Advertisement

Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation

  • Hosakatte Niranjana MurthyEmail author
  • Eun-Jung Lee
  • Kee-Yoeup PaekEmail author
Review

Abstract

Plant cell and organ cultures have emerged as potential sources of secondary metabolites, which are used as pharmaceuticals, agrochemicals, flavors, fragrances, coloring agents, biopesticides, and food additives. In recent years, various strategies have been developed to assess biomass accumulation and synthesis of secondary compounds in cultures. Biomass accumulation and metabolite biosynthesis are two-stage events, and the parameters that control the growth and multiplication of cultured cells/organs and biomass accumulation are controlled in the first stage. Parameters that assist with the biosynthesis of metabolites are controlled in the second stage. The selection of high-producing cells or organ clones; optimization of medium parameters such as suitable medium, salt, sugar, nitrogen, phosphate, and plant growth regulator levels; and physical factors such as temperature, illumination, light quality, medium pH, agitation, aeration, and environmental gas (e.g., oxygen, carbon dioxide, and ethylene) are controlled in the first stage of the culture process. Elicitation, replenishment of nutrient and precursor feeding, permeabilization, and immobilization strategies assist with the accumulation of metabolites and can be applied in the second stage of the culture process. By following stage-specific strategies, it is possible to produce large amounts of biomass with an increase in the accumulation of secondary compounds.

Keywords

Bioreactor cultures Elicitation Immobilization Permeabilization Plant cell cultures Secondary metabolites 

Abbreviations

ABA

Abscisic acid

BA

Benzyladenine

B5

Gamborg’s medium

2,4-D

2,4-Dichlorophenoxyacetic acid

DW

Dry weight

DMSO

Dimethylsulfoxide

FW

Fresh weight

GA

Gibberellic acid

HPLC

High performance liquid chromatography

HPTLC

High performance thin layer chromatography

2-iP

2-Isopentenyladenine

IAA

Indole-3-acetic acid

IBA

Indole-3-butyric acid

LS

Linsmaier and Skoog medium

MS

Murashige and Skoog medium

NAA

Naphthaleneacetic acid

NMR

Nuclear magnetic resonance

SH

Schenk and Hildebrandt medium

TLC

Thin layer chromatography

PUFAs

Polyunsaturated fatty acids

UV

Ultraviolet light

Notes

Acknowledgments

This study was supported by a grant from the Korea Healthcare Technology R&D project, Ministry of Health and Welfare, Republic of Korea (Grant No. A103017). Dr. H. N. Murthy is thankful to the Ministry of Education, Science, and Technology, Republic of Korea for the award of Brainpool Fellowship (131S-4-3-0523); this study was also supported by the Ministry of Science, ICT and Planning (MSIP).

References

  1. Anonymous (2013) 2012 Ginseng statistical year book. Ministry of Agriculture, Food and Rural Affairs, SeoulGoogle Scholar
  2. Aoyagi H, Kobayashi Y, Yamada K, Yokoyama M, Kusakari K, Tanaka H (2001) Efficient production of saikosaponins in Bupleurum falcatum root fragments combined with signal transducers. Appl Microbiol Biotechnol 57:482–488PubMedGoogle Scholar
  3. Archambault J, Volesky B, Kurz WGW (1989) Surface immobilization of plant cells. Biotechnol Bioeng 33:293–299PubMedGoogle Scholar
  4. Asada M, Shuler ML (1989) Stimulation of ajmalicine production and excretion from Catharanthus roseus: effects of adsorption in situ, elicitors, and alginate immobilization. Appl Microbiol Biotechnol 30:475–481Google Scholar
  5. Badaoui HE, Morard P, Henry M (1996) Stimulation of the growth and solamargine production by Solanum paludosum multiple shoot cultures using a new culture medium. Plant Cell Tiss Org Cult 45:153–158Google Scholar
  6. Bais HP, Sudha G, George J, Ravishankar GA (2001) Influence of exogenous hormones on growth and secondary metabolite production in hairy root cultures of Cichorium intybus L. cv. Lucknow local. In Vitro Cell Dev Biol Plant 37:293–999Google Scholar
  7. Banerjee S, Singh S, Rahaman LU (2012) Biotransformation studies using hairy root cultures—a review. Biotechnol Adv 30:461–468PubMedGoogle Scholar
  8. Baque MA, Moh SH, Lee EJ, Zhong JJ, Paek KY (2012) Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants in bioreactor. Biotechnol Adv 30:1255–1267PubMedGoogle Scholar
  9. Beaumont MD, Knorr D (1987) Effect of immobilizing agents and procedures on viability of cultured celery (Apium graveolens) cells. Biotechnol Lett 9:377–382Google Scholar
  10. Beiderbeck R, Knoop B (1988) Medicinal and aromatic plants Biotechnology in agriculture and forestry. In: Bajaj YPS (ed) Enhanced production of secondary substances addition of artificial accumulation sites to cultures, vol 4. Springer, Berlin, pp 123–135Google Scholar
  11. 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 5:163–174Google Scholar
  12. Biondi S, Lenzi C, Baraldi R, Bagni N (1997) Hormonal effects on growth and morphology of normal and hairy roots of Hyoscyamus muticus. J Plant Growth Regul 16:159–167Google Scholar
  13. Bramble JL, Graves DJ, Brodelius P (1991) Calcium and phosphate effects on growth and alkaloid production in Coffea arabica: experimental results and mathematical model. Biotechnol Bioeng 37:859–868PubMedGoogle Scholar
  14. Brodelius P (1988) Permeabilization of plant cells for release of intracellularly stored products: viability studies. Appl Micorbiol Biotechnol 27:561–566Google Scholar
  15. Brodelius P, Deus B, Mosbach K, Zenk MH (1979) Immobilized plant cells for the production of natural products. EEBS Lett 103:93–97Google Scholar
  16. Chan LK, Koay SS, Boey PL, Bhatt A (2010) Effect of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol Res 43:127–135PubMedGoogle Scholar
  17. Chattopadhyay S, Farkya S, Srivastava AK, Bisaria VS (2002) Bioprocess considerations for production of secondary metabolites. Biotechnol Bioprocess Eng 7:138–149Google Scholar
  18. Choi JW (1992) In situ berberine separation with immobilized adsorbent in cell suspension culture of Thalictrum rugosum. Korean J Chem Eng 9:128–134Google Scholar
  19. Choi SM, Son SH, Yun SR, Kwon OW, Seon JH, Paek KY (2000) Pilot-scale culture of adventitious roots of ginseng in a bioreactor system. Plant Cell Tiss Org Cult 62:187–193Google Scholar
  20. Contin A, van der Heijden R, Verpoorte R (1999) Effects of alkaloid precursor feeding and elicitation on the accumulation of secologanin in a Catharanthus roseus cell suspension culture. Plant Cell Tiss Org Cult 56:111–119Google Scholar
  21. Courtois D, Guern J (1980) Temperature response of Catharanthus roseus cells cultivated in liquid medium. Plant Sci Lett 17:473–482Google Scholar
  22. Dandin VS, Murthy HN (2012) Enhanced in vitro multiplication of Nothapodytes nimmoniana Graham using semisolid and liquid cultures and estimation of camptothecin in the regenerated plants. Acta Physiol Plant 34:1381–1386Google Scholar
  23. Dedaldechamp F, Uhel C, Macheix JJ (1995) Enhancement of anthocyanin synthesis and dihydroflavonol reductase (DFR) activity in response to phosphate deprivation in grape cell suspension. Phytochemistry 40:1357–1360Google Scholar
  24. DiCosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13:425–453PubMedGoogle Scholar
  25. DiCosmo F, Towers GHN (1984) Stress and Secondary metabolism in cultured plant cells. In: Timmermann BN, Steelink C, Loewus FA (eds) Phytochemical adaptations to stress: Recent advances in phytochemistry, vol 18. Springer, New York, pp 97–175Google Scholar
  26. DiCosmo F, Tanaka H, Neumann AW (1994) Cell immobilization by absorption to glass fiber mats. In: Veliky IA, McLean RJC (eds) Immobilized biosystems. Springer, New York, pp 263–287Google Scholar
  27. Do CB, Cormier F (1990) Accumulation of anthocyanins enhanced by a high osmotic potential in grape (Vitis vinifera L.) cell suspensions. Plant Cell Rep 9:143–146PubMedGoogle Scholar
  28. Dong J, Wan G, Liang Z (2010) Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture. J Biotechnol 148:99–104PubMedGoogle Scholar
  29. Dornenburg H (2004) Evaluation of immobilization effects on metabolic activities and productivity in plant cells processes. Process Biochem 39:1369–1375Google Scholar
  30. Dornenburg H, Knorr D (1993) Cellular permeabilization of cultured plant cell tissues by high electric pulses or ultrahigh pressure for recovery of secondary metabolites. Food Biotechnol 7:35–48Google Scholar
  31. Dornenburg H, Knorr D (1995) Strategies for improvement of secondary metabolite production in plant cell cultures. Enz Microb Technol 17:674–684Google Scholar
  32. Dougall DK (1980) Nutrition and metabolism. In: Staba EJ (ed) Plant tissue culture as a source of biochemicals. CRC Press, Boca Raton, pp 21–58Google Scholar
  33. 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 163–199Google Scholar
  34. Eibl R, Werner S, Eibl D (2010) Bag bioreactor based on wave induced motion: characteristics and applications. Adv Biochem Eng Biotechnol 115:55–87Google Scholar
  35. Fett-Neto AG, DiCosmo F (1996) Production of paclitaxel and related toxoids in cell cultures of Taxus cuspidata: perspectives for industrial applications. In: DiCosmo F, Misawa M (eds) Plant cell culture: secondary metabolism toward industrial application. CRC Press, New York, pp 139–166Google Scholar
  36. Folk LR, Doran PM (1996) Influence of inoculum morphology on growth of hairy roots and production of tropane alkaloids. Biotechnol Lett 18:1099–1104Google Scholar
  37. Fulzele DP, Heble MR, Rao PS (1995) Production of terpenoids from Artemisia annua L. plantlet cultures in bioreactor. J Biotechnol 40:139–143Google Scholar
  38. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158PubMedGoogle Scholar
  39. Gao JW, Lee JM (1992) Effect of oxygen supply on the suspension culture of genetically modified tobacco cells. Biotechnol Prog 8:285–290PubMedGoogle Scholar
  40. Georgiev MI, Weber J, Maciuk A (2009) Bioprocessing of plant cell cultures for mass production of targeted compounds. Appl Microbiol Biotechnol 83:809–823PubMedGoogle Scholar
  41. Giri A, Narasu ML (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18:1–22PubMedGoogle Scholar
  42. Giri A, Dhingra V, Giri CC, Singh A, Ward OP, Narasu ML (2001) Biotransformation using plant cells, organ cultures and enzyme systems: current trends and future prospects. Biotechnol Adv 19:175–199PubMedGoogle Scholar
  43. Gundlach H, Zenk MH (1998) Biological activity and biosynthesis of pentacyclic oxylipins: the linoleic acid pathway. Phytochemistry 47:527–537Google Scholar
  44. Hagimori M, Matsumoto T, Obi Y (1982) Studies on production of Digitalis cardenolides by plant tissue culture III. Effect of nutrients on digitoxin formation by shoot-forming cultures of Digitalis purpurea L. grown in liquid media. Plant Cell Physiol 23:1205–1211Google Scholar
  45. Hahlbrock K, Wellman E (1973) Light-independent induction of enzyme related to phenylpropanoid metabolism in cell suspension cultures from parsley. Biochem Biphys Acta 304:702–706Google Scholar
  46. Haldimann D, Brodelius P (1987) Redirecting cellular metabolism by immobilization of cultured plant cells: a model study with Coffea arabica. Phytochemistry 26:1431–1434Google Scholar
  47. Huang SY, Chou CJ (2000) Effect of gaseous composition on cell growth and secondary metabolite production in suspension culture of Stizolobium hassjoo cells. Bioprocess Eng 23:585–593Google Scholar
  48. Ilieva M, Pavlov A (1996) Rosamarinic acid by Lavandula vera MM cell suspension: phosphorous effect. Biotechnol Lett 18:913–916Google Scholar
  49. Jeong CS, Murthy HN, Hahn EJ, Paek KY (2008) Improved production of ginsenosides in suspension cultures of ginseng by medium replenishment strategy. J Biosci Bioeng 105:288–291PubMedGoogle Scholar
  50. Jeong CS, Murthy HN, Hahn EJ, Lee HL, Paek KY (2009) Inoculum size and auxin concentration influence the growth of adventitious roots and accumulation of ginsenosides in suspension cultures of ginseng (Panax ginseng C. A. Meyer). Acta Physiol Plant 31:219–222Google Scholar
  51. Kakegawa K, Hattori E, Koike K, Takeda K (1991) Induction of anthocyanin synthesis and related enzyme activities in cell cultures of Centaurea cyanus by UV-light irradiation. Phytochemistry 30:2271–2273Google Scholar
  52. Kanokwaree K, Doran PM (1997) Effect of inoculums morphology on growth of Atropa belladonna hairy root in shake flaks. J Ferment Bioeng 84:378–381Google Scholar
  53. Ketchum REB, Gison DM, Croteau RB, Shuler ML (1999) The kinetics of taxoid accumulation in cell suspension cultures of Texus following elicitation with methyl jasmonate. Biotechnol Bioeng 63:97–105Google Scholar
  54. Kim DI, Pedersen H, Chin CK (1991) Cultivation of Thalictrum rugosum cell suspension in an improved air-lift bioreactor: stimulatory effect of carbon dioxide and ethylene on alkaloid production. Biotechnol Bioeng 38:331–339PubMedGoogle Scholar
  55. Kim YS, Hahn EJ, Murthy HN, Paek KY (2004) Adventitious root growth and ginsenoside accumulation in Panax ginseng cultures as affected by methyl jasmonate. Biotechnol Lett 26:1619–1622PubMedGoogle Scholar
  56. Knorr D, Teutonico RA (1986) Chitoson immobilization and permeabilization of Amaranthus tricolor cells. J Agric Food Chem 34:96–97Google Scholar
  57. Kobayashi Y, Fukai H, Tabata M (1991) Effect of carbon dioxide and ethylene on berberine production and cell browning in Thalictrum minus cell cultures. Plant Cell Rep 9:496–499PubMedGoogle Scholar
  58. Konczak-Islam I, Yoshinaga M, Nakatani M, Terahara N, Yamakawa O (2000) Establishment and characteristics of an anthocyanin-producing cell line from sweet potato root. Plant Cell Rep 19:472–477Google Scholar
  59. Kreuzaler F, Hahlbrock K (1973) Flavonoid glycosides from illuminated cell suspension cultures of Petroselinum hortense. Phytochemistry 12:1149–1152Google Scholar
  60. Kutney JP (1993) Plant cell culture combined with chemistry: a powerful route to complex natural products. Acc Chem Res 26:559–566Google Scholar
  61. Kwon IC, Yoo YJ, Lee JH, Hyun JO (1998) Enhancement of taxol production by in situ recovery of product. Process Biochem 33:701–707Google Scholar
  62. Lee CWT, 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
  63. Li W, Koike K, Asada Y, Yoshikawa T, Nikaido T (2005) Biotransformation of paeonol by Panax ginseng root and cell cultures. J Mol Catalysis B Enz 35:117–121Google Scholar
  64. Liang LF, Keng CL, Lim BP (2006) Selection of cell lines for the production of rosmarinic acid from cell suspension cultures of Orthosiphon stamineus Benth. In Vitro Cell Dev Biol Plant 42:538–542Google Scholar
  65. Lin L, Wu J, Ho KP, Qi S (2001) Ultrasound-induced physiological effects and secondary metabolite (saponin) production in Panax ginseng cell cultures. Ultrasound Med Biol 27:1147–1152PubMedGoogle Scholar
  66. Lindsey K, Yeoman MM (1984) The synthetic potential of immobilized cells of Capsicum frutescens Mill. cv. annuum. Planta 162:495–501PubMedGoogle Scholar
  67. Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127Google Scholar
  68. Liu S, Zhnong JJ (1998) Phosphate effect on production of ginseng saponin and polysaccharide by cell suspension cultures of Panax ginseng and Panax quinquefolius. Proc Biochem 33:69–74Google Scholar
  69. Liu CZ, Wang YC, Ouyang F, Ye HC, Li GF (1997) Production of artemisinin in hairy root culture of Artemisia annua L. Biotechnol Lett 19:927–929Google Scholar
  70. Liu CZ, Guo C, Wang YC, Ouyang F (2002) Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Proc Biochem 38:581–585Google Scholar
  71. Mantell SH, Smith H (1984) Culture factors that influence secondary metabolite accumulation in plant cell and tissue cultures. In: Mantell SH, Smith H (eds) Plant biotechnology. Cambridge Univ Press, Cambridge, pp 75–108Google Scholar
  72. Matsubara K, Kitani S, Yoshioka T, Morimoto T, Fujita Y, Yamada Y (1989) High density culture of Coptis japonica cells increases berberine production. J Chem Technol Biotechnol 46:61–69Google Scholar
  73. Matsumoto T, Ikeda T, Kanno N, Kisaki T (1980) Noguchi M. Selection of high ubiquinone 10-producing strain of tobacco cultures by cell cloning technique. Agric Biol Chem 44:967–969Google Scholar
  74. Mavituna F, Buyukalaca S (1996) Somatic embryogenesis of pepper in bioreactors: a study of bioreactor type and oxygen-uptake rates. Appl Microbiol Biotechnol 46:327–333Google Scholar
  75. McDonald KA, Jackman AP (1989) Bioreactor studies of growth and nutrient utilization in alfalfa suspension cultures. Plant Cell Rep 8:455–458PubMedGoogle Scholar
  76. Meyer HJ, Van Staden J (1995) The in vitro production of anthocyanin from callus cultures of Oxalis linearis. Plant Cell Tiss Org Cult 40:55–58Google Scholar
  77. Miao GP, Zhu CS, Yang YQ, Feng MX, Ma ZQ, Feng JT, Zhang X (2013) Elicitation and in situ adsorption enhanced secondary metabolites production of Tripterygium wilfordii Hook. f. adventitious root fragment liquid cultures in shake flask and a modified bubble column bioreactor. Bioprocess Biosyst Eng. doi:  10.1007/s00449-013-1033-0
  78. Mok MC, Gabelman Wh, Skoog F (1976) Carotenoid synthesis in tissue cultures of Daucus carota. J Am Soc Hortic Sci 101:442–449Google Scholar
  79. Moreno PRH, Schlatmann JE, van der Heijden R, van Gulik WM, ten Hoopern HJG, Verpoorte R, Heijnen JJ (1993a) Induction of ajmalicine formation and related enzyme activities in Catharanthus roseus cells: effect of inoculum density. Appl Microbiol Biotechnol 39:42–47PubMedGoogle Scholar
  80. Moreno PRH, van der Heijden R, Verpoorte R (1993b) Effect of terpenoid precursor feeding and elicitation on formation of indole alkaloids in cell suspension cultures of Catharanthus roseus. Plant Cell Rep 199(12):702–705Google Scholar
  81. Morris P (1986) Regulation of product synthesis in cell cultures of Catharanthus roseus. Effect of culture temperature. Plant Cell Rep 5:427–429PubMedGoogle Scholar
  82. Mukherjee SK, Rathinasabapathi B, Gupta N (1991) Low sugar and osmotic requirements for shoot regeneration from leaf pieces of Solanum melongena L. Plant Cell Tiss Org Cult 25:13–16Google Scholar
  83. Mukundan U, Hjortso AM (1991) Growth and thiophene accumulation by hairy root cultures of Tagets petula in media of varying initial pH. Plant Cell Rep 9:627–630PubMedGoogle Scholar
  84. 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 50:241–245Google Scholar
  85. Mulder-Krieger TH, Verpoorte R, Svendse AB, Scheffer JJC (1988) Production of essential oils and flavours in plant cell and tissue cultures. A review. Plant Cell Tiss Org Cult 13:85–154Google Scholar
  86. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479Google Scholar
  87. Murthy HN, Hahn EJ, Paek KY (2008a) Adventitious root and secondary metabolism. Chin J Biotechnol 24:711–716Google Scholar
  88. Murthy HN, Dijkstra C, Anthony P, White DA, Davey MR, Power JB, Hahn EJ, Paek KY (2008b) Establishment of Withania somnifera hairy root cultures for the production of withanolide A. J Integr Plant Biol 50:975–981PubMedGoogle Scholar
  89. Nagella P, Murthy HN, Chung IM (2011) In vitro production of gymnemic acid from cell suspension cultures of Gymnema sylvestre R. Br Eng Life Sci 11:537–540Google Scholar
  90. Naik PM, Manohar SH, Praveen N, Murthy HN (2010) Effects of sucrose and pH levels on in vitro shoot regeneration from leaf explants of Bacopa monnieri and accumulation of bacoside A in regenerated shoots. Plant Cell Tiss Org Cult 100:235–239Google Scholar
  91. Naik PM, Manohar SH, Murthy HN (2011) Effects of macro elements and nitrogen source on biomass accumulation and bacoside A production from adventitious shoot cultures of Bacopa monnieri (L.). Acta Physiol Plant 33:1553–1557Google Scholar
  92. Naik PM, Manohar SH, Praveen N, Upadhya V, Murthy HN (2012) Evaluation of bacoside A content in different accessions and various organ of Bacopa monnieri (L.) Wettst. J Herbs Spices Med Plants 18:387–395Google Scholar
  93. Nakamura M, Takeuchi Y, Miyanaga K, Seki M, Furasaki S (1999) High anthocyanin accumulation in the dark by strawberry (Fragaria ananassa) callus. Biotechnol Lett 21:695–699Google Scholar
  94. Nigam SC, Saihpush AR, Wang HY (1990) Analysis of bioproduct separation using gel-enclosed adsorbents. AIChE J 36:1239–1248Google Scholar
  95. Nilsson K, Birnbaum S, Flygare S, Linse L, Schroder U, Jeppsson U, Larsson P, Mosbach K, Brodelius P (1983) A general method for the immobilization of cells with preserved viability. Eur J Appl Microbiol Biotechnol 17:319–326Google Scholar
  96. Panda AK, Bisaria VS, Mishra S (1992) Alkaloid production by plant cell cultures of Holarrhena antidysenterica: II Effect of precursor feeding and cultivation in stirred tank bioreactor. Biotechnol Bioeng 39:1052–1057PubMedGoogle Scholar
  97. Park YG, Kim SJ, Kang YM, Jung HY, Theerth Prasad D, Kim SW, Chung YG, Choi MS (2004) Production of ginkgolides and bilobalides from optimized the Ginkgo biloba cell cultures. Biotechnol Bioprocess Eng 9:41–46Google Scholar
  98. Pasqua G, Avato P, Monacelli B, Santamaria AR, Argentieri MP (2003) Metabolites in cell suspension cultures, calli, and in vitro regenerated organs of Hypericum perforatum cv. Topas. Plant Sci 165:977–982Google Scholar
  99. Prakash G, Srivastava AK (2007) Azadirachtin production in stirred tank reactors by Azadirachta indica suspension culture. Process Biochem 42:93–97Google Scholar
  100. Praveen N, Murthy HN (2010) Establishment of cell suspension cultures of Withania somnifera for the production of withanolide A. Bioresour Technol 101:6735–6739Google Scholar
  101. Praveen N, Murthy HN (2011) Effects of macroelements and nitrogen source on biomass accumulation and withanolide-A production from cell suspension cultures of Withania somnifera (L.) Dunal. Plant Cell Tiss Org Cult 104:119–124Google Scholar
  102. Praveen N, Murthy HN (2012) Synthesis of withanolide A depends on carbon source and medium pH in hairy root cultures of Withania somnifera. Ind Crops Prod 35:241–243Google Scholar
  103. Praveen N, Murthy HN (2013) Withanolide A production form Withania somnifera hairy root cultures with improved growth by altering the concentrations of macro elements and nitrogen source in the medium. Acta Physiol Plant 35:811–816Google Scholar
  104. Praveen N, Naik PM, Manohar SH, Nayeem A, Murthy HN (2009) In vitro regeneration of brahmi shoots using semisolid and liquid cultures and quantitative analysis of bacoside A. Acta Physiol Plant 31:723–728Google Scholar
  105. Praveen N, Murthy HN, Chung IM (2011) Improvement of growth and gymnemic acid production by altering the macro elements concentration and nitrogen source supply in cell suspension cultures of Gymnema sylvestre R. Br Ind Crops Prod 33:282–286Google Scholar
  106. Rajashekaran T, Rajendran I, Ravishankar GA, Venkataraman LV (1991) Influence of nutrient stress on pyrethrin production in cultured cells of pyrethrum (Chrysanthemum cinerariaefolium). Curr Sci 60:705–707Google Scholar
  107. Ramachandra Rao S, Ravishankar GA (2000) Biotransformation of protocatechuic aldehyde and caffeic acid to vanillin and capsaicin in freshly suspended and immobilized cell cultures of Capsicum frutescens. J Biotechnol 7:137–146Google Scholar
  108. Ramachandra Rao S, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153Google Scholar
  109. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress singles on secondary metabolites in plants. Plant Sign Behavior 6:1720–1731Google Scholar
  110. Ramesha BT, Amna T, Ravikanth G, Gunaga RP, Vasudeva R, Ganeshaiah KN, Uma Shaanker R, Khajuria RK, Puri SC, Qazi GN (2008) Prospecting for camptothecines form Nothapodytes nimmoniana in the Western Ghats, South India: identification of high-yielding sources of Camptothecin and new families of camptothecines. J Chromatographic Sci 46:362–368Google Scholar
  111. Ravishankar GA, Sarma KS, Venkataraman LV, Kodyan AK (1988) Effect of nutritional stress on capcinin production in immobilized cell cultures of Capsicum annuum. Curr Sci 57:381–383Google Scholar
  112. Robbins MP, Evans TE, Morries P (1996) The effect of plant growth regulators on growth, morphology and condensed tannin accumulation in transformed root cultures of Lotus corniculatus. Plant Cell Tiss Org Cult 44:219–227Google Scholar
  113. Saenz-Carbonell LA, Maldonado-Mendoza IE, Moreno-Valenzuela O, Ciau-Uitz R, Lopez-Meyer M, Oropeza C, Loyola-Vargas VM (1993) Effect of the medium pH on the release of secondary metabolites from roots of Datura stramonium, Catharanthus roseus, and Tagetes patula cultured in vitro. Appl Biochem Biotechnol 38:257–267Google Scholar
  114. Sahai OP, Shuler ML (1984) Environmental parameters influencing phenolics production by batch cultures of Nicotiana tabacum. Biotechnol Bioeng 26:111–120PubMedGoogle Scholar
  115. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50:199–204Google Scholar
  116. Schlatmann JE, Moreno PRH, Vinke JL, Ten Hoopen HJG, Verpoorte R, Heijnen JJ (1997) Gaseous metabolites and the ajmalicine production rate in high density cell cultures of Catharanthus roseus. Enzyme Microbial Technol 29:107–115Google Scholar
  117. Scragg AH, Cresswell R, Ashton S, York A, Bond P, Fowler MW (1988) Growth and secondary metabolite product formation of a selected Catharanthus roseus cell line. Enz Microbial Technol 10:532–536Google Scholar
  118. Seitz HU, Hinderer W (1988) Anthocyanins. In: Constabel F, Vasil I (eds) Cell culture and somatic cell genetics of plants, vol 5. Academic Press, San Diego, pp 49–76Google Scholar
  119. Shim JJ, Shin JH, Pai T, Chung IS, Lee HJ (1999) Permeabilization of elicited suspension culture of madder (Rubia akane Nakai) cells for release of anthraquinones. Biotechnol Techniques 13:249–252Google Scholar
  120. Shin KS, Murthy HN, Heo JW, Paek KY (2004) Induction of betalain pigmentation in hairy roots of red beat under different radiation sources. Biol Plant 47:149–152Google Scholar
  121. Shohael AM, Ali MB, Yu KW, Hahn EJ, Paek KY (2006) Effect of temperature on secondary metabolites production and antioxidant enzyme activities in Eleutherococcus senticosus somatic embryos. Plant Cell Tiss Org Cult 85:219–228Google Scholar
  122. Shohael AM, Murthy HN, Lee HL, Hahn EJ, Paek KY (2007) Methyl jasmonate induced overproduction of eleutherosides in somatic embryos of Eleutherococcus senticosus cultures in bioreactors. Electron J Biotechnol 10:633–637Google Scholar
  123. Shohael AM, Murthy HN, Lee HL, Hahn EJ, Paek KY (2008) Increased eleutheroside production in Eleutherococcus sessiliflorus embryogenic suspension cultures with methyl jasmonate treatment. Biochem Eng J 38:270–273Google Scholar
  124. Sivakumar G, Yu KW, Paek KY (2005a) Production of biomass and ginsenosides from adventitious roots of Panax ginseng in bioreactor cultures. Eng Life Sci 5:333–342Google Scholar
  125. Sivakumar G, Yu KW, Hahn EJ, Paek KY (2005b) Optimization of organic nutrients for ginseng hairy roots production in large-scale bioreactors. Curr Sci 89:641–649Google Scholar
  126. Srinivasan V, Ryu DD (1993) Improvement of shikonin productivity in Lithospermum erythrorhizon cell cultures by altering carbon and nitrogen feeding strategy. Biotechnol Bioeng 42:793–799PubMedGoogle Scholar
  127. Stafford A, Morris P, Fowler MW (1986) Plant cell biotechnology: a perspective. Enzyme Microb Technol 8:578–587Google Scholar
  128. Tabata M, Mizukami H, Hiraoka N, Konoshima M (1974) Pigment formation in callus cultures of Lithospermum erythrorhizon. Phytochemistry 13:927–932Google Scholar
  129. Terrier B, Courtois D, Henault N, Cuvier A, Bastin M, Aknin A, Dubreuil J, Petiard V (2007) Two new disposable bioreactors for plant cell culture: the wave and undertow bioreactor and the slug bubble bioreactor. Biotechnol Bioeng 96:914–923PubMedGoogle Scholar
  130. Thanh NT, Murthy HN, Yu KW, Hahn EJ, Paek KY (2005) Methyl jasmonate elicitation enhanced synthesis of ginsenoside by cell suspension cultures of Panax ginseng in 5-l balloon type bubble bioreactor. Appl Micorbiol Biotechnol 67:197–201Google Scholar
  131. Thanh NT, Murthy HN, Yu KW, Seung Jeong C, Hahn EJ, Paek KY (2006a) Effect of oxygen supply on cell growth and saponin production in bioreactor cultures of Panax ginseng. J Plant Physiol 163:1337–1341PubMedGoogle Scholar
  132. Thanh NT, Murthy HN, Pandey DM, Yu KW, Hahn EJ, Paek KY (2006b) Effect of carbon dioxide on cell growth and saponin production in suspension cultures of Panax ginseng. Biol Plant 50:752–754Google Scholar
  133. Toivonen L, Laakso S, Rosenqvist H (1992) The effect of temperature on growth, indole alkaloid accumulation and lipid composition of Catharanthus roseus cell suspension cultures. Plant Cell Rep 11:390–394PubMedGoogle Scholar
  134. Vanhala L, Eeva M, Lapinjoki S, Hiltunen R, Oksman-Caldentey KM (1998) Effect of growth regulators on transformed root cultures of Hyoscyamus muticus. J Plant Physiol 153:475–481Google Scholar
  135. Verpoorte R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1:13–25Google Scholar
  136. Wang Y, Weathers PJ (2007) Sugars proportionately affect artemisinin production. Plant Cell Rep 26:1073–1081PubMedGoogle Scholar
  137. Wang SJ, Zhong JJ (1996) A novel centrifugal impeller bioreactor. I. Fluid circulation, mixing, and liquid velocity profiles. Biotechnol Bioeng 51:511–519PubMedGoogle Scholar
  138. Wang C, Wu J, Mei X (2001) Enhanced taxol production and release in Taxus chinensis cultures with selected organic solvents and sucrose feeding. Biotechnol Prog 17:89–94PubMedGoogle Scholar
  139. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action on plant stress response, growth and development. Ann Bot 100:681–687PubMedCentralPubMedGoogle Scholar
  140. Weathers PJ, Bunk G, McCoy MC (2005) The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell Dev Biol Plant 41:47–53Google Scholar
  141. Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233Google Scholar
  142. Wu CH, Murthy HN, Hahn EJ, Paek KY (2007a) Improved production of caffeic derivatives in suspension cultures of Echinacea purpurea by medium replenishment strategy. Arch Pharm Res 30:945–949PubMedGoogle Scholar
  143. Wu CH, Murthy HN, Hahn EJ, Paek KY (2007b) Large scale cultivation of adventitious roots of Echinacea purpurea in airlift bioreactors for the production of chichoric acid, chlorogenic acid and caftaric acid. Biotechnol Lett 29:1179–1182PubMedGoogle Scholar
  144. Wu CH, Popova EV, Hahn EJ, Paek KY (2009) Linoleic acid and α-linolenic fatty acids affect biomass and secondary metabolite production and nutritive properties of Panax ginseng adventitious roots cultured in bioreactors. Biochem Eng J 47:109–115Google Scholar
  145. Yamamoto Y, Mizuguchi R (1982) Selection of a high and stable pigment-producing strain in cultured Euphorbia millii cells. Theor Appl Genet 61:113–116Google Scholar
  146. Yu KW, Gao W, Hahn EJ, Paek KY (2002) Jasmonic acid improving ginsenoside accumulation in adventitious root culture of Panax ginseng C. A. Meyer. Biochem Eng J 11:211–215Google Scholar
  147. Yu KW, Murthy HN, Hahn EJ, Paek KY (2005) Ginsenoside production by hairy root cultures of Panax ginseng: influence of temperature and light quality. Biochem Eng J 23:53–56Google Scholar
  148. Zenk MH (1978) The impact of plant cell cultures on industry. In: Thorpe EA (ed) Frontiers of plant tissue culture. The International Association of Plant Tissue Culture, Calgary, pp 1–13Google Scholar
  149. Zenk MH, El-Shagi H, Schulte U (1975) Anthraquinone production by cell suspension cultures of Morinda citrifolia. Planta Med Suppl 79–101Google Scholar
  150. Zhong JJ (2001) Biochemical engineering of the production of plant-specific secondary metabolites by cell suspension cultures. In: Scheper T (ed) Advances in biochemical engineering/biotechnology, vol 72. Springer, Berlin, pp 1–26Google Scholar
  151. Zhong JJ, Yoshida T (1995) High-density cultivation of Perilla frutescens cell suspensions for anthocyanin production: effects of sucrose concentration and inoculums size. Enz Microbial Technol 17:1073–1079Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Research Center for the Development of Advanced Horticultural TechnologyChungbuk National UniversityCh’ongjuRepublic of Korea
  2. 2.Department of BotanyKarnatak UniversityDharwadIndia
  3. 3.Cheongsol Biotech Co. Ltd., Industry Academic Cooperation Foundation Agribusiness Incubation Center, 205Chungbuk National UniversityCh’ongjuRepublic of Korea

Personalised recommendations