Skip to main content
SpringerLink
Log in

Bioprocessing technology for plant cell suspension cultures

  • Patents and Literature Review
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Considering various forms of in vitro plant tissue cultures, cell suspension culture is most amenable to large-scale production of natural compounds, owing primarily to its superior culture homogeneity. This fact has already been demonstrated in several largescale applications, including the commercial shikonin process. The scope of this work is to review the state of the art in bioprocessing technologies pertinent to the secondary metabolite production from suspension cultures of callus cells. In the first part of the review, plant cell physiology relevant to bioprocess design is considered. This is followed by an in-depth discussion on the bioreactor design and operation and its effect on plant cell suspension cultures. Finally, recent commercial exploitation and development are summarized. Following the review, related patents and literature are listed.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Fowler, M. W. (1986), Industrial applications of plant cell culture, inPlant Cell Culture Technology, Yeoman, M. M., ed., Blackwell, Oxford, pp. 202–207.

    Google Scholar 

  2. Fujita, Y. (1988), Industrial production of shikonin and berberine, inApplication of Plant Cell and Tissue Culture, Bock, G. and Marsh, J., eds., Wiley, New York, pp. 228–238.

    Chapter  Google Scholar 

  3. Ushiyama, K. (1991), Large scale culture of ginseng, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 92–98.

    Google Scholar 

  4. Doran, P. M. (1993), Design of reactors for plant cells and organs.Adv. Biochem. Eng. Biotechnol. 48, 113–168.

    Google Scholar 

  5. Payne, G. F., Bringi, V., Prince, C. L., and Shuler, M. L. (1992),Plant Cell and Tissue Culture in Liquid Systems, Hanser Publishers, Munich.

    Google Scholar 

  6. Becker, H. and Sauerwein, M. (1990), Manipulating the biosynthetic capacity of plant cell cultures. InSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 43–58.

    Google Scholar 

  7. Dixon, R. A. and Lamb, C. J. (1990), Regulation of secondary metabolism at the biochemical and genetic levels, inSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 103–118.

    Google Scholar 

  8. Yamada, Y., Hashimoto, T., Endo, T., Yukimune, Y., Kohno, J., Hamaguchi, N., and Drager, B. (1990), Biochemistry of alkaloid productionin vitro, inSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 227–242.

    Google Scholar 

  9. Cresswell, R. C., Fowler, M. W., Stafford, A., and Stephan-Sarkissian, G. (1989), Inputs and outputs: primary substrates and secondary metabolism, inPrimary and Secondary Metabolism of Plant Cell Cultures II, Kurz, W. G. W., ed., Springer-Verlag, Berlin, pp. 14–26.

    Google Scholar 

  10. Amino, S. and Tazawa, M. (1988), Uptake and utilization of sugars in cultured rice cells.Plant Cell Physiol. 29, 483–487.

    CAS  Google Scholar 

  11. Masuda, H., Takahashi, T., and Sugawara, S. (1988), Acid and alkaline intases in suspension cultures of sugar beet cells.Plant Physiol. 86, 312–317.

    CAS  Google Scholar 

  12. Kanabus, J., Bressan, R. A., and Carpita, N. C. (1986), Carbon assimilation in carrot cells in liquid culture.Plant physiol. 82, 363–368.

    CAS  Google Scholar 

  13. Su, W. W., Asali, E. C., and Humphrey, A. E. (1993),Anchusa officinalis: production of rosmarinic acid in perfusion cell cultures, inBiotechnology in Agriculture and Forestry, vol. 26, Bajaj, Y. P. S., ed., Springer-Verlag, Berlin, pp. 1–20.

    Google Scholar 

  14. Thayer, S. S. and Conn, E. E. (1981), Subcellular localization of dhurrin β-glycosidase and hydroxynitrile lyase in the mesophyll cells ofSorghum leaf blades.Plant Physiol. 67, 617–622.

    CAS  Google Scholar 

  15. DiCosmo, F. and Towers, G. (1984), Stress and secondary metabolism in cultured plant, inRecent Advances in Phytochemistry—Phytochemical Adaptations to Stress, Timmermann, B., Steelink, C., and Loewus, F., eds., Plenum, New York, pp. 97–157.

    Google Scholar 

  16. Do, C. and Cormier, F. (1990), Accumulation of anthocyanins enhanced by a high osmotic potential in grape cell suspensions.Plant Cell. Rep. 9, 143–146.

    Article  CAS  Google Scholar 

  17. Su, W. W. and Humphrey, A. E. (1990), Production of rosmarinic acid in the high density perfusion culture ofAnchusa officinalis using a high sugar medium.Biotechnol. Lett. 12, 793–798.

    Article  CAS  Google Scholar 

  18. De-Eknamkul, W. and Ellis, B. E. (1985), Effects of macronutrients on growth and rosmarinic acid formation in cell suspension cultures ofAnchusa officinalis.Plant Cell Rep. 4, 46–49.

    Article  CAS  Google Scholar 

  19. Dixon, R. A. (1985), Isolation and maintenance of callus and cell suspension cultures, inPlant Cell Cultures: A Practical Approach, Dixon, R. A., ed., IRL Press, Oxford, pp. 1–20.

    Google Scholar 

  20. Miflin, B. J. and Lea, P. J. (1977), Amino acid metabolism.Annu. Rev. Plant Physiol. 28, 299–329.

    Article  CAS  Google Scholar 

  21. Tabata, M. and Fujita, Y. (1985), Production of shikonin by plant cell cultures, inBiotechnology in Plant Science, Zeitlin, M., Day, P., and Hollaender, A., eds., Academic, New York, pp. 207–218.

    Google Scholar 

  22. Hirasuna, T. J., Shuler, M. L., Lackney, V. K., Spanswick, R. M. (1991), Enhanced anthocyanin production in grape cell cultures.Plant Sci. 78, 107–120.

    Article  CAS  Google Scholar 

  23. Brodelius, P. E. and Vogel, H. J. (1985), A phosphorus-31 nuclear magnetic resonance study of phosphate uptake and storage in culturedCatharanthus roseus andDaucus carota plant cells.Biol. Chem. 260, 3556–3560.

    CAS  Google Scholar 

  24. Ashihara, H. and Tokoro, T. (1985), Metabolic fate of inorganic phosphate absorbed by suspension cultured cells ofCatharanthus roseus.J. Plant Physiol. 118, 227–235.

    CAS  Google Scholar 

  25. Ashihara, H. and Ukaji, T. (1986), Inorganic phosphate absorption and its effect on the adenosine 5t’-triphosphate level in suspension cultured cells ofCatharanthus roseus.J. Plant Physiol. 124, 77–85.

    CAS  Google Scholar 

  26. Schiel, O., Jarchow-Redecker, K., Piehl, G-W., Lehmann, J., and Berlin, J. (1984), Increased formation of cinnamoyl putrescines by fedbatch fermentation of cell suspension cultures ofNicotiana tabacum.Plant Cell Rep. 3, 18–20.

    Article  CAS  Google Scholar 

  27. Komamine, A., Sakuta, M., Hirose, M., Hirano, H., Takagi, T., Kakegawa, K., and Ozeki, Y. (1989), Regulation of secondary metabolism in relation to growth and differentiation, inPrimary and Secondary Metabolism of Plant Cell Cultures II, Kurz, W. G.W., ed., Springer-Verlag, Berlin, pp. 49–52.

    Google Scholar 

  28. Wink, M. (1990), Physiology of secondary product formation in plants, inSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 23–42.

    Google Scholar 

  29. Ozeki, Y., Matsuoka, M., Ohashi, Y., Kano-Murakami, Y., Yamamoto, N., and Tanaka, Y. (1989), Induction and suppression of anthocyanin synthesis in carrot suspension cell cultures regulated by 2,4-D, inPrimary and Secondary Metabolism of Plant Cell Cultures II, Kurz, W. G. W., ed., SpringerVerlag, Berlin, pp. 102–109.

    Google Scholar 

  30. Brodelius, P. E. (1990), Transport and accumulation of secondary metabolites, inProgress in Plant Cellular and Molecular Biology, Nijkamp, H. J. J., van der Plas, L. H. W., and van Aartrijk, J., eds., Kluwer, Dordrecht, Netherlands, pp. 567–576.

    Google Scholar 

  31. Renaudin, J. P. and Guern, J. (1990), Transport and vacuolar storage of secondary metabolites in plant cell cultures, inSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 58–78.

    Google Scholar 

  32. Yamamoto, H., Suzuki, M., Suga, Y., Fukui, H., and Tabata, M. (1987), Participation of an active transport system in berberine-secreting cultured cells ofThalictrum minus. Plant Cell Rep. 6, 356–359.

    Article  CAS  Google Scholar 

  33. Guern, J., Renaudin, J. P., and Brown, S. C. (1987), The compartmentation of secondary metabolites in plant cell cultures, inCell Culture and Somatic Cell Genetics of Plants, vol. 4, Constabel, F., and Vasil, I. K., eds., Academic Press, San Diego, pp. 43–76.

    Google Scholar 

  34. Parr, A. J., Robins, R. J., and Rhodes, M. J. C. (1986), Alkaloid transport inCinchona sp. cell cultures.Physiologie V’eg’etale 24, 419–429.

    CAS  Google Scholar 

  35. McCaskill, D. G., Martin, D. L., and Scott, A.I. (1988), Characterization of alkaloid uptake byCatharantus roseus (L.) G. Don protoplasts.Plant Physiol. 87, 402–408.

    CAS  Google Scholar 

  36. Bouyssou, H., Pareilleux, A., and Marigo, G. (1987), The role of pH gradients across theplasmalemma ofCatharanthus roseus and its involvement in the release of alkaloids.Plant Cell Tissue Organ Culture 10, 91–99.

    Article  CAS  Google Scholar 

  37. Tsukada, M., and Tabata, M. (1984), Intracellular localization and secretion of naphtoquinone pigments in cell cultures ofLithospermum erythrorhizon.Planta Med. 50, 238–240.

    Article  Google Scholar 

  38. Barz, W., Deimen, A., Drager, B., Jaques, U., Otto, Ch., Super, E., and Upmeier, B. (1990), Turnover and storage of secondary products in cell cultures, inSecondary Products from Plant Tissue Culture, Charlwood, B. V. and Rhodes, M. J. C., eds., Oxford University Press, New York, pp. 79–102.

    Google Scholar 

  39. Eilert, U. (1987), Elicitation: methodology and aspects of application, inCell Culture and Somatic Cell Genetics of Plants, vol. 4, Constabel, F. and Vasil, I. K., eds., Academic, San Diego, pp. 153–196.

    Google Scholar 

  40. DiCosmo, F. and Misawa, M. (1985), Eliciting secondary metabolism in plant cell cultures.Trends Biotechnol. 3, 318–322.

    Article  CAS  Google Scholar 

  41. Boller, T. (1983), Ethylene-induced biochemical defenses against pathogens, inPlant Growth Substances, 1982, Wareing, P. F., ed., Academic, London, pp. 303–312.

    Google Scholar 

  42. Kohle, H., Jeblick, W., Poten, F., Blaschek, W., and Kauss, H. (1985), Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process.Plant Physiol. 77, 544–551.

    Google Scholar 

  43. Byun, S. Y. (1989), Studies on elicitation andin situ recovery of alkaloids in suspension cultures of California poppy. Ph.D. Thesis, Rutgers, The State University of New Jersey, NJ.

    Google Scholar 

  44. Barz, W., Daniel, S., Hinderer, W., Jaques, U., Kessmann, H., Koster, J., and Tiemann, K. (1988), Elicitation and metabolism of phytoalexins in plant cell cultures, inPlant Cell Biotechnology, NATO ASI Series, Vol. H18, Pais, M. S. S., et al., eds., Springer-Verlag, Berlin, pp. 211–230.

    Google Scholar 

  45. Hashimoto, T., and Azechi, S. (1988), Bioreactors for the large-scale culture of plant cells, inBiotechnology in Agriculture and Forestry, vol. 4, Bajaj, Y. P. S., ed., pp. 104–122.

  46. Kargi, F. and Rosenberg, M. Z. (1987), Plant cell bioreactors: present status and future trends.Biotechnol. Prog. 3, 1–8.

    CAS  Google Scholar 

  47. Payne, G. F., Shuler, M. L., and Brodelius, P. (1987), Large scale plant cell culture, inLarge Scale Cell Culture Technology, Lydersen, B. K., ed., Hanser, Munich, pp. 193–230.

    Google Scholar 

  48. Schuler, M. L. and Hallsby, G. A. (1985), Bioreactor considerations for chemical production from plant cell cultures, inBiotechnology in Plant Science, Zeitlin, M., Day, P., and Hollaender, A., eds., Academic, New York, pp. 191–206.

    Google Scholar 

  49. Aoyagi, H., Yokoi, H., and Tanaka, H. (1992), Measurement of fresh and dry densities of suspended plant cells and estimation of their water content.J. Ferment. Bioeng. 73, 490–496.

    Article  CAS  Google Scholar 

  50. Kato, A., Kawazoe, S., and Soh, Y. (1978), Viscosity of the broth of tobacco cells in suspension culture.J. Ferment. Technol. 56, 224–228.

    Google Scholar 

  51. Scragg, A. H., Allan, E. J., Bond, P. A., and Smart, N. J. (1986), Rheological properties of plant cell suspension cultures, inSecondary metabolism in plant cell cultures, Morris, P., Scragg, A. H., Stafford, A., and Fowler, M. W., eds., Cambridge University Press, Cambridge, UK, pp. 178–194.

    Google Scholar 

  52. Tanaka, H. (1981), Technological problems in cultivation of plant cells at high density.Biotechnol. Bioeng. 23, 1203–1218.

    Article  Google Scholar 

  53. Zhong, J-J., Seki, T., Kinoshita, S-I., and Yoshida, T. (1992), Rheological characteristics of cell suspension and cell culture ofPerilla ftutescens.Biotechnol. Bioeng. 40, 1258–1262.

    Article  Google Scholar 

  54. Bailey, J. E. and Ollis, D. F. (1986),Biochemical Engineering Fundamentals, 2nd ed., McGraw-Hill, New York.

    Google Scholar 

  55. Ballica, R. and Ryu, D. D. Y. (1993), Effects of rheological properties and mass transfer on plant cell bioreactor performance: production of tropane alkaloids.Biotechnol. Bioeng. 42, 1181–1189.

    Article  CAS  Google Scholar 

  56. Meijer, J. J., ten Hoopen, H. J. G., Luyben, K. Ch. A. M., and Libbenga, K. R. (1993), Effects of hydrodynamic stress on cultured plant cells: A literature survey.Enzyme Microb. Technol. 15, 234–238.

    Article  CAS  Google Scholar 

  57. Tanaka, H. (1987), Large-scale cultivation of plant cells at high density: a review.Proc. Biochem. August, 106–113.

  58. Hulst, A.C., Meyer, M. M. T., Breteler, H., and Tramper, J. (1989), Effect of aggregate size in cell cultures ofTagetes patula on thiophene production and cell growth.Appl. Microbiol. Biotechnol. 30, 18–25.

    Article  CAS  Google Scholar 

  59. Sahai, O. P. and Shuler, M. L. (1982), On the nonideality of chemostat operation using plant cell suspension cultures.Can. J. Bot. 60, 692–700.

    Google Scholar 

  60. De-Eknamkul, W. and Ellis, B. E. (1985) Effect of auxins and cytokinins on growth and rosmarinic acid formation in cell suspension cultures ofAnchusa officinalis.Plant Cell Rep. 4, 50–53.

    Article  CAS  Google Scholar 

  61. Su, W. W., Lei, F., and Su, L. Y. (1993), Perfusion strategy for rosmarinic acid production byAnchusa officinalis. Biotechnol.Bioeng. 42, 884–890.

    Article  CAS  Google Scholar 

  62. Bond, P. A., Fowler, M. W., and Scragg, A. H. (1988), Growth ofCatharanthus roseus cell suspensions in bioreactors: on-line analysis of oxygen and carbon dioxide levels in inlet and outlet gas streams.Biotechnol. Lett. 10, 713–718.

    Article  CAS  Google Scholar 

  63. Dalton, C. C. (1978), The culture of plant cells in fermenters.Heliosynthase et Aquaculture seminar de Martiques, C.N.R.S., pp. 1–11.

  64. Piehl, G-W., Berlin, J., Mollenschott, C., and Lehmann, J. (1988), Growth and alkaloid production of a cell suspension culture ofThalictrum rugosum in shake flasks and membrane-stirrer reactors with bubble free aeration.Appl. Microbiol. Biotechnol. 29, 456–461.

    Article  CAS  Google Scholar 

  65. Howell, J. A., Chi, C. T., and Pawlowsky, U. (1972), Effect of wall growth on scale-up problems and dynamic operating characteristics of the biological reactor.Biotechnol. Bioeng. 14, 253–265.

    Article  CAS  Google Scholar 

  66. Kim, D., Pedersen, H., and Chin, C. K. (1991), Cultivation ofThalictrum rugosum cell suspension in an improved air-lift bioreactor: stimulatory effect of carbon dioxide and ethylene on alkaloid production.Biotechnol. Bioeng. 38, 331–339.

    Article  CAS  Google Scholar 

  67. Sahai, O. P. and Shuler, M. L. (1984), Multistage Continuous culture to examine secondary metabolite formation in plant cells: phenolics fromNicotiana tabacum.Biotechnol. Bioeng. 26, 27–36.

    Article  CAS  Google Scholar 

  68. Davis, R. H. and Acrivos, A. (1985), Sedimentation of noncolloidal particles at low Reynolds numbers.Ann. Rev. Fluid Mech. 17, 91–118.

    Article  Google Scholar 

  69. Burrman, C., Resoort, G., and Plaschkes, A. (1986), Scaling-up rules for solids suspension in stirred vessels.Chem. Eng. Sci. 41, 2865.

    Article  Google Scholar 

  70. Galindo, E. and Nienow, A. W. (1992), Mixing of highly viscous simulated xanthan fermentation broths with the Lightnin A-315 impeller.Biotechnol. Prog. 8, 233–239.

    Article  CAS  Google Scholar 

  71. Nienow, A. W. (1992), New agitators v Rushton turbines: a critical comparison of transport phenomena, inHarnessing Biotechnology for the 21st Century, Ladisch, M. R. and Bose, A., eds., American Chemical Society, Washington, DC, pp. 193–196.

    Google Scholar 

  72. Nienow, A. W. (1985), The dispersion of solids in liquids, inMixing of Liquids by Mechanical Agitation, Ulbrecht, J. J. and Patterson, G. K., eds., Gordon and Breach, New York, pp. 273–308.

    Google Scholar 

  73. Prokop, A. and Rosenberg, M. Z. (1989), Bioreactor for mammalian cell culture,Adv. Biochem. Eng. Biotechnol. 39, 29–71.

    CAS  Google Scholar 

  74. Jolicoeur, M., Chavarie, C., Carreau, P. J., and Archambault, J. (1992), Development of a helical-ribbon impeller bioreactor for high-density plant cell suspension culture.Biotechnol. Bioeng. 39, 511–521.

    Article  CAS  Google Scholar 

  75. Ulbrich, B., Wiesner, W., and Arens, H. (1985), Large scale production of rosmarinic acid from plant cell cultures ofColeus blumei Benth, inPrimary and Secondary Metabolism of Plant Cell Cultures, Neumann, K.-H., Barz, W., and Reinhard, E., eds., Springer, Berlin, pp. 298–303.

    Google Scholar 

  76. Ulbrich, B. (1986), Nutrition and environment of plant cells in bioreactors, inProceedings of the Seventh Conference on Global Impacts of Applied Microbiology: Symposia on Alcohol Fermentation and Plant Cell Culture, Korhola, M., Tuompo, H., and Kauppinen, V., eds., Foundation for Biotechnical and Industrial Fermentation Research, Helsinki, pp. 147–164.

    Google Scholar 

  77. Yokoi, H., Koga, J., Yamamura, K., Seike, Y., and Tanaka, H. (1993), High density cultivation of plant cells in a new aeration-agitation type fermentor, Maxblend fermenter.J. Ferment. Bioeng. 75, 48–52.

    Article  CAS  Google Scholar 

  78. Hooker, B. S. and Lee, J. M. (1990), Cultivation of plant cells in a stirred vessel: effect of impeller design.Biotechnol. Bioeng. 35, 296–304.

    Article  CAS  Google Scholar 

  79. Matsubara, K., Kitani, S., Yoshioka, T., Morimoto, T., and Fujita, Y. (1989), High density culture ofCoptis japonica cells increases berberine production.J. Chem. Tech. Biotechnol. 46, 61–69.

    CAS  Google Scholar 

  80. Tanaka, H. (1982), Oxygen transfer in broths of plant cells at high density.Biotechnol. Bioeng. 24, 425–442.

    Article  CAS  Google Scholar 

  81. Gbewonyo, K., Dimasi, D., and Buckland, B. C. (1987), Characterization of oxygen transfer and power absorption of hydrofoil impellers in viscous mycelial fermentations, inBiotechnology Processes: Scale-up and Mixing, Ho, C. S. and Oldshue, J. Y., eds., AIChE, New York, pp. 128–134.

    Google Scholar 

  82. Chisti, M. Y. (1989),Airlift bioreactors. Elsevier Applied Science, London, UK.

    Google Scholar 

  83. Wagner, F. and Vogelmann, H. (1977), Cultivation of plant tissue cultures in bioreactors and formation of secondary metabolites, inPlant Tissue Culture and Its Biotechnological Application, Barz, W., Reinhard, M. H., and Zenk, M. H., eds., Springer-Verlag, Berlin, pp. 245–255.

    Google Scholar 

  84. Shibasaki, N., Hirose, K., Yonemoto, T., and Tadaki, T. (1992), Suspension culture ofNicotiana tabacum cells in a rotary-drum bioreactor.J. Chem. Tech. Biotechnol. 53, 359–363.

    CAS  Google Scholar 

  85. Takahashi, S. and Fujita, Y. (1991), Production of shikonin, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 72–78.

    Google Scholar 

  86. Tanaka, H., Nishijima, F., Suwam, M., and Iwamoto, T. (1983), Rotating drum fermenter for plant cell suspension cultures.Biotechnol. Bioeng. 25, 2359–2370.

    Article  CAS  Google Scholar 

  87. Drapeau, D., Blanch, H. W., and Wilke, C. R. (1986), Growth kinetics ofDioscorea deltoidea andCatharanthus roseus in batch culture.Biotechnol. Bioeng. 28, 1555–1563.

    Article  CAS  Google Scholar 

  88. Hong, Y. C., Labuza, T. P., and Harlander, S. K. (1989), Growth kinetics of strawberry cell suspension cultures in shake flask, airlift, stirred-jar and roller bottle bioreactors.Biotechnol. Prog. 5, 137–143.

    Article  Google Scholar 

  89. De-Eknamkul, W. and Ellis, B. E. (1984), Rosmarinic acid production and garowth characteristicsof Anchusa officinalis cell suspension cultures.Planta Med. 51, 346–350.

    Article  Google Scholar 

  90. Kessell, R. H. J. and Carr, A. H. (1972), The effect of dissolved oxygen concentration on growth and differentiation of carrot (Daucus carota) tissue.J. Exp. Bot. 23, 996–1007.

    Article  CAS  Google Scholar 

  91. Pareilleux, A. and Vinas, R. A. (1983), Influence of the aeration rate on the growth yield in suspension cultures ofCatharanthus roseus.J. Ferment. Technol. 61, 429–433.

    CAS  Google Scholar 

  92. Schlatmann, J. E., Nuutila, A. M., van Gulik, W.M., ten Hoopen, H. J. G., Verpoorte, R., and Heijnen, J. J. (1993), Scaleup of ajmalicine production by plant cell cultures ofCatharanthus roseus.Biotechnol. Bioeng. 41, 253–262.

    Article  CAS  Google Scholar 

  93. Yang, J-D. and Wang, N. S. (1992), Cell activation in the presence of sparging and mechanical agitation.Biotechnol. Bioeng. 40, 806–816.

    Article  CAS  Google Scholar 

  94. Aunins, J. G. and Henzler, H-J. (1993), Aeration in cell culture bioreactors, inBiotechnology, vol. 3, Bioprocessing, Rehm, H.-J., Reed, G., Puhler, A., and Sadler, P., eds., VCH, Weinheim, Germany, pp. 219–282.

    Google Scholar 

  95. Su, W. W. and Humphrey, A. E. (1991), Production of rosmarinic acid from perfusion culture ofAnchusa officinalis in a membrane aerated bioreactor.Biotechnol. Lett. 13, 889–892.

    Article  CAS  Google Scholar 

  96. Su, W. W. and Humphrey, A. E. (1992), Production of plant secondary metabolites from high density perfusion cultures, inBiochemical Engineering for 2001, Furusaki, S., Endo, I., and Matsuno, R., eds., Springer-Verlag, Tokyo, pp. 266–269.

    Google Scholar 

  97. Su, W. W., Caram, H. S., and Humphrey, A. E. (1992), Optimal design of the tubular microporous membrane aerator for shear sensitive cell cultures.Biotechnol. Prog. 8, 19–24.

    Article  CAS  Google Scholar 

  98. Pareilleux, A. (1988), The large scale cultivation of plant cells, inPlant Cell Biotechnology, NATO ASI Series, Vol. H18, Pais, M. S. S., et. al., eds., Springer-Verlag, Berlin, pp. 313–328.

    Google Scholar 

  99. Smart, N. J. and Fowler, M. W. (1984), An air-lift column bioreactor suitable for large-scale cultivation of plant cell suspensions.J. Exp. Bot. 35, 531–537.

    Article  Google Scholar 

  100. Wilson, G. (1980), Continuous culture of plant cells using the chemostat principle.Adv. Biochem. Eng. Biotechnol. 16, 1–25.

    Google Scholar 

  101. Hooker, B. S., Lee, J. M., and An, G. (1989), Response of plant tissue culture to a high shear environment.Enz. Microb. Technol. 11, 484–490.

    Article  CAS  Google Scholar 

  102. Markx, G. H., ten Hoopen, H. J. G., Meijer, J. J., and Vinke, K. L. (1991), Dielectric spectroscopy as a novel and convenient tool for the study of the shear sensitivity of plant cells in suspension culture.J. Biotechnol. 19, 145–158.

    Article  CAS  Google Scholar 

  103. Metzner, A. B. and Otto, R. E. (1957), Agitation of non-Newtonian fluids.AIChE J. 3, 3–10.

    Article  CAS  Google Scholar 

  104. Nishikawa, M., Kato, H., and Hashimoto, K. (1977), Heat transfer in aerated tower filled with non-Newtonian liquid.Ind. Eng. Chem. Proc. Des. Devp. 16, 133–137.

    Article  CAS  Google Scholar 

  105. Robertson, B. and Ulbrecht, J. (1987), Measurement of shear rate on an agitator in a fermentation broth, inBiotechnology Processes Scale-up and Mixing, Ho, C. S. and Oldshue, J. Y., eds., AIChE, New York, pp. 31–35.

    Google Scholar 

  106. Wichterle, K., Zak, L., and Mitschka, P. (1985) Shear stresses on the walls of agitated vessels.Chem. Eng. Commun. 32, 289–305.

    Article  CAS  Google Scholar 

  107. Kim, I-H., Cho, M. H., and Wang, S. S. (1993), Measurement of hydrodynamic shear by using a dissolved oxygen probe.Biotechnol. Bioeng. 41, 296–302.

    Article  CAS  Google Scholar 

  108. Croughan, M. S. and Wang, D. I. C. (1991), Hydrodynamic effects on animal cells in microcarrier bioreactors, inAnimal cell Bioreactors, Ho, C. S. and Wang, D. I. C., eds., Butterworth-Heinemann, Boston, pp. 213–252.

    Google Scholar 

  109. Cherry, R. S. and Huile, C. T. (1992), Cell death in the thin films of bursting bubbles.Biotechnol. Prog. 8, 11–18.

    Article  CAS  Google Scholar 

  110. Moreno, P. R. H., Schlatmann, J. E., Heijden, R. V. D., Gulik, W. M. V., Hoopen, H. J. G., Verpoorte, R., et al. (1993), Induction of ajmalicine formation and related enzyme activities inCatharanthus roseus cells; effect of inoculum density.Appl. Microbial. Biotechnol. 39, 42–47.

    CAS  Google Scholar 

  111. Su, W. W. and Lei, F. (1993), Rosmarinic acid production in perfusedAnchusa officinalis culture: effect of inoculum size.Biotechnol. Lett. 15, 1035–1038.

    Article  CAS  Google Scholar 

  112. Kreis, W. and Reinhard, E. (1989), The production of secondary metabolites by plant cells cultivated in bioreactors.Planta Med. 55, 409–416.

    Article  CAS  Google Scholar 

  113. Lipsky, A.Kh. (1992), Problems of optimization of plant cell culture processes.J. Biotechnol. 26, 83–97.

    Article  Google Scholar 

  114. Kobayashi, Y., Akita, M., Sakamoto, K., Liu, H., Shigeoka, T., Koyano, T., Kawamura, M., and Furuya, T. (1993), Large-scale production of anthocyanin byAralia cordata cell suspension cultures.Appl. Microb. Biotechnol. 40, 215–218.

    Article  CAS  Google Scholar 

  115. Kim, D. I., Cho, G. H., Pedersen, H., and Chin, C. K. (1991), A hybrid bioreactor for high density cultivation of plant cell suspensions.Appl. Microbiol. Biotechnol. 34, 726–729.

    Article  CAS  Google Scholar 

  116. Batt, B. C., Davis, R. H., and Kompala, D. S. (1990), Inclined sedimentation for selective retention of viable hybridomas in a continuous suspension bioreactor.Biotechnol. Prog. 6, 458–464.

    Article  CAS  Google Scholar 

  117. Davison, B. H., San, K. Y., and Stephanopoulos, G. (1985), Stable competitive coexistence in a continuous fermenter with size-selective properties.Biotechnol. Prog. 1, 260–268.

    Article  CAS  Google Scholar 

  118. Hamamoto, K., Ishimaru, K., and Tokashiki, M. (1989), Perfusion culture of hybridoma cells using a centrifuge to separate cells from culture mixture.J. Ferment. Bioeng. 67, 190–194.

    Article  Google Scholar 

  119. Pareilleux, A. and Vinas, R. A. (1984), A study on the alkaloid production by resting cell suspensions ofCatharanthus roseus in a continuous flow reactor.Appl. Microbiol. Biotechnol. 19, 316–320.

    Article  CAS  Google Scholar 

  120. Sato, S., Kawamura, K., and Fujiyoshi, N. (1983), Animal cell cultivation for production of biological substances with a novel perfusion culture apparatus.J. Tiss. Cult. Meth. 8, 167–171.

    Article  CAS  Google Scholar 

  121. Tabera, J. and Iznaola, M. A. (1989), Design of a Lamella settler for biomass recycling in continuous ethanol fermentation process.Biotechnol. Bioeng. 33, 1296–1305.

    Article  CAS  Google Scholar 

  122. Tokashiki, M. (1991), High density cell culture, inAnimal Cell Bioreactors, Ho, C. S. and Wang, D. I. C., eds., Butterworth-Heinemann, Boston, pp. 327–356.

    Google Scholar 

  123. Tyo, M. A. and Thilly, W. G. (1989), Novel high density perfusion system for suspension culture metabolic studies. Paper #30G presented at the 1989 AIChE Annual Meeting, San Francisco, CA.

  124. Van Wie, B.J., Brouns, T. M., Elliott, M. L., and Davis, W. C. (1991), A novel continuous centrifugal bioreactor for high-density cultivation of mammalian and microbial cells.Biotechnol. Bioeng. 38, 1190–1202.

    Article  Google Scholar 

  125. Wiesmann, U. and Binder, H. (1982), Biomass separation from liquids by sedimentation and centrifugation.Adv. Biochem. Eng. Biotechnol. 24, 119–171.

    Google Scholar 

  126. Su, W. W. (1994), External-loop perfusion air-lift bioreactor, US Pat.5, 342, 781.

    Google Scholar 

  127. Payne, G. F., Payne, N. N., and Shuler, M. L. (1988), Bioreactor considerations for secondary metabolite production from plant cell tissue culture: indole alkaloids fromCatharanthus roseus.Biotechnol. Bioeng. 31, 905–912.

    Article  CAS  Google Scholar 

  128. Feder, J. and Tolbert, W. R. (1983), The large-scale cultivation of mammalian cells.Sci.Am. 248, 24–31.

    Article  Google Scholar 

  129. Ammirato, P. V. and Styer, D. J. (1985), Strategies for large-scale manipulation of somatic embryos in suspension culture, inBiotechnology in Plant Science, Zaitlin, M., Day, P., and Hollaender, A., eds., Academic, New York, pp. 161–178.

    Google Scholar 

  130. Yabannavar, V. M., Singh, V., and Connelly, N. V. (1992), Mammalian cell retention in a spin filter perfusion bioreactor.Biotechnol. Bioeng. 40, 925–933.

    Article  CAS  Google Scholar 

  131. Wagner, R. and Lehmann, J. (1988), The growth and productivity of recombinant animal cells in a bubble-free aeration system.Trends Biotechnol. 6, 101–104.

    Article  Google Scholar 

  132. Beiderbeck, R. and Knoop, B. (1987), Two-phase culture, inCell Culture and Somatic Cell Genetics of Plants, vol. 4, Constabel, F. and Vasil, I. K., eds., Academic, San Diego, CA, pp. 255–266.

    Google Scholar 

  133. Payne, G. F., Payne, N. N., Shuler, M. L., and Asada, M., (1988),In situ adsorption for enhanced alkaloid production byCatharanthus roseus.Biotechnol. Lett. 10, 187–182.

    Article  CAS  Google Scholar 

  134. Williams, R. D., Chauret, N., Bedard, C., and Archambault, J. (1992), Effect of polymeroc adsorbents on the production of sanguinarine byPapaver somniferum cell cultures.Biotechnol. Bioeng. 40, 971–977.

    Article  CAS  Google Scholar 

  135. Berlin, J., Witte, L., Schubert, W., and Wray, V. (1984), Determination and quantification of monoterpenoids secreted into the medium of cell cultures ofThuja occidentalis.Phyto. Chem. 23, 1277–1279.

    CAS  Google Scholar 

  136. Byun, S. Y., Pedersen, H., and Chin, C. K. (1991), Two-phase culture for the enhanced production of benzophenanhtridine alkaloids in cell suspensions ofEschscholtzia californica.Phytochemistry 29, 3135–3139.

    Article  Google Scholar 

  137. Pedersen, H. (1992), Increasing secondary metabolite production byin vivo extraction and elicitation, inBiochemical Engineering for 2001, Furusaki, S., Endo, I., and Matsuno, R., eds., Springer-Verlag, Tokyo, pp. 254–257.

    Google Scholar 

  138. Brodelius, P. E. and Nilsson, K. (1983), Permeabilization of immobilized plant cells, resulting in release of intracellularly stored products with preserved cell viability.Eur. J. Microbiol. Biotechnol. 17, 275–280.

    Article  CAS  Google Scholar 

  139. Park, C. H. and Martinez, B. C. (1992), Enhanced release of rosmarinic acid fromColeus blumei permeabilized by dimethyl sulfoxide (DMSO) while preserving cell viability and growth.Biotechnol. Bioeng. 40, 459–464.

    Article  CAS  Google Scholar 

  140. Parr, A. J., Robins, R. J., and Rhodes, M. J. C. (1984), Permeabilization ofCinchona ledgeriana cells by dimethylsulfoxide: Effects on alkaloid release and long-term membrane integrity.Plant Cell Rep. 3, 262–265.

    Article  CAS  Google Scholar 

  141. Misawa, M. (1991), Research activities in Japan, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., MCM, Tokyo, pp. 3–7.

    Google Scholar 

  142. Matsubara, K. and Fujita, Y. (1991), Production of berberine, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 39–44.

    Google Scholar 

  143. Ikeda, T. (1991), Production of anti-plant-viral protein byMirabilis jalapa L. cells in suspension culture, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 45–57.

    Google Scholar 

  144. Yamamoto, Y. (1991), Production of lichen substances, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 58–71.

    Google Scholar 

  145. Yokoyama, M., and Yanagi, M. (1991), High-level production of arbutin by biotransformation, inPlant Cell Culture in Japan, Komamine, A., Misawa, M., and DiCosmo, F., eds., CMC, Tokyo, pp. 79–91.

    Google Scholar 

  146. Buitelaar, R. M. and Tramper, J. (1992), Strategies to improve the production of secondary metabolites with plant cell cultures: A literature review.J. Biotechnol. 23, 111–141.

    Article  CAS  Google Scholar 

  147. Hirasuna, T. J., Willard, D. M., and Shuler, M. L. (1992), Prospects for taxol production from cell culture. Paper #163a presented at the AIChE Annual Meeting, Miami Beach, FL.

  148. Goldstein, W. E. (1992), Development of taxol plant cell culture processes. Paper presented at the ACS Spring National Meeting, San Francisco, CA.

  149. Camaron, D. C., Ellis, D. D., McCown, B. H., Zeldin, E. L., Russin, W. A., and Evert, R. F. (1992), Differentiated tissue culture for the production of taxol and taxanes. Paper #163b presented at the AIChE Annual Meeting, Miami Beach, FL.

  150. Thorup, J., McDonald, K. and Jackman, A. (1992), Studies of ribosome inactivating protein production fromTrichosanthes kirlowii plant cell cultures. Paper #163d presented at the AIChE Annual Meeting, Miami Beach, FL.

  151. Savary, B. J. and Flores, H. (1992), Biosynthesis of ribosome-inactivating and pathogenesis-related proteins in hairy root cultures ofTrichosanthes sp. Paper #163c presented at the AIChE Annual Meeting, Miami Beach, FL.

  152. Westphal, K. (1990), Large-scale production of new biologically active compounds in plant cell cultures, inProgress in Plant Cellular and Molecular Biology, Nijkamp, H. J. J., van der Plas, L. H. W., and van Aartijk, J., eds., Kluwer, Dordrecht, Netherlands, pp. 601–609.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biochemical Engineering Laboratory, Department of Biosystems Engineering, University of Hawaii at Manoa, 96822, Honolulu, HI

    Wei wen Su

Authors
  1. Wei wen Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Su, W.w. Bioprocessing technology for plant cell suspension cultures. Appl Biochem Biotechnol 50, 189–230 (1995). https://doi.org/10.1007/BF02783455

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02783455

Index Entries

Search

Navigation