Hairy Root Culture: An Efficient System for Secondary Metabolite Production

  • Shiwali Sharma
  • Anwar Shahzad
  • Aastha Sahai


Plants are a potential source for the discovery of new products of medicinal value and served as lead compounds for drug development. Tremendous efforts have been made to commercialize production of plant metabolites employing plant cell culture in bioreactors, but very few have achieved commercial success. Hairy root culture is an unsurpassed choice for bio-processing system for various root associated pharmaceuticals due to fast growth rate, easy culture, genetic manipulations and most important biochemical stability of neoplastic roots. It serves as a model system for plant metabolism and physiology and utilized as a technical alternative to plant cell suspension culture. Moreover, hairy root culture plays a significant role in design the principle for plant metabolic engineering, germplasm conservation, expression of foreign protein and phytoremedaition. However, its global utilization requires attempts on the establishment of effective and economical scaled up culture that can reduce the consumption, but obtain the biggest benefits.


Hairy Root Hairy Root Culture Rosmarinic Acid Secondary Metabolite Production Tropane Alkaloid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Dr. Anwar Shahzad gratefully acknowledges the financial support provided by the Council of Science and Technology, Uttar Pradesh (Project No. CST/D3836) and UGC (Project No. 39-369/2010). Dr. Shiwali Sharma is thankful to UGC, for the award of BSR Fellowship in Science (1st April 2010) for providing research assistance.



Agrobacterium is a genus of Gram-negative bacteria established by H. J. Conn that uses horizontal gene transfer to cause tumors in plants. Agrobacterium is well known for its ability to transfer DNA between itself and plants, and for this reason it has become an important tool for genetic engineering.


An extra-chromosomal, autonomous circular DNA molecule found in certain bacteria, capable of autonomous replication. Plasmids can transfer genes between bacteria and are important tools of transformation.


Transferred DNA of the tumor-inducing (Ti) plasmid of some species of bacteria such as Agrobacterium tumefaciens and Agrobacterium rhizogenes. It derives its name from the fact that the bacterium transfers this DNA fragment into the host plant’s nuclear DNA genome.

Hairy root

A phase of crown gall (especially in apples) during which there is abnormal development of fine fibrous roots.

Secondary metabolite

Organic compounds that are not directly involved in the normal growth, development, or reproduction of an organism. Secondary metabolites often play an important role in plant defense against herbivory and other interspecies defenses. Humans use secondary metabolites as medicines, flavorings, and recreational drugs.


The treatment of environmental problems (bioremediation) through the use of plants that mitigate the environmental problem without the need to excavate the contaminant material and dispose of it elsewhere.


Low molecular weight compounds found in plant crown gall tumors or hairy root tumors produced by parasitic bacteria of the genus Agrobacterium. Opine biosynthesis is catalyzed by specific enzymes encoded by genes contained in a small segment of DNA (known as the T-DNA, for ‘transfer DNA’), which is part of the Ti plasmid, inserted by the bacterium into the plant genome. The opines are used by the bacterium as an important source of nitrogen and energy. Each strain of Agrobacterium induces and catabolizes a specific set of opines.


  1. Ackermann, C. (1977). Pflanzen aus Agrobacterium rhizogenes Tumoren an Nicotiana tabacum. Plant Science Letters, 8, 23–30.Google Scholar
  2. Asada, Y., Saito, H., Yoshikawa, T., Sakamoto, K., & Furuya, T. (1993). Biotransformation of 18β-glycyrrhetinic acid by ginseng hairy root culture. Phytochemicals, 34(4), 1049–1052.Google Scholar
  3. Asada, Y., Li, W., & Yoshikawa, T. (1998). Isoprenylated flavonoids from hairy root cultures of Glycyrrhiza glabra. Phytochemistry, 47, 389–392.Google Scholar
  4. Ayora-Talavera, T., Chappell, J., Lozoya-Gloria, E., & Loyola-Vargas, V. M. (2002). Over-­expression in Catharanthus roseus hairy roots of a truncated hamster 3-hydroxy-3-­methylglutaryl-CoA reductase gene. Applied Biochemistry and Biotechnology, 97, 135–145.Google Scholar
  5. Azlan, G. J., Marziah, M., Radzali, M., & Johari, R. (2002). Establishment of Physalis minima hairy root culture for the production of physalins. Plant Cell Tissue and Organ Culture, 69, 271–278.Google Scholar
  6. Bakkali, A. T., Jaziri, M., Foriers, A., Vander Heyden, Y., Vanhaelen, M., & Homes, J. (1997). Lawsone accumulation in normal and transformed cultures of henna, Lawsonia inermis. Plant Cell Tissue and Organ Culture, 51, 83–87.Google Scholar
  7. Balandrin, M. F., Klocke, J. A., Wurtele, E. S., & Bollinger, W. H. (1985). Natural plant chemicals: Sources of industrial and medicinal material. Science, 228, 1154–1160.Google Scholar
  8. Banerjee, S., Rahman, L., Uniyal, G. C., & Ahuja, P. S. (1998). Enhanced production of valepotriates by Agrobacterium rhizogenes induced hairy root cultures of Valeriana wallichi DC. Plant Science, 131, 203–208.Google Scholar
  9. Bastian, P., Chavarria-Krauser, A., Engwer, C., Jager, W., Marnach, S., & Ptashnyk, M. (2008). Modeling in vitro growth of dense root networks. Journal of Theoretical Biology, 254, 99–109.Google Scholar
  10. Berkov, S., Pavlov, A., Kovatcheva, P., Stanimirova, P., & Philipov, S. (2003). Alkaloid spectrum in diploid and tetraploid hairy root cultures of Datura stramonium. Zeitschrift Für Naturforschung, 58, 42–46.Google Scholar
  11. Berlin, J., Beier, H., Fecker, L., Forche, E., Noe, W., Sasse, F., Schiel, O., & Wray, V. (1985). Conventional and new approaches to increase the alkaloid production of plant cell cultures. In K. H. Neumann, W. Barz, & E. Reinhard (Eds.), Primary and secondary metabolism of plant cell cultures (pp. 272–280). Berlin: Springer.Google Scholar
  12. Bhadra, R., & Shanks, J. V. (1997). Transient studies of nutrient uptake, growth and indole alkaloid accumulation in heterotrophic cultures of hairy roots of Catharanthus roseus. Biotechnology and Bioengineering, 55, 527–534.Google Scholar
  13. Bhadra, R., Morgan, J. A., & Shanks, J. V. (1998). Transient studies of light-adapted cultures of hairy roots of Catharanthus roseus: Growth and indole alkaloid accumulation. Biotechnology and Bioengineering, 60, 670–678.Google Scholar
  14. Bhadra, R., Wayment, D. G., Hughes, J. B., & Shanks, J. V. (1999). Confirmation of conjugation processes during TNT metabolism by axenic plant roots. Environmental Science and Technology, 33, 446–452.Google Scholar
  15. Binns, A. N., & Thomashow, M. F. (1988). Cell biology of Agrobacterium infection and transformation of plants. Annual Review of Microbiology, 42, 575–606.Google Scholar
  16. Cain, C. C., Saslowsky, D. E., Walker, R. A., & Shirley, B. W. (1997). Expression of chalcone synthase and chalcone isomerase proteins in Arabidposis seedlings. Plant Molecular Biology, 35, 377–381.Google Scholar
  17. Charlwood, B. V., & Charlwood, K. A. (1991). Terpenoid production in plant cell cultures. In J. B. Harborne & F. A. Thomas-Barberan (Eds.), Ecological chemistry and biochemistry of plant terpenoids (pp. 95–132). Oxford: Clarendon.Google Scholar
  18. Chinou, I. (2008). Primary and secondary metabolites and their biological activity. In M. Waksmundzka-Hajnos, J. Sherma, & T. Kowalska (Eds.), Thin layer chromatography in photochemistry. Boca Raton: CRC Press.Google Scholar
  19. Cho, H. J., & Wildholm, J. M. (2002). Improved shoot regeneration protocol for hairy roots of the legume Astragalus sinicus. Plant Cell Tissue and Organ Culture, 69, 259–269.Google Scholar
  20. Choi, D. W., et al. (2005). Analysis of transcripts in methyl jasmonate-treated ginseng hairy roots to identify genes involved in the biosynthesis of ginsenosides and other secondary metabolites. Plant Cell Reports, 23, 557–566.Google Scholar
  21. Condori, J., Sivakumar, G., Hubstenberger, J., Dolan, M., Sobolev, V., & Medina-Boliver, F. (2010). Induced biosynthesis of resveratrol and the prenylated stilbenoids arachidin-1 and arachidin-­3 in hairy root cultures of peanut: Effects of culture medium and growth stage. Plant Physiology and Biochemistry, 48, 310–318.Google Scholar
  22. Deboer, K. D., Lye, J. C., Aitken, C. D., Su, A. K., & Hamill, J. D. (2009). The A622 gene in Nicotiana glauca (tree tobacco): Evidence for a functional role in pyridine alkaloid synthesis. Plant Molecular Biology, 69, 299–312.Google Scholar
  23. Dechaux, C., & Boitel-Conti, M. (2005). A strategy for over accumulation of scopolamine in Datura innoxia hairy root culture. Acta Biologica Coviensia Series Botanica, 47, 101–107.Google Scholar
  24. De Jesus-Gonzalez, L., & Weathers, P. J. (2003). Tetraploid Artemisia annua hairy roots produce more artemisinin than diploids. Plant Cell Reports, 21(8), 809–813.Google Scholar
  25. Dhakulkar, S., Ganapathi, T. R., Bhargava, S., & Bapat, V. A. (2005). Induction of hairy roots in Gmelina arborea Roxb. and production of verbascoside in hairy roots. Plant Science, 169, 812–818.Google Scholar
  26. Dixit, A. K., & Vaidya, S. (2010). Agrobacterium rhizogenes induced hairy root development and its effect on production of glycyrrhizin in Abrus precatorious (L.). International Journal of Current Research, 6, 033–038.Google Scholar
  27. Doran, P. M. (2006). Foreign protein degradation and instability in plants and plant tissue cultures. Trends in Biotechnology, 24, 426–432.Google Scholar
  28. Flores, H. E., Dai, Y. R., Freyer, A. J., & Michaels, P. J. (1994). Biotransformation of butylated hydroxytoluene in ‘hairy root’ cultures. Plant Physiology and Biochemistry, 32, 511–519.Google Scholar
  29. Flores, H. E., & Filner, P. (1985). Metabolic relationships of putrescine, GABA, and alkaloids in cell and root cultures of Solanaceae. In K. H. Neumann, W. Barz, & E. Reinhard (Eds.), Primary and secondary metabolism of plant cell cultures (pp. 174–186). Berlin: Springer.Google Scholar
  30. Flores, H. E., Vivanco, J. M., & Loyola-Vargas, V. M. (1999). Radicle biochemistry: The biology of root-specific metabolism. Trends in Plant Science, 4, 220–226.Google Scholar
  31. Fu, C. X., Zhao, D. X., Xue, X. F., Jin, Z. P., & Ma, F. S. (2005). Transformation of Saussurea involucrate by Agrobacterium rhizogenes: Hairy root induction and syringing production. Process Biochemistry, 40, 3789–3794.Google Scholar
  32. Fukui, H., Hasan, A. F. M. F., Ueoka, T., & Kyo, M. (1998). Formation and secretion of a new brown bezoquinone by hairy root cultures of Lithospermum erythrorhizon. Phytochemistry, 47, 1037–1039.Google Scholar
  33. Gamborg, O. L., Miller, R. A., & Ojima, K. (1968). Nutrient requirements of suspension cultures of soyabean root cells. Experimental Cell Research, 50, 151–158.Google Scholar
  34. Gaume, A., et al. (2003). Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Reports, 22, 344–349.Google Scholar
  35. Gelvin, S. B. (2000). Agrobacterium and plant genes involved in T-DNA transfer and integration. Annual Review of Plant Physiology and Plant Molecular Biology, 51, 223–256.Google Scholar
  36. Georgiev, M., Heinrich, M., Kerns, G., Pavlov, A., & Bley, T. (2006). Production of iridoids and phenolics by transformed harpagophytum procumbens root cultures. Engineering in Life Sciences, 6(6), 593–596.Google Scholar
  37. Giovanni, A., Pecchioni, N., Rabaglio, M., & Allavena, A. (1997). Characterization of ornamental Datura plants transformed by Agrobacterium rhizogenes. In Vitro Cellular and Developmental Biology-Plant, 33, 101–106.Google Scholar
  38. Giri, A., & Narasu, M. L. (2000). Transgenic hairy roots recent trends and applications. Biotechnology Advances, 18, 1–22.Google Scholar
  39. Giri, A., Banerjee, S., Ahuja, P. S., & Giri, C. C. (1997). Production of hairy roots in Aconitum heterophyllum wall. using Agrobacterium rhizogenes. In Vitro Cellular and Developmental Biology-Plant, 33, 280–284.Google Scholar
  40. Giri, A., Ravindra, S. T., Dhingra, V., & Narasu, M. L. (2001). Influence of different strains of Agrobacterium rhizogenes on induction of hairy root and artemisinin production in Artemisia annua. Current Science, 81, 378–382.Google Scholar
  41. Han, K. H., Kethley, D. E., Davis, J. M., & Gordon, M. P. (1993). Regeneration of a transgenic woody legume (Robonia pseudoacacia L. black locust) and morphological alternations induced by Agrobacterium rhizogenes-mediated transformation. Plant Science, 88, 149–157.Google Scholar
  42. Hyon, K. J. I., & Yoo, Y. J. E. (2002). Optimization of SOD biosynthesis by controlling sucrose concentration in the culture of carrot hairy root. Journal of Microbiology and Biotechnology, 12, 617–621.Google Scholar
  43. Jaziri, K. H., Shimomura, K., Yoshimatsu, K., Fauconnier, M. L., Marlier, M., & Homes, J. (1995). Establishment of normal and transformed root cultures of Artemisia aanua L. for artemisinin production. Journal of Plant Physiology, 145, 175–177.Google Scholar
  44. Jeong, G.-T., Park, D.-H., Ryu, H.-W., Hwang, B., & Woo, J.-C. (2004). Effects of inoculum conditions on growth of hairy roots of Panax ginseng C.A. Meyer. Applied Biochemistry and Biotechnology, 113–116, 1193–1203.Google Scholar
  45. Jin, U. H., Chun, J. A., Han, M. O., Lee, J. W., Yi, Y. B., Lee, S. W., & Chung, C. H. (2005). Sesame hairy root cultures for extra-cellular production of a recombinant fungal phytase. Process Biochemistry, 40, 3754–3762.Google Scholar
  46. Jouhikainen, K., Lindgren, L., Jokelainen, T., Hiltunen, R., Teeri, T. H., & Oksman-Caldentey, K. M. (1999). Enhancement of scopolamine production in Hyoscyamus muticus L. hairy root cultures by genetic engineering. Planta, 208, 545–551.Google Scholar
  47. Kajikawa, M., Hirai, N., & Hashimoto, T. (2009). A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Molecular Biology, 69, 287–298.Google Scholar
  48. Kawaguchi, K., Hirotani, M., Yoshikawa, T., & Furuya, T. (1990). Biotransformation of digitoxigenin by ginseng hairy root cultures. Phytochemistry, 29(3), 837–843.Google Scholar
  49. Khas, J., Burkhard, J., Demnerova, K., Kostal, J., Macek, T., Mackovq, M., & Pazlarova, J. (1997). Perspective in biodegradation of alkanes and PCBs. Pure and Applied Chemistry, 69, 2357–2369.Google Scholar
  50. Kim, Y. H., & Yoo, Y. J. (1996). Peroxidase production from carrot hairy root cell culture. Enzyme and Microbial Technology, 18, 531–535.Google Scholar
  51. Kim, J. S., Lee, S. Y., & Park, S. U. (2008). Resveratrol production in hairy root culture of peanut, Arachis hypogea L. transformed with different Agrobacterium rhizogenes strains. African Journal of Biotechnology, 7, 3785–3787.Google Scholar
  52. Kim, Y. K., Xu, H., Park, W. T., Park, N. I. I., Lee, S. Y., & Park, S. U. (2010). Genetic transformation of rutin in transformed root cultures. Australian Journal of Crop Science, 4, 485–490.Google Scholar
  53. Kittipongpatana, N., Hock, R. S., & Porter, J. R. (1998). Production of solasodine by hairy root, callus, and cell suspension cultures of Solanum aviculare Forst. Plant Cell, Tissue and Organ Culture, 52, 133–143.Google Scholar
  54. Koehle, A., Sommer, S., Yazaki, K., et al. (2002). High level expression of solasodine by hairy root callus, and cell suspension cultures of Solanum aviculare Forst. Plant Cell Tissue and Organ Culture, 52, 133–143.Google Scholar
  55. Komaraiah, P., et al. (2003). Enhanced production of antimicrobial sesquiterpenes and lipoxygenase metabolites in elicitor-treated hairy root cultures of Solanum tuberosum. Biotechnology Letters, 25, 593–597.Google Scholar
  56. Krolicka, A., Staniszewska, I., Bielawski, K., Malinski, E., Szafranek, J., & Lojkowska, E. (2001). Establishment of hairy root cultures of Ammi majus. Plant Science, 160, 259–264.Google Scholar
  57. Kumagi, H., & Kouchi, H. (2003). Gene silencing by expression by hairpin RNA in Lotus japonicas roots and root nodules. Molecular Plant-Microbe Interactions, 16, 663–668.Google Scholar
  58. Kumar, V., Jones, B., & Davey, M. R. (1991). Transformation by Agrobacterium rhizogenes of transgenic shoots of the wild soyabean Glycine argyrea. Plant Cell Reports, 10, 135–138.Google Scholar
  59. Lan, X., & Quan, H. (2010). Hairy root culture of Przewalskia tangutica for enhanced pro­duction of pharmaceutical tropane alkaloids. Journal of Medicinal Plants Research, 4, 1477–1481.Google Scholar
  60. Lavania, U. (2005). Genomic and ploidy manipulation for enhanced production of phyto-­pharmaceuticals. Plant Genetic Resources, 3, 170–177.Google Scholar
  61. Le Flem-Bonhomme, V., Laurain-Mattar, D., & Fliniaux, M. A. (2004). Hairy root induction of Papaver somniferum var. album, a difficult-to-transform plant by A. rhizogenes LBA 9402. Planta, 218, 890–893.Google Scholar
  62. Lee, J. H., Loc, N. H., Kwon, T. H., & Yang, M. S. (2004). Partitioning of recombinant human granulocyte-macrophage colony stimulating factor (hGM-CSF) from plant cell suspension culture in PEG/sodium phosphate aqueous two-phase systems. Biotechnology and Bioprocess Engineering, 9, 12–16.Google Scholar
  63. Li, W., Asada, Y., & Yoshikawa, T. (1998). Antimicrobial flavonoids from Glycyrrhiza glabra hairy root cultures. Planta Medica, 64, 746–747.Google Scholar
  64. Li, W., Koike, K., Asada, Y., Hirotani, M., Rui, H., Yoshikawa, T., & Nikaido, T. (2002). Flavonoids from Glycyrrhiza pallidiflora hairy root cultures. Phytochemistry, 60, 351–355.Google Scholar
  65. Liu, C. Z., Wang, Y. C., Zhao, B., Guo, C., Ouyang, F., Ye, H. C., & Li, G. F. (1999). Development of a nutrient and bioreactor for growth of hairy roots. In Vitro Cellular and Developmental Biology-Plant, 35, 271–274.Google Scholar
  66. Lu, M. B., Wong, H. L., & Teng, W. L. (2001). Effects of elicitation on the production of saponin in cell culture of Panax ginseng. Plant Cell Reports, 20, 674–677.Google Scholar
  67. Mahagamasekera, M. G. P., & Doran, P. M. (1998). Intergeneric co-culture of genetically transformed organs for the production of scoplolamine. Phytochemistry, 47, 17–25.Google Scholar
  68. Mavituna, F. (1992). Applications of plant biotechnology in industry and agriculture. In F. Vardar-­Sukan & S. S. Sukan (Eds.), Recent advances in biotechnology (pp. 209–226). Boston: Kluwer Academic.Google Scholar
  69. Medina-Bolivar, F., et al. (2003). A non-toxin lectin for antigen delivery of plant-based mucosal vaccines. Vaccine, 21, 997–1005.Google Scholar
  70. Menzel, G., Harloff, H. J., & Jung, C. (2003). Expression of bacterial poly (3-hydroxybutyrate) synthesis genes in hairy roots of sugar beet (Beta vulgaris L.). Applied Microbiology and Biotechnology, 60, 571–576.Google Scholar
  71. Moyano, E., Jouhikainen, K., Tammela, P., Palaźon, J., Cusido, R. M., Piñol, M. T., Teeri, T. H., & Oksman-Caldentey, K. M. (2003). Effect of pmt gene over-expression on tropane alkaloid production in transformed root cultures of Datura metel and Hyoscyamus muticus. Journal of Experimental Botany, 54, 203–211.Google Scholar
  72. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum, 15, 473–497.Google Scholar
  73. Nakanishi, F., et al. (2005). Characterization of lucidin formation in Rubia tinctorum L. Plant Physiology and Biochemistry, 43, 921–928.Google Scholar
  74. Nakashimada, Y., Uozemi, N., & Kobayashi, T. (1995). Production of plantlets for use as artificial seeds from horseradish hairy roots fragmented in a blender. Journal of Fermentation and Bioengineering, 79, 458–464.Google Scholar
  75. Nesi, N., Jond, C., Debeaujon, I., Caboche, M., & Lepiniec, I. (2001). The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. The Plant Cell, 13, 2099–2114.Google Scholar
  76. Nguyen, C., Bourgaud, F., Forlot, P., & Guckert, A. (1992). Establishment of hairy root cultures of Psoralea species. Plant Cell Reports, 11, 424–427.Google Scholar
  77. Nilsson, O., & Olsson, O. (1997). Getting to the root: The role of the Agrobacterium rhizogenes rol genes in formation of hairy root. Physiologia Plantarum, 100, 403–473.Google Scholar
  78. Nin, S., Bennici, A., Roselli, G., Mariotti, D., Schiff, S., & Magherini, R. (1997). Agrobacterium-­mediated transformation of Atremisia absinthium L. (wornwood) and production of secondary metabolites. Plant Cell Reports, 16, 725–730.Google Scholar
  79. Nishikawa, K., & Ishimaru, K. (1997). Flavonoids in root cultures of Scutellaria baicalensis. Journal of Plant Physiology, 151, 633–636.Google Scholar
  80. Ohkawa, H., Kamda, H., Sudo, H., & Harada, H. (1989). Effects of gibberellic acid on hairy root growth in Datura innoxia. Journal of Plant Physiology, 134, 633–636.Google Scholar
  81. Oksman-Caldentey, K. M., & Strauss, A. (1986). A somaclonal variation of scopolamine content in protoplast-derived cell culture clones of Hyoscyamus muticus. Planta Medica, 52, 6–12.Google Scholar
  82. Ono, N. N., & Tian, L. (2011). The multiplicity of hairy root cultures: Prolific possibilities. Plant Science, 180(3), 439–446.Google Scholar
  83. Ooms, G., Twell, D., Bossen, M. E., Hoge, J. H. C., & Burrell, M. M. (1986). Development regulation of Ri T DNA gene expression in root, shoots and tubers of transformed potato (Solanum tuberosum cv. Desiree). Plant Molecular Biology, 6, 321–330.Google Scholar
  84. Palazon, J., et al. (2003). Elicitation of different Panax ginseng-transformed root phenotypes for an improved ginsenoside production. Plant Physiology and Biochemistry, 41, 1019–1025.Google Scholar
  85. Pang, Y., Peel, G. J., Sharma, S. B., Tang, Y., & Dixon, R. A. (2008). A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula. Proceedings of the National Academy of Sciences of the United States of America, 105, 14210–14215.Google Scholar
  86. Park, S.-U., & Facchini, P. J. (2000). Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and California poppy, Eschscholzia californica Cham., root cultures. Journal of Experimental Botany, 51, 1005–1016.Google Scholar
  87. Parr, A. J. (1989). The production of secondary metabolites by plant cell cultures. Journal of Biotechnology, 10, 1–25.Google Scholar
  88. Pavlov, A., Georgiev, V., & Kovatcheva, P. (2002a). Relationship between type and age of inoculum and betalains biosynthesis by B. vulgaris hairy root culture. Biotechnology Letters, 25, 307–309.Google Scholar
  89. Pavlov, A., Kovatcheva, P., Georgiev, V., Koleva, I., & Ilieva, M. (2002b). Biosynthesis and radical scavenging activity of betalanins during the cultivation of Red beet (Beta Vulagris) hairy root cultures. Zeitschrift für Naturforschung, 57, 640–644.Google Scholar
  90. Pavlov, A., Georgiev, V., & Kovatcheva, P. (2003). Relationship between type and age of the inoculum cultures and betalains biosynthesis by Beta vulgaris hairy root culture. Biotechnology Letters, 25(4), 307–309.Google Scholar
  91. Pavlov, A., Berkov, S., Weber, J., & Bley, T. (2009). Hyoscyamine biosynthesis in Datura stramonium hairy root in vitro systems with different ploidy levels. Applied Biochemistry and Biotechnology, 157, 210–225.Google Scholar
  92. Peebles, C. A., Sander, G. W., Li, M., Shanks, J. V., & San, K. Y. (2009). Five year maintenance of the inducible expression of anthranilacte synthase in Catharanthus roseus hairy roots. Biotechnology and Bioengineering, 102, 1521–1525.Google Scholar
  93. Petit, A., David, C., Dahl, G. A., Ellis, J. G., Guyon, P., Casse-Delbart, F., & Tempe, A. J. (1983). Further extension of the opine concept: Plasmids in Agrobacterium rhizogenes cooperate for opine degradation. Molecular and General Genetics, 190, 204–214.Google Scholar
  94. Phunchindawan, M., Hirata, K., Sakai, A., & Miyamoto, K. (1997). Cryopreservation of encapsulated shoot primordial induced in horse radish (Armoracia rusticana) hairy root cultures. Plant Cell Reports, 16, 469–473.Google Scholar
  95. Prakash, O., Mehrotra, S., Krishna, A., & Mishra, B. (2010). A neural network approach for the prediction of in vitro culture parameters for maximum biomass yields in hairy root cultures. Journal of Theoretical Biology, 265, 579–585.Google Scholar
  96. Rahman, L., Ikenaga, T., & Kitamura, Y. (2004). Penicillin derivatives induce chemical structure-­dependent root development, and application for plant transformation. Plant Cell Reports, 22, 668–677.Google Scholar
  97. Ralston, L., Subramanian, S., Matsuno, M., & Yu, O. (2005). Partial reconstruction of flavonoid and isoflavonoid biosynthesis in yeast using soyabean type I and type II chalcone isomerases. Plant Physiology, 137, 1375–1388.Google Scholar
  98. Ramachandra, R. S., & Ravishankar, G. A. (2002). Plant cell cultures: Chemical factories of secondary metabolites. Biotechnology Advances, 20(2), 101–153.Google Scholar
  99. Richter, U., Rothe, G., Fabian, A. K., Rahfeld, B., & Dräger, B. (2005). Over-expression of tropinone reductases alters alkaloid composition in Atropa belladonna root cultures. Journal of Experimental Botany, 56, 645–652.Google Scholar
  100. Riker, A. J., Banpield, W. M., Wright, W. H., Knitt, G. W., & Sagen, H. E. (1930). Studies on infectitious hairy root of nursery apple trees. Journal of Agriculture Research, 41, 507–540.Google Scholar
  101. Rischer, H., et al. (2006). Gene-to-metabolite networks for terpene indole alkaloid biosynthesis in Catharanthus roseus cells. Proceedings of the National Academy of Sciences of the United States of America, 103, 5614–5619.Google Scholar
  102. Rokem, J. S., & Goldberg, I. (1985). Secondary metabolites from plant cell suspension cultures: methods for yield improvement in advances in biotechnological processes (Vol. 4, pp. 241–274). New York: Alam R Liss Inc.Google Scholar
  103. Rothe, G., Garske, U., & Draeger, B. (2001). Calystegines in root cultures of Atropa belladonna respond to sucrose, not to elicitation. Plant Science, 160, 1043–1053.Google Scholar
  104. Sato, F., Hashimoto, T., Hachiya, A., Tamura, K., Choi, K., Morishige, T., Fujimoto, H., & Yamada, Y. (2001). Metabolic engineering of plant alkaloid biosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 98, 367–372.Google Scholar
  105. Seki, H., et al. (2005). Hairy root-activation tagging: A high-throughput system for activation tagging in transformed hairy roots. Plant Molecular Biology, 59, 793–807.Google Scholar
  106. Sevon, N., & Oksman-Caldentey, K.-M. (2002). Agrobacterium rhizogenes-mediated transformation root cultures as a source of alkaloid. Planta Medica, 68, 859–868.Google Scholar
  107. Sharp, J. M., & Doarn, P. M. (2001). Strategies for enhancing monoclonal antibody accumulation in plant cell and organ cultures. Biotechnology Progress, 17, 979–992.Google Scholar
  108. Shen, W. H., Petit, A., Guern, J., & Tempe, J. (1988). Hairy roots are more sensitive to auxin than normal roots. Proceedings of the National Academy of Sciences of the United States of America, 35, 3417–3421.Google Scholar
  109. Shinde, A., Malpathak, N., & Fulzele, D. (2010). Impact of nutrient components on production of the phytoestrogens daidzein and genistein by hairy roots of Psoralea corylifolia. Journal of Natural Medicines, 64, 346–353.Google Scholar
  110. Shul’ts, E. E., Petrova, T. N., Shakirov, M. M., Chernyak, E. I., & Tolstikov, G. A. (2000). Flavonoids of roots of Glycyrrhiza uralensis growing in Siberia. Chemistry of Natural Compounds, 36, 362–368.Google Scholar
  111. Sivakumar, G. (2006). Bioreactor technology: A novel industrial tool for high-tech production of bioactive molecules and biopharmaceuticals from plant roots. Biotechnology Journal, 1, 1419–1427.Google Scholar
  112. Sivakumar, G., Yu, K. W., Hahn, E. J., & Pack, K. Y. (2005). Optimization of organic nutrients for ginseng hairy roots production in large-scale bioreactors. Current Science, 89, 641–649.Google Scholar
  113. Sivanesan, I., & Jeong, B. R. (2009). Induction and establishment of adventitious and hairy root cultures of Plumbago zeylanica L. African Journal of Biotechnology, 8(20), 5294–5300.Google Scholar
  114. Srivastava, S., & Srivastava, A. K. (2007). Hairy root culture for mass-production of high-value secondary metabolites. Critical Reviews in Biotechnology, 27, 29–43.Google Scholar
  115. Stewart, F. C., Rolfs, F. M., & Hall, F. H. (1900). A fruit disease survey of western New York in 1900. New York State Agricultural Experiment Station Technical Bulletin, 191, 291–331.Google Scholar
  116. Subruto, S. E., Kwok, K. H., Hamid, J. D., & Doran, P. M. (1996). Co-culture of genetically transformed roots and shoots for synthesis, translocation, and biotransformation of secondary metabolites. Biotechnology and Bioengineering, 49, 481–494.Google Scholar
  117. Sudha, C. G., Obul Reddy, B., Ravishankar, G. A., & Seeni, S. (2003). Production of ajmalicine and ajmaline in hairy root cultures of Rauvolfia micrantha Hook f., a rare and endemic medicinal plant. Biotechnology Letters, 25, 631–636.Google Scholar
  118. Sung, L.-S., & Huang, S.-Y. (2000). Median optimization of transformed root cultures of Stizolobium hassjoo producing I-DOPA with response surface methodology. Biotechnology Progress, 16, 1135–1140.Google Scholar
  119. Sung, L.-S., & Huang, S.-Y. (2006). Lateral root bridging as a strategy to enhance L-DOPA production in Stizolobium hassjoo hairy root cultures by using a mesh hindrance mist trickling bioreactor. Biotechnology and Bioengineering, 94(3), 441–447.Google Scholar
  120. Thorup, J. E., McDonald, K. A., Jackman, A. P., Bhatia, N., & Dandekar, A. M. (1994). Ribosome-­inactivating protein production from Trichosanthes kirilowii plant cell cultures. Biotechnology Progress, 10, 345–352.Google Scholar
  121. Trick, H. N., & Finer, J. J. (1997). SAAT: Sonication-assisted Agrobacterium-mediated transformation. Transgenic Research, 6, 329–336.Google Scholar
  122. Uozumi, N. (2004). Large-scale production of hairy root. Advances in Biochemical Engineering/Biotechnology, 91, 75–103.Google Scholar
  123. Ushiyana, M., & Furuya, T. (1989). Glycosylation of phenolic compounds by root cultures of Panax ginseng. Phytochemistry, 28, 3009–3013.Google Scholar
  124. Wallaart, T. E., Pras, N., & Quax, W. J. (1999). Isolation and identification of dihydroartemisinic acid hydro peroxide from Artemisia annua: A novel biosynthetic precursor of artemisinin. Journal of Natural Products, 62, 1160–1162.Google Scholar
  125. Weathers, P. J., Bunk, G., & McCoy, M. C. (2005). The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cellular and Developmental Biology-Plant, 41(1), 47–53.Google Scholar
  126. Weathers, P. J., Hemmavanh, D. D., Walcerz, D. B., & Cheetham, R. D. (1997). Interactive effects of nitrate and phosphate salts, sucrose and inoculums culture age on growth and sesquiterpene production in Artemisia annua hairy root cultures. In Vitro Cellular and Developmental Biology-Plant, 33, 306–312.Google Scholar
  127. Wilhelmson, A., Hakkinen, S. T., Kallio, P. T., Oksman-Caldentey, K.-M., & Nuutila, A. M. (2006). Heterologous expression of Vitreoscilla hemoglobin (VHb) and cultivation conditions affect the alkaloid profile of Hyoscyamus muticus hairy roots. Biotechnology Progress, 22, 350–358.Google Scholar
  128. Wilson, P. D. G., Hilton, M. G., Robins, R. J., & Rhodes, M. J. C. (1987). Fermentation studies of transformed root cultures. In G. W. Moody & P. B. Baker (Eds.), Bioreactors and biotransformation (pp. 38–51). London: Elsevier.Google Scholar
  129. Wink, M., Alfermann, A. W., Franke, R., Wetterauer, B., Distl, M., Windhovel, J., Krohn, O., Fuss, E., Garden, H., Mohagheghzadeh, A., Wildi, E., & Ripplinger, P. (2005). Sustainable bioproduction of phyto-chemicals by plant in vitro cultures: Anticancer agents. Plant Genetic Resources, 3, 90–100.Google Scholar
  130. Wongsamuth, R., & Doran, P. M. (1997). Production of monoclonal antibodies by tobacco hairy roots. Biotechnology and Bioengineering, 54, 401–415.Google Scholar
  131. Xie, D. Y., Zou, Z. R., Ye, H. C., Li, G. F., & Guo, Z. C. (2001). Selection of hairy root clones of Artemisia annua L. for artemisinin production. Israel Journal of Plant Sciences, 49, 129–134.Google Scholar
  132. Xu, Z. Q., & Jia, J. F. (1996). The reduction of chromosome number and the loss of regeneration ability during subculture of hairy root cultures of Onobrychis viciaefolia transformed by Agrobacterium rhizogenes A4. Plant Sciences, 120, 107–112.Google Scholar
  133. Yang, Y. K. (2010). Exogenous auxins and polyamines enhance growth and rosmarinic acid production in hairy root cultures of Nepeta cataria L. Plant Omics, 3(6), 190–193.Google Scholar
  134. Yaoya, S., et al. (2004). Umbelliferone released from hairy root cultures of Pharabitis nil treated with copper sulfate and its subsequent glycosylation. Bioscience, Biotechnology, and Biochemistry, 68, 1837–1841.Google Scholar
  135. Yazaki, K., Sugiyama, A., Morita, M., & Shitan, N. (2008). Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochemistry Reviews, 7, 513–524.Google Scholar
  136. Yoshikawa, T., & Furuya, T. (1987). Saponin production by cultures of Panax ginseng transformed with Agrobacterium rhizogenes. Plant Cell Reports, 6(6), 449–453.Google Scholar
  137. Yoshimatsu, K., Yamaguchi, H., & Shimomura, K. (1996). Traits of Panax ginseng hairy roots after cold storage and cryopreservation. Plant Cell Reports, 15, 555–560.Google Scholar
  138. Yun, D. J., Hashimoto, T., & Yamada, Y. (1992). Metabolic engineering of medicinal plants: Transgenic Atropa belladonna with an improved alkaloid composition. Proceedings of the National Academy of Sciences of the United States of America, 89, 11799–11803.Google Scholar
  139. Zhang, L., Ding, R., Chai, Y., Bonfill, M., Moyano, E., Oksman-Caldentey, K. M., Xu, T., Pi, Y., Wang, Z., Zhang, H., Kai, G., Liao, Z., Sun, X., & Tang, K. (2004). Engineering tropane biosynthetic in Hyoscyamus niger hairy root cultures. Proceedings of the National Academy of Sciences of the United States of America, 101, 6786–6791.Google Scholar
  140. Zhang, L., Kai, G. Y., LU, B. B., Zhang, H. M., Tang, K. X., Jiang, J. H., & Chen, W. S. (2005). Metabolic engineering of tropane alkaloid biosynthesis in plants. Journal of Integrative Plant Biology, 47, 136–143.Google Scholar
  141. Zhang, H.-C., Liu, J.-M., Lu, H.-Y., & Gao, S.-L. (2009). Enhanced flavonoid production in hairy root cultures of Glycyrrhiza uralensis Fisch by combining the over-expression of chalcone isomerase gene with the elicitation treatment. Plant Cell Reports, 28, 1205–1213.Google Scholar
  142. Zhou, Y., Hirotani, M., Yoshikava, T., & Furuya, T. (1997). Flavonoids and phenylethanoids from hairy root cultures of Scutellaria baicalensis. Phytochemistry, 44, 83–87.Google Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Plant Biotechnology Section, Department of BotanyAligarh Muslim UniversityAligarhIndia

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