzel M (2005) Urinary pharmacokinetics of betalains following consumption of red beet juice in healthy humans. Pharmacol Res 52:290–297PubMedCrossRefGoogle Scholar
  28. Galati EM, Mondello MR, Giuffrida D, Dugo G, Miceli N, Pergolizzi S, Taviano MF (2003) Chemical characterization and biological effects of Sicilian Opuntia ficus-indica (L.) Mill. fruit juice: antioxidant and antiulcerogenic activity. J Agric Food Chem 51:4903–4908PubMedCrossRefGoogle Scholar
  29. Galati EM, Mondello MR, Lauriano ER, Taviano MF, Galluzzol M, Miceli N (2005) Opuntia ficus indica (L.) Mill. Fruit juice protects liver from carbon tetrachlorideinduced injury. Phytother Res 19:796–800PubMedCrossRefGoogle Scholar
  30. Gandía-Herrero F, Escribano J, García-Carmona F (2005a) Betaxanthins as pigments responsible for visible fluorescence in flowers. Planta 222:586–593PubMedCrossRefGoogle Scholar
  31. Gandía-Herrero F, García-Carmona F, Escribano J (2005b) Botany: floral fluorescence effect. Nature 437:334PubMedCrossRefGoogle Scholar
  32. Gandía-Herrero F, García-Carmona F, Escribano J (2006) Development of a protocol for the semi-synthesis and purification of betaxanthins. Phytochem Anal 17:262–269PubMedCrossRefGoogle Scholar
  33. Georgiev M, Pavlov A, Bley Th (2006) Betalains by transformed Beta vulgaris roots in stirred tank bioreactor: batch and fed-batch processes. FinMed 2006—2nd International conference on bioreactor technology in cell, tissue culture and biomedical applications. Saariselkä, Finland, pp.22–28Google Scholar
  34. Georgiev MI, Pavlov AI, Bley Th (2007) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185PubMedCrossRefGoogle Scholar
  35. Girod PA, Zryd JP (1987) Clonal variability and light induction of betalain synthesis in red beet cell cultures. Plant Cell Rep 6:27–30CrossRefGoogle Scholar
  36. Girod PA, Zryd JP (1991) Secondary metabolism in cultured red beet (Beta vulgaris L.) cells: differential regulation of betaxanthin and betacyanin biosynthesis. Plant Cell Tiss Org Cult 25:1–12CrossRefGoogle Scholar
  37. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780PubMedCrossRefGoogle Scholar
  38. Guillon S, Tremouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 9:341–346PubMedCrossRefGoogle Scholar
  39. Hamill JD, Parr AJ, Robins RJ, Rhodes MJC (1986) Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes. Plant Cell Rep 5:111–114CrossRefGoogle Scholar
  40. Hancock M (1997) Potential for colourants from plant sources in England & Wales. ADAS Arable Crops & Horticulture Division, Boxworth, pp 4–52Google Scholar
  41. Hempel J, Böhm H (1997) Betaxanthin pattern of hairy roots from Beta vulgaris var. Lutea and its alteration by feeding of amino acids. Phytochemistry 44:847–852CrossRefGoogle Scholar
  42. Hilpert H, Dreiding AS (2007) Betalains—the colors of succulents. Historical review of chemical works in Zürich. 75th Anniversary of the Zürich succulent plant collection. https://www.uzh.ch/oci/ssl-dir/efiles/betalain.pdf
  43. Hitaka Y, Takahashi Y, Kino-Oka M, Taya M, Tone S (2000) Culture of red beet hairy roots by considering variation in sensitivity of tip meristems to hydraulic stress. Biochem Eng J 6:1–6PubMedCrossRefGoogle Scholar
  44. Hunter S, Kilby NJ (1999) Betalains: their accumulation and release in vitro. In: Hall RF (ed) Methods in molecular biology: plant cell culture protocols, vol 111. Humana Press Inc., Totowa, pp 403–410CrossRefGoogle Scholar
  45. Ibdah M, Krins A, Seidlitz HK, Heller W, Strack D, Vogt T (2002) Spectral dependence of flavonol and betacyanin accumulation in Mesembryanthemum crystallinum under enhanced ultraviolet radiation. Plant Cell Environ 25:1145–1154CrossRefGoogle Scholar
  46. Jimenez-Aparicio А, Gutierrez-Lopez G (1999) Production of food related colorants by culture of plant cells. The case of betalains. Adv Exp Med Biol 464:195–210PubMedGoogle Scholar
  47. Kanner J, Harel S, Granit R (2001) Betalains—a new class of dietary cationized antioxidants. J Agric Food Chem 49:5178–5185PubMedCrossRefGoogle Scholar
  48. Kapadia GJ, Azuine MA, Sridhar R, Okuda Y, Tsuruta A, Ichiishi E, Mukainake T, Takasaki M, Konoshima T, Nishino H, Tokuda H (2003) Chemoprevention of DMBA-induced UV-B promoted, NOR-1-induced TPA promoted skin carcinogenesis, and DEN-induced phenobarbital promoted liver tumors in mice by extract of beetroot. Pharmacol Res 47:141–148PubMedCrossRefGoogle Scholar
  49. Kapadia GJ, Balasubramanian V, Tokuda H, Iwashima A, Nishino H (1997) Inhibition of 12-O-tetradecanoylphorbol-13-acetate induced Epstein-Barr virus early antigen activation by natural colorants. Cancer Lett 115:173–178PubMedCrossRefGoogle Scholar
  50. Kapadia GJ, Tokuda H, Konoshima T, Nishino H (1996) Chemoprevention of lung and skin cancer by Beta vulgaris (beet) root extract. Cancer Lett 100:211–214PubMedCrossRefGoogle Scholar
  51. Khlebnikov A, Dubuis B, Kut OM, Prenosil JE (1995) Growth and productivity of Beta vulgaris cell culture in fluidized bed reactors. Bioproc Eng 14:51–56CrossRefGoogle Scholar
  52. Kino-Oka M, Taya M, Tone S (1995) Culture of red beet hairy roots in a column-type reactor associated with pigment release. Plant Tiss Cult Lett 12:201–204Google Scholar
  53. Kishima Y, Shimaya A, Adachi T (1995) Evidence that blue light induces betalain pigmentation in Portulaca callas. Plant Cell Tiss Org Cult 43:67–70CrossRefGoogle Scholar
  54. Kobayashi N, Schmidt J, Wray V, Schliemann W (2001) Formation and occurrence of dopamine-derivated betacyanins. Phytochemistry 56: 429–436PubMedCrossRefGoogle Scholar
  55. Kumar JK, Sinha AK (2004) Resurgence of natural colourants: a holistic view. Nat Prod Lett 18:59–84Google Scholar
  56. Leathers RR, Davin C, Zryd JP (1992) Betalain producing cell cultures of Beta vulgaris L var Bikores Monogerm (Red Beet). In Vitro Cell Dev Plant 28:39–45CrossRefGoogle Scholar
  57. Lee JC, Kim HR, Kim J, Jang YS (2002) Antioxidant property of an ethanol extract of the stem of Opuntia ficus-indica var. Saboten. J Agric Food Chem 50:6490–6496PubMedCrossRefGoogle Scholar
  58. Lee MH, Kim JY, Yoon JH, Lim HJ, Kim TH, Jin C, Kwak WJ, Han CK, Ryu JH (2006) Inhibition of nitric oxide synthase expression in activated microglia and peroxynitrite scavenging activity by Opuntia ficus indica var. Saboten. Phytother Res 20:742–747PubMedCrossRefGoogle Scholar
  59. Lila MA (2004) Plant pigments and human health. In: Davies K (ed) Plant pigments and their manipulation. Annu. Plant Rev. vol 14. CRC Press/Blackwell, Oxford, pp 248–274Google Scholar
  60. Mabry TJ (2001) Selected topics from forty years of natural products research: betalains to flavonoids, antiviral proteins, and neurotoxic nonprotein amino acids. J Nat Prod 64:1596–1604PubMedCrossRefGoogle Scholar
  61. Moßhammer MR, Stintzing FC, Carle R (2005) Development of a process for the production of a betalain-based colouring foodstuff from cactus pear. Innov Food Sci Emerg 6:221–231CrossRefGoogle Scholar
  62. Moreno DA, Garcia-Viguera C, Gil JI, Gil-Izquierdo A (2008) Betalains in the era of global agri-food science, technology and nutritional health. Phytochem Rev. doi:10.1007/s11101-007-9084-y
  63. Mukundan U, Bhide V, Dawda H (1999) Production of betalains by hairy root cultures of Beta vulgaris L. In: Fu TJ, Singh G, Curtis WR (eds) Plant cell and tissue culture for the production of food ingradients. Kluwer Academic/Plenum Publishers, New York, pp 121–127Google Scholar
  64. Mukundan U, Bhide V, Singh G, Curtis WR (1998) pH-mediated release of betalains from transformed root cultures of Beta vulgaris L. Appl Microbiol Biotechnol 50:241–245CrossRefGoogle Scholar
  65. Netzel M, Stintzing FC, Quaas D, Strass G, Carle R, Bitsch R, Bitsch I, Frank T (2005) Renal excretion of antioxidative constituents from red beet in humans. Food Res Int 38:1051–1058CrossRefGoogle Scholar
  66. Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol Plant 100:463–473CrossRefGoogle Scholar
  67. Nilsson T (1970) Studies into the pigments in beetroot (Beta vulgaris L. ssp. vulgaris var. rubra L.). Lantbrukshog Ann 36:179–219Google Scholar
  68. Ou B, Haung D, Hampsch-Woodill M, Flanagan JA, Deemer EK (2002) Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: a comparative study. J Agric Food Chem 50:3122–3128PubMedCrossRefGoogle Scholar
  69. Parkinson TM, Brown JP (1981) Metabolic fate of food colorants. Annu Rev Nutr 1:175–205PubMedCrossRefGoogle Scholar
  70. Pavlov A, Bley Th (2006) Betalains biosynthesis by Beta vulgaris L. hairy root culture in a temporary immersion cultivation system. Process Biochem 41:848–852CrossRefGoogle Scholar
  71. Pavlov A, Georgiev V, Ilieva M (2005a) Betalain biosynthesis by red beet (Beta vulgaris L.) hairy root culture. Process Biochem 40:1531–1533CrossRefGoogle Scholar
  72. Pavlov A, Georgiev V, Kovatcheva P (2003) Relationship between type and age of the inoculum cultures and betalains biosynthesis by Beta vulgaris hairy root culture. Biotechnol Lett 25:307–309PubMedCrossRefGoogle Scholar
  73. Pavlov A, Kovatcheva P, Georgiev V, Koleva I, Ilieva M (2002) Biosynthesis and radical scavenging activity of betalains during the cultivation of red beet (Beta vulgaris) hairy root cultures. Z Naturforsch C 57:640–644PubMedGoogle Scholar
  74. Pavlov A, Kovatcheva P, Tuneva D, Ilieva M, Bley Th (2005) Radical scavenging activity and stability of betalains from Beta vulgaris hairy root culture in simulated conditions of human gastrointestinal tract. Plant Foods Hum Nutr 60:43–47PubMedCrossRefGoogle Scholar
  75. Piattelli M (1976) Betalains. In: Goodwin TW (eds) Chemistry and biochemistry of plant pigments, vol 1. Academic Press, London, pp 560–596Google Scholar
  76. Ramakrishnan D, Luyk D, Curtis WR (1999) Monitoring biomass in root culture systems. Biotechnol Bioeng 62:711–721PubMedCrossRefGoogle Scholar
  77. Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153PubMedCrossRefGoogle Scholar
  78. Rodríguez-Monroy M, Galindo E (1999) Broth rheology, growth and metabolite production of Beta vulgaris suspension culture: a comparative study between cultures grown in shake flasks and in a stirred tank. Enzyme Microb Technol 24:687–693CrossRefGoogle Scholar
  79. Rodríguez-Monroy M, Jiménez-Aparicio A, Dávila-Ortíz G, Sepúlveda-Jiménez G (1994) Effect of carbon source on cell growth and betalain production in cell suspension culture of Beta vulgaris. Biotechnol Lett 16:853–858CrossRefGoogle Scholar
  80. Rudat A, Göring H (1995) Induction of betacyanin formation in cell cultures of Chenopodium album under UV-light irradiation. J Exp Bot 46:129–134CrossRefGoogle Scholar
  81. Sajilata MG, Singhal RS (2006) Isolation and stabilisation of natural pigments for food applications. Stewart Postharvest Rev 2:1–29CrossRefGoogle Scholar
  82. Sakuta M, Hirano H, Komamine A (1991) Stimulation by 2,4-dichlorophenoxyacetic acid of betacyanin accumulation in suspension cultures of Phytolacca americana. Physiol Plantarum 83:154–158CrossRefGoogle Scholar
  83. Sánchez MJ, Jiménez-Aparicio A, López GG, Trejo-Tapia G, Rodríguez-Monroy M (2002) Broth rheology of Beta vulgaris cultures growing in an air lift bioreactor. Biochem Eng J 12:37–41CrossRefGoogle Scholar
  84. Santos-Díaz MS, Velásquez-Garciía Y, González-Chávez MM (2005) Pigment production by callus of Mammillaria candida Scheidweiler (Cactaceae). Agrociencia 39:619–626Google Scholar
  85. Sasson A (1991) Production of useful biochemicals by higher-plant cell cultures: biotechnological and economic aspects. CIHEAM-IAMZ, Options Méditerranéennes - Série Séminaires 14:59–74Google Scholar
  86. Savitha BC, Thimmaraju R, Bhagyalakshmi N, Ravishankar GA (2006) Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor. Process Biochem 41:50–60CrossRefGoogle Scholar
  87. Schliemann W, Joy RW 4th, Komamine A, Metzger JW, Nimtz M, Wray V, Strack D (1996) Betacyanins from plants and cell cultures of Phytolacca americana. Phytochem 42:1039–1046CrossRefGoogle Scholar
  88. Schliemann W, Kobayashi N, Strack D (1999) The decisive step in betaxanthin biosynthesis is a spontaneous reaction. Plant Physiol 119:1217–1232PubMedCrossRefGoogle Scholar
  89. Schoefs B (2004) Determination of pigments in vegetables. J Chromatogr A 1054:217–226PubMedCrossRefGoogle Scholar
  90. Schwartz SJ, von Elbe JH (1983) Inability of red beet betalain pigments to initiate or promote hepatocarcinogenesis. Food Chem Toxicol 21:531–535PubMedCrossRefGoogle Scholar
  91. Sepúlveda-Jiménez G, Rueda-Benítez P, Porta H, Rocha-Sosa M (2004) Betacyanin synthesis in red beet (Beta vulgaris) leaves induced by wounding and bacterial infiltration is preceded by an oxidative burst. Physiol Mol Plant Pathol 64:125–133CrossRefGoogle Scholar
  92. Sepúlveda-Jiménez G, Rueda-Benítez P, Porta H, Rocha-Sosa M (2005) A red beet (Beta vulgaris) UDP-glucosyltransferase gene induced by wounding, bacterial infiltration and oxidative stress. J Exp Bot 56:605–611PubMedCrossRefGoogle Scholar
  93. Shanks JV, Morgan J (1999) Plant “hairy root” culture. Curr Opin Biotech 10:151–155PubMedCrossRefGoogle Scholar
  94. Shin KS, Chakrabarty D, Ko JY, Han SS, Paek KY (2003) Sucrose utilization and mineral nutrient uptake during hairy root growth of red beet (Beta vulgaris L.) in liquid culture. Plant Growth Regul 39:187–193CrossRefGoogle Scholar
  95. Shin KS, Murthy HN, Heo JW, Paek KY (2003a) Induction of betalain pigmentation in hairy roots of red beet under different radiation sources. Biol Plant 47:149–152CrossRefGoogle Scholar
  96. Shin KS, Murthy HN, Ko JY, Peak KY (2002) Growth and betacyanin production by hairy roots of Beta vulgaris in airlift bioreactors. Biotechnol Lett 24:2067–2069CrossRefGoogle Scholar
  97. Silva NCB, Macedo AF, Lage CLS, Esquibel MA, Sato A (2005) Developmental effects of additional ultraviolet A radiation, growth regulators and tyrosine in Alternanthera brasiliana (L.) Kuntze cultured in vitro. Braz Arc Biol Technol 48:779–786Google Scholar
  98. Sreekanth D, Arunasree MK, Roy KR, Chandramohan T, Reddy GV, Reddanna P (2007) Betanin a betacyanin pigment purified from fruits of Opuntia ficus-indica induces apoptosis in human chronic myeloid leukemia Cell line-K562. Phytomedicine 14:739–746PubMedCrossRefGoogle Scholar
  99. Steiner U, Schliemann W, Böhm H, Strack D (1999) Tyrosinase involved in betalain biosynthesis of higher plants. Planta 208:114–124CrossRefGoogle Scholar
  100. Stintzing FC, Carle R (2004) Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci Technol 15:19–38CrossRefGoogle Scholar
  101. Stintzing FC, Carle R (2007) Betalains—emerging prospets for food sciences. Trends Food Sci Technol 18:514–525CrossRefGoogle Scholar
  102. Stintzing FC, Carle R (2008a) N-heterocyclic pigments: betalains. In: Socaciu C (eds) Food colorants: chemical and functional properties. CRC Press/Taylor & Francis, Boca Raton/London, pp 87–100Google Scholar
  103. Stintzing FC, Carle R (2008b) Betalains in food: occurrence, stability, and postharvest modifications. In: Socaciu C (eds) Food colorants: chemical and functional properties. CRC Press/Taylor & Francis, Boca Raton/London, pp 277–302Google Scholar
  104. Stintzing FC, Herbach KM, Moßhammer MR, Carle R, Yi WG, Sellappan S, Akoh CC, Bunch R, Felker P (2005) Color, betalain pattern, and antioxidant properties of cactus pear (Opuntia spp.) clones. J Agric Food Chem 53:442–451PubMedCrossRefGoogle Scholar
  105. Strack D, Vogt T, Schliemann W (2003) Recent advances in betalain research. Phytochemistry 62:247–269PubMedCrossRefGoogle Scholar
  106. Suresh B, Thimmaraju R, Bhagyalakshmi N, Ravishankar GA (2004) Polyamine and methyl jasmonate-induced enhancement of betalaine production in hairy root cultures of Beta vulgaris grown in bubble column reactor and studies on efflux of pigments. Process Biochem 39:2091–2096CrossRefGoogle Scholar
  107. Takahashi Y, Hitaka Y, Kino-Oka M, Taya M, Tone S (2001) Evaluation of growth property of red beet hairy roots depending on condition of inocula and its application to culture control with fuzzy logic theory. Biochem Eng J 8:121–127CrossRefGoogle Scholar
  108. Taya M, Mine K, Kino-Oka M, Tone S, Ichi T (1992) Production and release of pigments by culture of transformed hairy root of red beet. J Fermen Bioeng 73:31–36CrossRefGoogle Scholar
  109. Taya M, Yakura K, Kino-Oka M, Tone S (1994) Influence of medium constituents on enhancement of pigment production by batch culture of red beet hairy roots. J Ferment Bioeng 77:215–217CrossRefGoogle Scholar
  110. Tesoriere L, Allegra M, Butera D, Livrea MA (2004) Absorption, excretion, and distribution of dietary antioxidant betalains in LDLs: potential health effects of betalains in humans. Am J Clin Nutr 80:941–945PubMedGoogle Scholar
  111. Tesoriere L, Butera D, Pintaudi AM, Allegra M, Livrea MA (2004a) Supplementation with cactus pear (Opuntia ficus-indica) fruit decreases oxidative stress in healthy humans: a comparative study with vitamin C. Am J Clin Nutr 80:391–395PubMedGoogle Scholar
  112. Thimmaraju R, Bhagyalakshmi N, Narayan MS, Ravishankar GA (2003a) Kinetics of pigment release from hairy root cultures of Beta vulgaris under the influence of pH, sonication, temperature and oxygen stress. Process Biochem 38:1069–1076CrossRefGoogle Scholar
  113. Thimmaraju R, Bhagyalakshmi N, Narayan MS, Ravishankar GA (2003) Food-grade chemical and biological agents permeabilize red beet hairy roots, assisting the release of betalaines. Biotechnol Prog 19:1274–1282PubMedCrossRefGoogle Scholar
  114. Trejo-Tapia G, Jimenez-Aparicio A, Rodriguez-Monroy M, De Jesus-Sanchez A, Gutierrez-Lopez G (2001) Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tiss Org Cult 67:19–23CrossRefGoogle Scholar
  115. Uozumi N (2004) Large-scale production of hairy root. Adv Biochem Eng Biotehnol 91:75–103Google Scholar
  116. Vanisree M, Lee CY, Lo SF, Nalawade SM, Lin CY, Tsay HS (2004) Studies on the production of some important secondary metabolites from medicinal plants by plant tissue cultures. Bot Bull Acad Sin 45:1–22Google Scholar
  117. Vieira CC, Braga MR, Figueiredo-Ribeiro RC (1995) Fructans in callus of Gomphrena macrocephala St.-Hil. Plant Cell Tiss Org Cult 42:233–238CrossRefGoogle Scholar
  118. von Elbe JH, Schwartz SJ (1981) Absence of mutagenic activity and short-term toxicity study of beet pigments as food colorants. Arch Toxicol 49:93–98CrossRefGoogle Scholar
  119. Vygodin VA, Babodei AP, Ivanov VV, Frolov VL, Yu LC (1995) Colouring agent from beetroot. Molochnaya Promyshlennost 1:6–16Google Scholar
  120. Wybranec S (2005) Formation of decarboxylated betacyanins in heated purified betacyanin fractions from red beet root (Beta vulgaris L.) monitored by LC-MS/MS. J Agric Food Chem 59: 3483–3487CrossRefGoogle Scholar
  121. Wybranec S, Mizrahi Y (2005) Generation of decarboxylated and dehydrogenated betacyanins in thermally treated purified fuit extracts from purple pitaya (Hylocereus polyrhyzus) monitored by LC-MS/MS. J Agric Food Chem 53:6704–6712CrossRefGoogle Scholar
  122. Weathers PJ, Zobel RW (1992) Aeroponics for the culture of organisms, tissues and cells. Biotechnol Adv 10:93–115PubMedCrossRefGoogle Scholar
  123. Wettasinghe M, Bolling B, Plhak L, Parkin K (2002a) Screening for phase II enzyme-inducing and antioxidant activities of common vegetables. J Food Sci 67:2583–2588CrossRefGoogle Scholar
  124. Wettasinghe M, Bolling B, Plhak L, Xiao H, Parkin K (2002b) Phase II enzyme-inducing and antioxidant activities of beetroot (Beta vulgaris L.) extracts from phenotypes of different pigmentation. J Agric Food Chem 50:6704–6709PubMedCrossRefGoogle Scholar
  125. Wohlpart A, Black SM (1973) Accumulation of betanin in disks of Beta vulgaris leaves. Phytochemistry 12:1325–1329CrossRefGoogle Scholar
  126. Yang RYK, Bayraktar O, Pu HT (2003) Plant-cell bioreactors with simultaneous electropermeabilization and electrophoresis. J Biotechnol 100:13–22PubMedCrossRefGoogle Scholar
  127. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333PubMedCrossRefGoogle Scholar
  128. Zrÿd JP, Christinet L (2004) Betalains. In: Davies K (eds) Plant pigments and their manipulation, Annu. Plant Rev., vol 14. CRC Press/Blackwell, Oxford, pp 185–213Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2008

Authors and Affiliations

  • Vasil Georgiev
    • 1
  • Mladenka Ilieva
    • 1
  • Thomas Bley
    • 2
  • Atanas Pavlov
    • 1
  1. 1.Department of Microbial Biosynthesis and Biotechnologies, Laboratory in PlovdivThe Stephan Angeloff Institute of Microbiology, Bulgarian Academy of SciencesPlovdivBulgaria
  2. 2.Institute of Food Technology and Bioprocess EngineeringDresden University of TechnologyDresdenGermany

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