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Hairy Root Culture for In Vitro Production of Secondary Metabolites: A Promising Biotechnological Approach

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Biotechnological Approaches for Medicinal and Aromatic Plants

Abstract

Hairy root culture (HRC)-based in vitro production system has become a promising biotechnological approach in recent years. The hairy root formation is the result of Agrobacterium rhizogenes-induced pathogenesis in plants, characterized by high growth rate, growth in hormone-free media besides genetic stability. These roots can imitate intact plants in the production of secondary metabolites and also amenable to upscaling in the bioreactor. HRCs are being harnessed as one of the methods of choice in tissue culture for high yield of valuable secondary metabolites of medicinal and other commercial importance. Many secondary metabolites, which were earlier extracted from wild plants from their natural habitat, are now being produced using plant cell cultures including HRCs. This book chapter is focussed mainly on the development of hairy root culture in different medicinal plants and its application, challenges, and prospects in the production of valuable secondary metabolites.

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References

  • Abbott, J. A., Medina-Bolivar, F., Martin, E. M., Engelberth, A. S., Villagarcia, H., Clausen, E. C., & Carrier, D. J. (2010). Purification of resveratrol, arachidin-1, and arachidin-3 from hairy root cultures of peanut (Arachis hypogaea) and determination of their antioxidant activity and cytotoxicity. Biotechnology Progress, 26, 1344–1351.

    Article  PubMed  CAS  Google Scholar 

  • Amdoun, R., Khelifi, L., Khelifi-Slaoui, M., Amroune, S., Asch, M., Assaf-Ducrocq, C., & Gontier, E. (2010). Optimization of the culture medium composition to improve the production of hyoscyamine in elicited Datura stramonium L. hairy roots using the response surface methodology (RSM). International Journal of Molecular Sciences, 11, 4726–4740.

    Article  CAS  Google Scholar 

  • Banerjee, S., Singh, S., & Ur Rahman, L. (2012). Biotransformation studies using hairy root cultures – A review. Biotechnology Advances, 30(3), 461–468.

    Article  PubMed  CAS  Google Scholar 

  • Bapat, V. A., & Ganapathi, T. R. (2005). Hairy roots –A novel source for plant products and improvement. National Academy Science Letters, 28, 61–69.

    CAS  Google Scholar 

  • Baskaran, P., & Jayabalan, N. (2009). Psoralen production in hairy roots and adventitious roots cultures of Psoralea coryfolia. Biotechnology Letters, 31, 1073–1077.

    Article  PubMed  CAS  Google Scholar 

  • Bauer, N., Kiseljak, D., & Jelaska, S. (2009). The effect of yeast extract and methyl jasmonate on rosmarinic acid accumulation in Coleus blumei hairy roots. Biologia Plantarum, 53, 650–656.

    Article  CAS  Google Scholar 

  • Bayindir, U., Alfermann, A., & Fuss, E. (2008). Hinokinin biosynthesis in Linum corymbulosum Reichenb. The Plant Journal, 55, 810–820.

    Article  PubMed  CAS  Google Scholar 

  • Bettini, P., Michelotti, S., Bindi, D., Giannini, R., Capuana, M., & Buiatti, M. (2003). Pleiotropic effect of the insertion of the Agrobacterium rhizogenes rolD gene in tomato (Lycopersicon esculentum mill.). Theoretical and Applied Genetics, 107, 831–836.

    Article  PubMed  CAS  Google Scholar 

  • Cardarelli, M., Mariotti, D., Pomponi, M., Spanò, L., Capone, I., & Costantino, P. (1987a). Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Molecular & General Genetics, 209, 475–480.

    Article  CAS  Google Scholar 

  • Cardarelli, M., Spanò, L., Mariotti, D., Mauro, L., van Sluys, M. A., & Costantino, P. (1987b). The role of auxin in hairy root induction. Molecular & General Genetics, 208, 457–463.

    Article  CAS  Google Scholar 

  • Cardillo, A. B., Otalvaro, A. A. M., Busto, V. D., Talou, J. R., Velasquez, L. M. E., & Giulietti, A. M. (2010). Scopolamine, anisodamine and hyoscya- mine production by Brugmansia candida hairy root cultures in bioreactors. Process Biochemistry, 45, 1577–1581.

    Article  CAS  Google Scholar 

  • Charlwood, B. V., & Charlwood, K. A. (1991). Terpenoid production in plant cell culture. In J. B. Harborne & F. A. Tomas-Barberan (Eds.), Ecological chemistry and biochemistry of plant terpenoids (pp. 95–132). Oxford: Clarendon Press.

    Google Scholar 

  • Chaudhury, A., & Pal, M. (2010). Induction of shikonin production in hairy root cultures of Arnebia hispididdima via Agrobacterium rhizogenes-mediated genetic transformation. Journal of Crop Science and Biotechnology, 13, 99–106.

    Article  Google Scholar 

  • Chilton, M. D., Tepfer, D. A., Petit, A., David, C., Casse-Delbart, F., & Tempe, J. (1982). Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature, 295, 432–434.

    Article  CAS  Google Scholar 

  • Choi, D. W., Jung, J. D., HaY, P. H. 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.

    Article  PubMed  CAS  Google Scholar 

  • Christey, M. C. (2001). Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cellular & Developmental Biology Plant, 37, 687–700.

    Article  CAS  Google Scholar 

  • Costantino, P., Spano, L., Pomponi, M., Benvenuto, E., & Ancora, G. (1984). The T-DNA of Agrobacterium rhizogenes is transmitted through meiosis to the progeny of hairy root plants. Journal of Molecular and Applied Genetics, 2, 465–470.

    PubMed  CAS  Google Scholar 

  • De Boer, K., Dalton, H., Edward, F., & Hamill, J. (2011). RNAi mediated down-regulation of ornithine decarboxylase (ODC) leads to reduced nicotine and increased anatabine levels in transgenic Nicotiana tabacum L. Phytochemistry, 72, 344–355.

    Article  CAS  Google Scholar 

  • Dehio, C., & Schell, J. (1993). Stable expression of a single-copy rolA gene in transgenic Arabidopsis thaliana plants allows an exhaustive mutagenic analysis of the transgene-associated phenotype. Molecular & General Genetics, 241, 359–366.

    CAS  Google Scholar 

  • Dehio, C., Grossmann, K., Schell, J., & Schmulling, T. (1993). Phenotype and hormonal status of transgenic tobacco plants overexpressing the rolA gene of Agrobacterium rhizogenes T-DNA. Plant Molecular Biology, 23, 1199–1210.

    Article  PubMed  CAS  Google Scholar 

  • Drobot, K. O., Matvieieva, N. A., Ostapchuk, A. M., Kharkhota, M. A., & Duplij, V. P. (2017). Study of artemisinin and sugar accumulation in Artemisia vulgaris and Artemisia dracunculus “hairy” root cultures. Preparative Biochemistry & Biotechnology, 23, 1–6.

    Google Scholar 

  • Durand-Tardif, M., Broglie, R., Slightom, J., & Tepfer, D. (1985). Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabacum. Journal of Molecular Biology, 186, 557–564.

    Article  PubMed  CAS  Google Scholar 

  • Eapen, S., & Mitra, R. (2001). Plant hairy root cultures: Prospects and limitations. Proceedings of Indian National Sciences Academy, B67(3&4), 107–120.

    Google Scholar 

  • Estramareix, C., Ratet, P., Boulanger, F., & Richaud, F. (1986). Multiple mutations in the transferred regions of the Agrobacterium rhizogenes root-inducing plasmids. Plasmid, 15, 245.

    Article  PubMed  CAS  Google Scholar 

  • Estruch, J. J., Schell, J., & Spena, A. (1991a). The protein encoded by rolB plant oncogene hydrolyses indoleglucosides. The EMBO Journal, 10, 3125–3128.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Estruch, J. J., Chriqui, D., Grossmann, K., Schell, J., & Spena, A. (1991b). The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. The EMBO Journal, 10, 2889–2895.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Estruch, J. J., Parets-Soler, A., Schmülling, T., & Spena, A. (1991c). Cytosolic localization in transgenic plants of the rolC peptide from Agrobacterium rhizogenes. Plant Molecular Biology, 17, 547–550.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Gai, Q.-Y., Jiao, J., Luo, M., Wei, Z.-F., Zu, Y.-G., Ma, W., et al. (2015). Establishment of hairy root cultures by Agrobacterium rhizogenes mediated transformation of Isatis tinctoria L. for the efficient production of flavonoids and evaluation of antioxidant activities. PLoS One, 10(3), e0119022.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gangopadhyay, M., Dewanjee, S., & Bhattacharya, S. (2011). Enhanced plumbagin production in elicited Plumbago indica hairy root cultures. Journal of Bioscience and Bioengineering, 111, 706–710.

    Article  PubMed  CAS  Google Scholar 

  • Gao, W., Hillwig, M., Huang, L., Cui, G., et al. (2009). A functional genomics approach to tanshinone biosynthesis provides stereochemical insights. Organic Letters, 11, 5170–5173.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Georgiev, V. G., Weber, J., Kneschke, E. M., Denev, P. N., Bley, T., & Pavlov, A. I. (2010). Antioxidant activity and phenolic content of betalain extracts from intact plants and hairy root cultures of the red beet root Beta vulgaris cv. Detroit dark red. Plant Foods for Human Nutrition, 65, 105–111.

    Article  PubMed  CAS  Google Scholar 

  • Georgiev, M. I., Agostini, E., Ludwig-Müller, J., & Xu, J. (2012). Genetically transformed roots: From plant disease to biotechnological resource. Trends in Biotechnology, 30(10), 528–537.

    Article  PubMed  CAS  Google Scholar 

  • Giri, A., & Narasu, M. L. (2000). Transgene hairy roots: Recent trends and application. Biotechnology Advances, 18, 1–22.

    Article  PubMed  CAS  Google Scholar 

  • Goklany, S., Loring, R. H., Glick, J., & Lee-Parsons, C. W. T. (2010). Assessing the limitations to terpenoid indole alkaloid biosynthesis in Catharanthus roseus hairy root cultures through gene expression profiling and precursor feeding. Biotechnology Progress, 25, 1289–1296.

    Article  CAS  Google Scholar 

  • Guillon, S., Trémouillaux-Guiller, J., Pati, P. K., Rideau, M., & Gantet, P. (2006). Harnessing the potential of hairy roots: Dawn of a new era. Trends in Biotechnology, 24(9), 403–409.

    Article  PubMed  CAS  Google Scholar 

  • Häkkinen, S. T., Moyano, E., Cusidó, R. M., & Oksman-Caldentey, K. M. (2016). Exploring the metabolic stability of engineered hairy roots after 16 years maintenance. Frontiers in Plant Science, 7, 1486.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hildebrand, E. (1934). Life history of the hairy-root organism in relation to its pathogenesis on nursery apple trees. Journal of Agricultural Research, 48, 857–885.

    Google Scholar 

  • Hu, Z. B., & Du, M. (2006). Hairy root and its application in plant genetic engineering. Journal of Integrative Plant Biology, 48(2), 121–127.

    Article  CAS  Google Scholar 

  • Jaber-Vazdekis, N., Barres, M. L., Ravelo, A. G., & Zarate, R. (2008). Effects of elicitors on tropane alkaloids and gene expression in Atropa baetica transgenic hairy roots. Journal of Natural Products, 71, 2026–2031.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, Y. N., Wang, B., Li, H., Yao, L. M., et al. (2010). Flavonoid production is effectively regulated by RNAi interference of two flavone synthase genes from Glycine max. J Plant Biol, 53, 425–432.

    Google Scholar 

  • Jung, J. D., Park, H. W., Hahn, Y., Hur, C. G., et al. (2003). Discovery of genes for ginsenoside biosynthesis by analysis of ginseng expressed sequence tags. Plant Cell Reports, 22, 224–230.

    Article  PubMed  CAS  Google Scholar 

  • Kai, G., Xu, H., Zhou, C., Liao, P., Xiao, J., Luo, X., You, L., & Zhang, L. (2011). Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metabolic Engineering, 13, 319–327.

    Article  PubMed  CAS  Google Scholar 

  • Kai, G., Yang, S., Zhang, Y., Luo, X., et al. (2012). Effects of different elicitors on yield of tropane alkaloids in hairy roots of Anisodus acutangulus. Molecular Biology Reports, 39, 1721–1729.

    Article  PubMed  CAS  Google Scholar 

  • Kajikawa, M., Hirai, N., & Hashimoto, T. (2009). APIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Molecular Biology, 69, 287–298.

    Article  PubMed  CAS  Google Scholar 

  • Kastell, A. (2009). Induction of hairy root culture by Agrobacterium rhizogenes in different Brassica plants impact of phytohormones and precursors in the glucosinolates accumulation. Diploma thesis (Diplomarbeit in german), Berlin University of Technology.

    Google Scholar 

  • Kim, Y. J., Wyslouzil, B. E., & Weathers, P. J. (2002). Invited review: Secondary metabolism of hairy root cultures in bioreactors. In Vitro Cellular & Developmental Biology Plant, 38, 1–10.

    Article  CAS  Google Scholar 

  • Kim, O. T., Bang, K. H., Kim, Y. C., Hyun, D. Y., et al. (2009). Upregulation of ginsenoside and gene expression related to triterpene biosynthesis in ginseng hairy root cultures elicited by methyl jasmonate. Plant Cell Tissue and Organ Culture, 98, 25–33.

    Article  CAS  Google Scholar 

  • Kim, O. T., Kim, S. H., Ohyama, K., Muranaka, T., et al. (2010a). Upregulation of phytosterol and triterpene biosynthesis in Centella asiatica hairy roots over expressed ginseng farnesyl diphosphate synthase. Plant Cell Reports, 29, 403–411.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y. K., Xu, H., Park, W. T., Park, N. I., Lee, S. Y., & Park, S. U. (2010b). Genetic transformation of buckwheat (Fagopyrum esculentum M.) with Agrobacterium rhizogenes and production of rutin in trans- formed root cultures. Australian Journal of Crop Science, 4, 485–490.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kuzma, L., Bruchajzer, E., & Wysokinska, H. (2009). Methyl jasmonate effect on diterpenoid accumulation in Salvia sclarea hairy root culture in shake flasks and sprinkle bioreactor. Enzyme and Microbial Technology, 44, 406–410.

    Article  CAS  Google Scholar 

  • Levesque, H., Delepelaire, P., Rouze, P., Slightom, J., & Tepfer, D. (1988). Common evolutionary origin of the central portions of the Ri TLDNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens. Plant Molecular Biology, 11, 731–744.

    Article  PubMed  CAS  Google Scholar 

  • Ling, A. P. K., Ong, S. L., & Sobri, H. (2011). Strategies in enhancing secondary metabolites production in plant cell cultures. Medicinal and Aromatic Plant Science and Biotechnology, 5(2), 94–101.

    Google Scholar 

  • Liu, C. Z., Wang, Y. C., Zhao, B., Guo, C., Ouyang, F., Ye, H. C., & Li, G. F. (1999). Development of a nutrient mist bioreactor for growth of hairy roots. In Vitro Cellular & Developmental Biology. Plant, 35, 271–274.

    Article  Google Scholar 

  • Ludwig-Muller, J., Georgiev, M., & Bley, T. (2008). Metabolite and hormonal status of hairy root cultures of Devail’s claw (Harpagophytum procumbens) in flaks and in a bubble column bioreactor. Process Biochemistry, 43, 15–23.

    Article  CAS  Google Scholar 

  • Martin-Tanguy, J. (2001). Metabolism and function of polyamines in plants: Recent development (new approaches). Plant Growth Regulation, 34, 135–148.

    Article  CAS  Google Scholar 

  • Martin-Tanguy, J., Sun, Y., Burtin, D., Vernoy, R., Rossin, N., & Tepfer, D. (1996). Attenuation of the phenotype caused by the root-inducing, left hand, transferred DNA and its rolA gene (correlations with changes in polyamine metabolism and DNA methylation). Plant Physiology, 111, 259–267.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mathur, A., Gangwar, A., Mathur, A. K., Verma, P., Uniyal, G. C., & Lal, R. K. (2010). Growth kinetics and ginsenosides production in trans- formed hairy roots of American ginseng-Panax quinquefolium L. Biotechnology Letters, 32, 457–461.

    Article  PubMed  CAS  Google Scholar 

  • Maurel, C., Barbier-Brygoo, H., Spena, A., Tempe, J., & Guern, J. (1991). Single rol genes from the Agrobacterium rhizogenes T(L)-DNA alter some of the cellular responses to auxin in Nicotianatabacum. Plant Physiology, 97, 212–216.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maurel, C., Leblanc, N., Barbier-Brygoo, H., Perrot-Rechenmann, C., Bouvier-Durand, M., & Guern, J. (1994). Alterations of auxin perception in rolB-transformed tobacco protoplasts. Time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin. Plant Physiology, 105, 1209–1215.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mauro, M. L., Trovato, M., Paolis, A. D., Gallelli, A., Costantino, P., & Altamura, M. M. (1996). The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Developmental Biology, 180, 693–700.

    Article  PubMed  CAS  Google Scholar 

  • Mehrotra, S., Rahman, L. U., & Kukreja, A. K. (2010). An extensive case study of hairy-root cultures for enhanced secondary-metabolite production through metabolic-pathway engineering. Biotechnology and Applied Biochemistry, 56(4), 161–172.

    Article  PubMed  CAS  Google Scholar 

  • Meyer, A., Tempe, J., & Costantino, P. (2000). Hairy root: A molecular overview functional analysis of Agrobacterium rhizogenes T-DNA genes. In G. Stacey & N. Keen (Eds.), Plant-microbe interactions (Vol. 5, pp. 93–139). St. Paul: APS Press.

    Google Scholar 

  • Min, J. Y., Jung, H. Y., Kang, S. M., Kim, Y. D., Kang, Y. M., Park, D. J., Prasad, D. T., & Choi, M. S. (2007). Production of tropane alkaloids by small-scale bubble column bioreactor cultures of Scopolia parviflora adventitious roots. Bioresource Technology, 98, 1748–1753.

    Article  PubMed  CAS  Google Scholar 

  • Moharrami, F., Hosseini, B., Sharafi, A., & Farjaminezhad, M. (2017). Enhanced production of hyoscyamine and scopolamine from genetically transformed root culture of Hyoscyamus reticulatus L. elicited by iron oxide nanoparticles. In Vitro Cellular & Developmental Biology Plant, 53(2), 104–111.

    Article  CAS  Google Scholar 

  • Moore, L., Warren, G., & Strobel, G. (1979). Involvement of a plasmid in the hairy root disease of plants caused by Agrobacterium rhizogenes. Plasmid, 2, 617–626.

    Article  PubMed  CAS  Google Scholar 

  • Moriguchi, K., Maeda, Y., Satou, M., Hardayani, N. S., Kataoka, M., Tanaka, N., & Yoshida, K. (2001). The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rhizobiaceae. Journal of Molecular Biology, 307, 771–784.

    Article  PubMed  CAS  Google Scholar 

  • Moyano, E., Jouhikainen, K., Tammela, P., Palazoan, J., et al. (2003). Effect of pmt gene overexpression on tropane alkaloid production in transformed root cultures of Datura metel and Hyoscyamus muticus. Journal of Experimental Botany, 54, 203–211.

    Article  PubMed  CAS  Google Scholar 

  • Murthy, H. N., Dijkstra, C., Anthony, P., White, D. A., Davey, M. R., Power, J. B., Hahn, E. J., & Paek, K. Y. (2008). Establishment of Withania somnifera hairy root cultures for the production of withanolide A. Journal of Integrative Plant Biology, 50(8), 975–981.

    Article  PubMed  CAS  Google Scholar 

  • Nandagopal, K., Halder, M., Dash, B., Nayak, S., & Jha, S. (2017). Biotechnological approaches for production of anti-cancerous compounds resveratrol, podophyllotoxin and zerumbone. Current Medicinal Chemistry. https://doi.org/10.2174/0929867324666170404145656.

  • Nilsson, O., & Olsson, O. (1997). Getting to the root: The role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiologia Plantarum, 100, 463–473.

    Article  CAS  Google Scholar 

  • Nilsson, O., Crozier, A., Schmülling, T., Sandberg, G., & Olsson, O. (1993a). Indole-3-acetic acid homeostasis in transgenic tobacco plants expressing the Agrobacterium rhizogenes rolB gene. The Plant Journal, 3, 681–689.

    Article  CAS  Google Scholar 

  • Nilsson, O., Moritz, T., Imbault, N., Sandberg, G., & Olsson, O. (1993b). Hormonal characterization of transgenic tobacco plants expressing the rolC gene of Agrobacterium rhizogenes TL-DNA. Plant Physiology, 102, 363–371.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okuzumi, K., Hara, N., Fujimoto, Y., Yamada, J., et al. (2003). Biosynthesis of phytoecdysteroids in Ajuga hairy roots: Clerosterol as a precursor of cyasterone, isocyasterone and 29-norcyasterone. Tetrahedron Letters, 44, 323–326.

    Article  CAS  Google Scholar 

  • Pang, Y., Peel, G. J., Sharma, S. B., Tang, Y., et al. (2008). A transcript profiling approach reveals an epicatechin-specific glucosyl transferase expressed in the seed coat of Medicago truncatula. Proceedings of the National Academy of Sciences of the United States of America, 105, 14210–14215.

    Article  PubMed  PubMed Central  Google Scholar 

  • Phelep, M., Petit, A., Martin, L., Duhoux, E., & Tempe, J. (1991). Transformation and regeneration of a nitrogen-fixing tree, Allocasuarina verticillata Lam. Bio-Tech, 9, 461–466.

    CAS  Google Scholar 

  • Prinsen, E., Chriqui, D., Vilaine, F., Tepfer, M., & Van Onckelen, H. (1994). Endogenous phytohormones in tobacco plants transformed with Agrobacterium rhizogenesp Ri TL-DNA genes. Plant Physiology, 144, 80–85.

    Article  CAS  Google Scholar 

  • Riker, A. J., Banfield, W. M., Wright, W. H., Keitt, G. W., & Sagen, H. E. (1930). Studies on infectious hairy root of nursery-apple tree. Journal of Agricultural Research, 41, 507–540.

    Google Scholar 

  • Satdive, R. K., Fulzele, D. P., & Eapen, S. (2007). Enhanced production of azadirachtin by hairy root cultures of Azadirachta indica A. Juss by elicitation and media optimization. Journal of Biotechnology, 128(2), 281–289.

    Article  PubMed  CAS  Google Scholar 

  • Schmulling, T., Schell, J., & Spena, A. (1988). Single genes from Agrobacterium rhizogenes influence plant development. The EMBO Journal, 7, 2621–2629.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmülling, T., Fladung, M., Grossmann, K., & Schell, J. (1993). Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. The Plant Journal, 3, 371–382.

    Article  Google Scholar 

  • Sevon, N., & Oksman-Caldentey, K. M. (2002). Agrobacterium rhizogenes mediated transformation: Root cultures as a source of alkaloids. Planta Medica, 68, 859–868.

    Article  PubMed  CAS  Google Scholar 

  • Shen, W. H., Davioud, E., David, C., Barbier-Brygoo, H., Tempe, J., & Guern, J. (1990). High sensitivity to auxin is a common feature of hairy root. Plant Physiology, 94, 554–560.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shinde, A. N., 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.

    Article  PubMed  CAS  Google Scholar 

  • Singh, R. S., Gara, R. K., Bhardwaj, P. K., Kaachra, A., Malik, S., Kumar, R., Sharma, M., Ahuja, P. S., & Kumar, S. (2010). Expression of 3-hydroxy-3-methylglutaryl-CoA reductase, p-hydroxybenzoate-m-geranyltransferase and genes of phenylpropanoid pathway exhibits positive correlation with shikonins content in arnebia [Arnebia euchroma (Royle) Johnston]. BMC Molecular Biology, 11, 88.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sircar, D., & Mitra, A. (2009). Accumulation of p-hydroxybenzoic acid in hairy roots of Daucus carota: Confirming biosynthetic steps through feeding of inhibitors and precursors. Journal of Plant Physiology, 166, 1370–1380.

    Article  PubMed  CAS  Google Scholar 

  • Sirikantaramas, S., Sudo, H., Asano, T., Yamazaki, M., et al. (2007). Transport of camptothecin in hairy roots of Ophiorrhiza pumila. Phytochemistry, 68, 2881–2886.

    Article  PubMed  CAS  Google Scholar 

  • Sivakumar, G. (2006). Bioreactor technology: A novel industrial tool for high-tech production of bioactive molecules and biopharmaceuticals from plant roots. Biotechnology Journal, 1(12), 1419–1427.

    Article  PubMed  CAS  Google Scholar 

  • Skorupinska-Tudek, K., Poznanski, J., Wojcik, J., Bienkowski, T., et al. (2008). Contribution of the mevalonate and methyl erythritol phosphate pathways to the biosynthesis of dolichols in plants. The Journal of Biological Chemistry, 283, 21024–21035.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Slightom, J. L., Durand-Tardif, M., Jouanin, L., & Tepfer, D. (1986). Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenesagropine type plasmid. Identification of open reading frames. The Journal of Biological Chemistry, 261, 108–121.

    PubMed  CAS  Google Scholar 

  • Spanò, L., Pomponi, M., Costantino, P., Van Slogteren, G. M. S., & Tempé, J. (1982). Identification of T-DNA in the root-inducing plasmid of the agropine-type Agrobacterium rhizogenes 1855. Plant Molecular Biology, 1, 291–300.

    Article  PubMed  Google Scholar 

  • Spena, A., Schmülling, T., Koncz, C., & Schell, J. (1987). Independent and synergistic activity of rolA, B and C loci in stimulating abnormal growth in plants. The EMBO Journal, 6(3), 891–3899.

    Google Scholar 

  • Srivastava, S., & Srivastava, A. K. (2007). Hairy root culture for mass-production of high-value secondary metabolites. Critical Reviews in Biotechnology, 27(1), 29–43.

    Article  PubMed  CAS  Google Scholar 

  • Srivastava, M., Sharma, S., & Misra, P. (2016). Elicitation based enhancement of secondary metabolites in Rauwolfia serpentine and Solanum khasianum hairy root cultures. Pharmacognosy Magazine, 12(Suppl 3), S315–S320.

    PubMed  PubMed Central  Google Scholar 

  • Sun, L.-Y., Monneuse, M.-O., Martin-Tanguy, J., & Tepfer, D. (1991). Changes in flowering and accumulation of polyamines and hydroxycinnamic acid-polyamine conjugates in tobacco plants transformed by the rolA locus from the Ri TL-DNA of Agrobacterium rhizogenes. Plant Science, 80, 145–146.

    Article  CAS  Google Scholar 

  • Suzuki, M. (1989). SPXX, a frequent sequence motif in gene regulatory proteins. Journal of Molecular Biology, 207(1):61–84.

    Google Scholar 

  • Syklowska-Baranek, K., Pietrosiuk, A., Kokoszka, A., & Furmanowa, M. (2009). Enhancement of taxane production in hairy root culture of Taxus x media var. Hicksii. Journal of Plant Physiology, 166, 1950–1954.

    Article  PubMed  CAS  Google Scholar 

  • Tepfer, D. (1990). Genetic transformation using Agrobacterium rhizogenes. Physiologia Plantarum, 79, 140–146.

    Article  CAS  Google Scholar 

  • Terrier, N., Torregrosa, L., Ageorges, A., Vialet, S., et al. (2009). Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiology, 149, 1028–1041.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tisserant, L. P., Aziz, A., Jullian, N., Jeandet, P., Clément, C., Courot, E., & Boitel-Conti, M. (2016). Enhanced stilbene production and excretion in Vitis vinifera cv pinot noir hairy root cultures. Molecules, 21(12), pii: E1703.

    Article  CAS  Google Scholar 

  • Trovato, M., Maras, B., Linhares, F., & Constantino, P. (2001). The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proceedings of the National Academy of Sciences of the United States of America, 98, 13449–13453.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Udomsom, N., Rai, A., Suzuki, H., Okuyama, J., Imai, R., Mori, T., Nakabayashi, R., Saito, K., & Yamazaki, M. (2016). Function of AP2/ERF transcription factors involved in the regulation of specialized metabolism in Ophiorrhiza pumila revealed by transcriptomics and metabolomics. Frontiers in Plant Science, 7, 1861.

    Article  PubMed  PubMed Central  Google Scholar 

  • van Altvorst, A. C., Bino, R. J., van Dijk, A. J., Lamers, A. M. J., Lindhout, W. H., van der Mark, F., & Dons, J. J. M. (1992). Effects of the introduction of Agrobacterium rhizogenesrol genes on tomato plant and flower development. Plant Science, 83, 77–85.

    Article  Google Scholar 

  • Veena, V., & Taylor, C. G. (2007). Agrobacterium rhizogenes: Recent developments and promising applications. In Vitro Cellular & Developmental Biology. Plant, 43, 383–403.

    Article  CAS  Google Scholar 

  • Verma, P. C., Trived, I., Singh, H., Shukla, A. K., Kumar, M., Upadhyay, S. K., Pandey, P., Hans, A. L., & Singh, P. K. (2009). Efficient production of gossypol from hairy root cultures of cotton (Gossypium hirsutum L.). Current Pharmaceutical Biotechnology, 10, 691–700.

    Article  PubMed  CAS  Google Scholar 

  • Vilaine, F., Charbonnier, C., & Casse-Delbart, F. (1987). Further insight concerning the TL-region of the Ri plasmid of Agrobacterium rhizogenes strain A4: Transfer of a 1.9 kb fragment is sufficient to induce transformed roots on tobacco leaf fragments. Molecular & General Genetics, 210, 111–115.

    Article  CAS  Google Scholar 

  • Wang, C. T., Liu, H., Gao, X. S., & Zhang, H. X. (2010). Overexpression of G10H and ORCA3 in the hairy roots of Catharanthus roseus improves catharanthine production. Plant Cell Reports, 29, 887–894.

    Article  PubMed  CAS  Google Scholar 

  • White, F. F., & Nester, E. W. (1980). Hairy root: Plasmid encodes virulence traits in Agrobacterium rhizogenes. Journal of Bacteriology, 141, 1134–1141.

    PubMed  PubMed Central  CAS  Google Scholar 

  • White, F. F., Taylor, B. H., Huffman, G. A., Gordon, M. P., & Nester, E. W. (1985). Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. Journal of Bacteriology, 164, 33–44.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wielanek, M., & Urbanek, H. (2006). Enhanced glucotropaeolin production in hairy root cultures of Tropaeolum majus(L.) by combining elicitation and precursor feeding. Plant Cell, Tissue and Organ Culture, 86, 177–186.

    Article  CAS  Google Scholar 

  • Xiao, Y., Gao, S., Peng, D., Chen, J., et al. (2010). Lithospermic acid B is more responsive to silver ions (ag+) than rosmarinic acid in Salvia miltiorrhiza hairy root cultures. Bioscience Reports, 30, 33–40.

    Article  CAS  Google Scholar 

  • Yadav, N. S., Van der Leyden, J., Bennett, D. R., Barnes, W. M., & Chilton, M.-D. (1982). Short direct repeats flank the T-DNA on a nopaline Ti plasmid. Proceedings of the National Academy of Sciences of the United States of America, 79, 6322–6326.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamazaki, Y., Kitajima, M., Arita, M., Takayama, H., et al. (2004). Biosynthesis of camptothecin. In silico and in vivo tracer study from [1–13C] glucose. Plant Physiology, 134, 161–170.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan, Q., Shi, M., Ng, J., & Wu, J. Y. (2006). Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Science, 170, 853–858.

    Article  CAS  Google Scholar 

  • Yan, Q., Wu, J., & Liu, R. (2011). Modeling of tanshinone synthesis and phase distribution under the combined effect of elicitation and in situ adsorption in Salvia miltiorrhiza hairy root cultures. Biotechnology Letters, 33, 813–819.

    Article  PubMed  CAS  Google Scholar 

  • Yang, D., Ma, P., Liang, X., Liang, Z., et al. (2012). Metabolic profiles and cDNA-AFLP analysis of Salvia miltiorrhiza and Salviacastanea Diel f. tomentosa Stib. PLoS One, 7, e29678.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yi, J., Derynck, M. R., Li, X., Telmer, P., et al. (2010). A single repeat Myb transcription factor, GmMYB176, regulates CHS8 gene expression and affects isoflavonoid biosynthesis in soybean. The Plant Journal, 62, 1019–1034.

    PubMed  CAS  Google Scholar 

  • Zang, Y. X., Kim, D. H., Park, B. S., & Hong, S. B. (2009). Metabolic engineering of indole glucosinolates in chinese cabbage hairy roots express- ing Arabidopsis CYP79B2, CYP79B3, and CYP83B1. Biotechnology and Bioprocess Engineering, 14, 467–473.

    Article  CAS  Google Scholar 

  • Zhai, D. D., & Zhong, J. J. (2010). Simultaneous analysis of three bioactive compounds in Artemisia annua hairy root cultures by reversed-phase high-performance liquid chromatography-diode array detector. Phytochemical Analysis, 21, 524–530.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, H. L., Xue, S. H., Pu, F., Tiwari, R. K., & Wang, X. Y. (2010). Establishment of hairy root lines and analysis of gentiopicroside in the medicinal plant Gentiana macrophylla. Russian Journal of Plant Physiology, 57, 110–117.

    Article  CAS  Google Scholar 

  • Zhao, B. (2014). Alkaloid production by hairy root cultures. All graduate theses and dissertations. Paper 3884. Utah State University Logan Utah.

    Google Scholar 

  • Zhou, M. L., Zhu, X. M., Shao, J. R., Wu, Y. M., et al. (2010). Transcriptional response of the catharanthine biosynthesis pathway to methyl jasmonate/nitric oxide elicitation in Catharanthus roseus hairy root culture. Applied Microbiology and Biotechnology, 88, 737–750.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Depeartment of Plant Breeding and Genetics, Bihar Agricultural University, Bhagalpur, Bihar, India

    Ravi Shankar Singh, Tirthartha Chattopadhyay & Prabhash Kumar Singh

  2. Depeartment of Molecular Biology and Genetic Engineering, Bihar Agricultural University, Bhagalpur, Bihar, India

    Dharamsheela Thakur

  3. Department of Biotechnology, School of Earth, Biological and Environmental Sciences, Central University of South Bihar, Gaya, Bihar, India

    Nitish Kumar

  4. Depeartment of Plant Breeding and Genetics, Mandan Bharti Agricultural College (Bihar Agricultural University), Saharsa, Bihar, India

    Tribhuwan Kumar

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  1. Ravi Shankar Singh
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  1. Department of Biotechnology, Central University of South Bihar, Panchanpur, Gaya, Bihar, India

    Nitish Kumar

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Singh, R.S., Chattopadhyay, T., Thakur, D., Kumar, N., Kumar, T., Singh, P.K. (2018). Hairy Root Culture for In Vitro Production of Secondary Metabolites: A Promising Biotechnological Approach. In: Kumar, N. (eds) Biotechnological Approaches for Medicinal and Aromatic Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-0535-1_10

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