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

Plant Cell, Tissue and Organ Culture

Volumn 118, Issue 1, 2014, Pages 1-16

  Murthy, Hosakatte Niranjana ^a,b   Lee, Eun Jung ^a   Paek, Kee Yoeup ^a  

^a Chungbuk National University   (South Korea)

^b KARNATAK UNIVERSITY   (India)

Author keywords

Bioreactor cultures; Elicitation; Immobilization; Permeabilization; Plant cell cultures; Secondary metabolites

Indexed keywords

AGRICULTURAL CHEMICALS; BIOCHEMISTRY; BIOMASS; BIOMOLECULES; BIOSYNTHESIS; CARBON DIOXIDE; CLONE CELLS; ETHYLENE; FLAVORS; GROWTH KINETICS; NITROGEN; PLANT CELL CULTURE; QUALITY CONTROL; RADIOACTIVE WASTE VITRIFICATION;

BIOMASS ACCUMULATION; BIOREACTOR CULTURES; ELICITATION; PERMEABILIZATION; PLANT GROWTH REGULATORS; POTENTIAL SOURCES; SECONDARY COMPOUNDS; SECONDARY METABOLITES;

METABOLITES;

EID: 84902333640     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-014-0467-7     Document Type: Review

References (151)

1. Anonymous (2013) 2012 Ginseng statistical year book. Ministry of Agriculture, Food and Rural Affairs, Seoul.
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: 482-488.
3. Archambault J, Volesky B, Kurz WGW (1989) Surface immobilization of plant cells. Biotechnol Bioeng 33: 293-299.
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: 475-481.
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: 153-158.
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: 293-999.
7. Banerjee S, Singh S, Rahaman LU (2012) Biotransformation studies using hairy root cultures-a review. Biotechnol Adv 30: 461-468.
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: 1255-1267.
9. Beaumont MD, Knorr D (1987) Effect of immobilizing agents and procedures on viability of cultured celery (Apium graveolens) cells. Biotechnol Lett 9: 377-382.
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 123-135.
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: 163-174.
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: 159-167.
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: 859-868.
14. Brodelius P (1988) Permeabilization of plant cells for release of intracellularly stored products: viability studies. Appl Micorbiol Biotechnol 27: 561-566.
15. Brodelius P, Deus B, Mosbach K, Zenk MH (1979) Immobilized plant cells for the production of natural products. EEBS Lett 103: 93-97.
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: 127-135.
17. Chattopadhyay S, Farkya S, Srivastava AK, Bisaria VS (2002) Bioprocess considerations for production of secondary metabolites. Biotechnol Bioprocess Eng 7: 138-149.
18. Choi JW (1992) In situ berberine separation with immobilized adsorbent in cell suspension culture of Thalictrum rugosum. Korean J Chem Eng 9: 128-134.
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: 187-193.
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: 111-119.
21. Courtois D, Guern J (1980) Temperature response of Catharanthus roseus cells cultivated in liquid medium. Plant Sci Lett 17: 473-482.
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: 1381-1386.
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: 1357-1360.
24. DiCosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13: 425-453.
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 97-175.
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 263-287.
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: 143-146.
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: 99-104.
29. Dornenburg H (2004) Evaluation of immobilization effects on metabolic activities and productivity in plant cells processes. Process Biochem 39: 1369-1375.
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: 35-48.
31. Dornenburg H, Knorr D (1995) Strategies for improvement of secondary metabolite production in plant cell cultures. Enz Microb Technol 17: 674-684.
32. Dougall DK (1980) Nutrition and metabolism. In: Staba EJ (ed) Plant tissue culture as a source of biochemicals. CRC Press, Boca Raton, pp 21-58.
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 163-199.
34. Eibl R, Werner S, Eibl D (2010) Bag bioreactor based on wave induced motion: characteristics and applications. Adv Biochem Eng Biotechnol 115: 55-87.
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 139-166.
36. Folk LR, Doran PM (1996) Influence of inoculum morphology on growth of hairy roots and production of tropane alkaloids. Biotechnol Lett 18: 1099-1104.
37. Fulzele DP, Heble MR, Rao PS (1995) Production of terpenoids from Artemisia annua L. plantlet cultures in bioreactor. J Biotechnol 40: 139-143.
38. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50: 151-158.
39. Gao JW, Lee JM (1992) Effect of oxygen supply on the suspension culture of genetically modified tobacco cells. Biotechnol Prog 8: 285-290.
40. Georgiev MI, Weber J, Maciuk A (2009) Bioprocessing of plant cell cultures for mass production of targeted compounds. Appl Microbiol Biotechnol 83: 809-823.
41. Giri A, Narasu ML (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18: 1-22.
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: 175-199.
43. Gundlach H, Zenk MH (1998) Biological activity and biosynthesis of pentacyclic oxylipins: the linoleic acid pathway. Phytochemistry 47: 527-537.
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: 1205-1211.
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: 702-706.
46. Haldimann D, Brodelius P (1987) Redirecting cellular metabolism by immobilization of cultured plant cells: a model study with Coffea arabica. Phytochemistry 26: 1431-1434.
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: 585-593.
48. Ilieva M, Pavlov A (1996) Rosamarinic acid by Lavandula vera MM cell suspension: phosphorous effect. Biotechnol Lett 18: 913-916.
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: 288-291.
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: 219-222.
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: 2271-2273.
52. Kanokwaree K, Doran PM (1997) Effect of inoculums morphology on growth of Atropa belladonna hairy root in shake flaks. J Ferment Bioeng 84: 378-381.
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: 97-105.
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: 331-339.
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: 1619-1622.
56. Knorr D, Teutonico RA (1986) Chitoson immobilization and permeabilization of Amaranthus tricolor cells. J Agric Food Chem 34: 96-97.
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: 496-499.
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: 472-477.
59. Kreuzaler F, Hahlbrock K (1973) Flavonoid glycosides from illuminated cell suspension cultures of Petroselinum hortense. Phytochemistry 12: 1149-1152.
60. Kutney JP (1993) Plant cell culture combined with chemistry: a powerful route to complex natural products. Acc Chem Res 26: 559-566.
61. Kwon IC, Yoo YJ, Lee JH, Hyun JO (1998) Enhancement of taxol production by in situ recovery of product. Process Biochem 33: 701-707.
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: 61-71.
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: 117-121.
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: 538-542.
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: 1147-1152.
66. Lindsey K, Yeoman MM (1984) The synthetic potential of immobilized cells of Capsicum frutescens Mill. cv. annuum. Planta 162: 495-501.
67. Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18: 100-127.
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: 69-74.
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: 927-929.
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: 581-585.
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 75-108.
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: 61-69.
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: 967-969.
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: 327-333.
75. McDonald KA, Jackman AP (1989) Bioreactor studies of growth and nutrient utilization in alfalfa suspension cultures. Plant Cell Rep 8: 455-458.
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: 55-58.
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: 442-449.
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: 42-47.
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): 702-705.
81. Morris P (1986) Regulation of product synthesis in cell cultures of Catharanthus roseus. Effect of culture temperature. Plant Cell Rep 5: 427-429.
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: 13-16.
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: 627-630.
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: 241-245.
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: 85-154.
86. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-479.
87. Murthy HN, Hahn EJ, Paek KY (2008a) Adventitious root and secondary metabolism. Chin J Biotechnol 24: 711-716.
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: 975-981.
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: 537-540.
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: 235-239.
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: 1553-1557.
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: 387-395.
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: 695-699.
94. Nigam SC, Saihpush AR, Wang HY (1990) Analysis of bioproduct separation using gel-enclosed adsorbents. AIChE J 36: 1239-1248.
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: 319-326.
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: 1052-1057.
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: 41-46.
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: 977-982.
99. Prakash G, Srivastava AK (2007) Azadirachtin production in stirred tank reactors by Azadirachta indica suspension culture. Process Biochem 42: 93-97.
100. Praveen N, Murthy HN (2010) Establishment of cell suspension cultures of Withania somnifera for the production of withanolide A. Bioresour Technol 101: 6735-6739.
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: 119-124.
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: 241-243.
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: 811-816.
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: 723-728.
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: 282-286.
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: 705-707.
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: 137-146.
108. Ramachandra Rao S, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20: 101-153.
109. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress singles on secondary metabolites in plants. Plant Sign Behavior 6: 1720-1731.
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: 362-368.
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: 381-383.
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: 219-227.
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: 257-267.
114. Sahai OP, Shuler ML (1984) Environmental parameters influencing phenolics production by batch cultures of Nicotiana tabacum. Biotechnol Bioeng 26: 111-120.
115. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50: 199-204.
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: 107-115.
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: 532-536.
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 49-76.
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: 249-252.
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: 149-152.
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: 219-228.
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: 633-637.
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: 270-273.
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: 333-342.
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: 641-649.
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: 793-799.
127. Stafford A, Morris P, Fowler MW (1986) Plant cell biotechnology: a perspective. Enzyme Microb Technol 8: 578-587.
128. Tabata M, Mizukami H, Hiraoka N, Konoshima M (1974) Pigment formation in callus cultures of Lithospermum erythrorhizon. Phytochemistry 13: 927-932.
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: 914-923.
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: 197-201.
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: 1337-1341.
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: 752-754.
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: 390-394.
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: 475-481.
135. Verpoorte R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1: 13-25.
136. Wang Y, Weathers PJ (2007) Sugars proportionately affect artemisinin production. Plant Cell Rep 26: 1073-1081.
137. Wang SJ, Zhong JJ (1996) A novel centrifugal impeller bioreactor. I. Fluid circulation, mixing, and liquid velocity profiles. Biotechnol Bioeng 51: 511-519.
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: 89-94.
139. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action on plant stress response, growth and development. Ann Bot 100: 681-687.
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: 47-53.
141. Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75: 225-233.
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: 945-949.
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: 1179-1182.
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: 109-115.
145. Yamamoto Y, Mizuguchi R (1982) Selection of a high and stable pigment-producing strain in cultured Euphorbia millii cells. Theor Appl Genet 61: 113-116.
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: 211-215.
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: 53-56.
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 1-13.
149. Zenk MH, El-Shagi H, Schulte U (1975) Anthraquinone production by cell suspension cultures of Morinda citrifolia. Planta Med Suppl 79-101.
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 1-26.
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: 1073-1079.