The Current Status and Future Applications of Hairy Root Cultures

Dhiman, Nisha; Patial, Vanita; Bhattacharya, Amita

doi:10.1007/978-981-13-0535-1_5

Nisha Dhiman^2,3^na1,
Vanita Patial^2,3^na1 &
Amita Bhattacharya^2,3^na1

1500 Accesses
9 Citations

Abstract

Hairy roots are produced when the soil phytopathogen, Agrobacterium rhizogenes, infects a host plant. Just like normal roots, the hairy roots have the capacity to absorb target elements and produce valuable phytochemicals. Hairy roots have thus been exploited in applications like large-scale production of secondary metabolites and recombinant proteins, upscaling in bioreactors, phytomining and phytoremediation. The hairy roots have industrial applications and are used as important research tool for elucidation of secondary metabolite biosynthetic pathways and also expression and function of key genes and regulatory elements. The status of research conducted till date on hairy roots of medicinally important plants with respect to secondary metabolites production, elicitation, recombinant proteins, genetic manipulation, phytoremediation and phytomining is reviewed in the present chapter.

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Hairy Root Culture for the Production of Useful Secondary Metabolites

Hairy Root Culture: Secondary Metabolite Production in a Biotechnological Perspective

Advances in Transformed Root Cultures for Root Biofactory and Phytoremediation Research

Abbreviations

ABA:: Abscisic acid
ASA:: Acetylsalicylic acid
AS:: Acetosyringone
BA:: Benzyladenine
BAP:: 6-Benzylamino purine
B5:: Gamborg’s B5 medium (Gamborg et al. 1968)
bp:: Base pair
Cd:: Cadmium
2, 4-D:: 2, 4-Dichlorophenoxy acetic acid
2, 4-DCP:: 2, 4-Dichlorophenol
4′-DM6MPTOX:: 4′-Demethyl-6-methoxy podophyllotoxin
DDT:: Dichlorodiphenyltrichloroethane
H₂O₂ :: Hydrogen peroxide
IAA:: Indole-3-acetic acid
IBA:: Indole-3-butyric acid
JA:: Jasmonic acid
Kn:: Kinetin
kb:: Kilobase
L-DOPA:: L-3, 4-dihydroxyphenylalanine
L:: Litre
LS:: Linsmaier and Skoog medium (Linsmaier and Skoog 1965)
MES:: 2-(N-morpholino)ethanesulfonic acid
MPTOX:: 6-Methoxy podophyllotoxin
MS:: Murashige and Skoog medium (Murashige and Skoog 1962)
MSRT:: MS + *RT vitamin complex (Khanna and Staba 1968)
NAA:: α-Naphthalene acetic acid
Ni:: Nickel
NiSO₄ :: Nickel sulphate
MeJa:: Methyl jasmonate
mM:: Millimole
nM:: Nanomole
PCBs:: Polychlorinated biphenyls
pM:: Picomole
ppm:: Parts per million
rpm:: Revolutions per minute
SA:: Salicylic acid
SH:: Schenk and Hildebrandt medium (Schenk and Hildebrandt 1972)
TCE:: Trichloroethylene
TDZ:: Thidiazuron
TNT:: 2, 4, 6-Trinitrotoluene
μM:: Micromole
UM:: Uchimiya and Murashige medium (Uchimiya and Murashige 1974)
U:: Uranium
WPM:: Woody Plant Medium (Lloyd and McCown 1981)
YE:: Yeast extract
YPS:: Yeast polysaccharide

References

Abbasi, B. H., Liu, R., Saxena, P. K., & Liu, C. Z. (2009). Cichoric acid production from hairy root cultures of Echinacea purpurea grown in a modified airlift bioreactor. Journal of Chemical Technology and Biotechnology, 84, 1697–1701. https://doi.org/10.1002/jctb.2233.
Article CAS Google Scholar
Agostini, E., Coniglio, M. S., Milrad, S. R., Tigier, H. A., & Giulietti, A. M. (2003). Phytoremediation of 2, 4-dichlorophenol by Brassica napus hairy root cultures. Biotechnology and Applied Biochemistry, 37, 139–144.
Article PubMed CAS Google Scholar
Alderete, L. G. S., Talano, M. A., Ibáñez, S. G., Purro, S., Agostini, E., Milrad, S. R., & Medina, M. I. (2009). Establishment of transgenic tobacco hairy roots expressing basic peroxidases and its application for phenol removal. Journal of Biotechnology, 139(4), 273–279.
Article CAS Google Scholar
Allan, E. J., Eeswara, J. P., Jarvis, A. P., Mordue (Luntz), A. J., Morgan, E. D., & Stuchbury, T. (2002). Induction of hairy root cultures of Azadirachta indica A. Juss. and their production of azadirachtin and other important insect bioactive metabolites. Plant Cell Reports, 21, 374–379. https://doi.org/10.1007/s00299-002-0523-3.
Article CAS Google Scholar
Al-Shalabi, Z., & Doran, P. M. (2013). Metal uptake and nanoparticle synthesis in hairy root cultures. In P. Doran (Ed.), Biotechnology of Hairy Root Systems. Advances in Biochemical Engineering/Biotechnology (Vol. 134). Berlin/Heidelberg: Springer.
Google Scholar
Angelini, V. A., Agostini, E., Medina, M. I., & González, P. S. (2014). Use of hairy roots extracts for 2, 4-DCP removal and toxicity evaluation by Lactuca sativa test. Environmental Science and Pollution Research, 21, 2531–2539.
Google Scholar
Araujo, B. S., Charlwood, V. B., & Pletsch, M. (2002). Tolerance and metabolism of phenol and chloroderivatives by hairy root cultures of Daucus carota L. Environmental Pollution, 117, 329–335.
Article PubMed Google Scholar
Araujo, B. S., Dec, J., Bollag, J. M., & Pletsch, M. (2006). Uptake and transformation of phenol and chlorophenols by hairy root cultures of Daucus carota, Ipomoea batatas and Solanum aviculare. Chemosphere, 63(4), 642–651.
Article PubMed CAS Google Scholar
Arellano, J., Vazquez, F., Villegas, T., & Hernandez, G. (1996). Establishment of transformed root cultures of Perezia cuernavacana producing the sesquiterpene quinone perezone. Plant Cell Reports, 15, 455–458.
Article PubMed CAS Google Scholar
Asada, Y., Saito, H., Yoshikawa, T., Sakamoto, K., & Furuya, T. (1993). Biotransformation of 18/3-glycyrrhetinic acid by Ginseng hairy root culture. Phytochemistry, 34(4), 1049–1052.
Article PubMed CAS Google Scholar
Bai, A. L. G., & Agastian, P. (2013). Agrobacterium rhizogenes mediated hairy root induction for increased colchicine content in Gloriosa superba L. Journal of Academia and Industrial Research (JAIR), 2(1), 68–73.
Google Scholar
Bais, H. P., Sudha, G., & Ravishankar, G. A. (2000). Enhancement of growth and coumarin production in hairy root cultures of Cichorium intybus, L. cv. Lucknow Local (Witloof Chicory) under the influence of fungal elicitors. Journal of Bioscience and Bioengineering, 90, 640–645.
Article Google Scholar
Bais, H. P., Suresh, B., Raghavarao, K. S. M. S., & Ravishankar, G. A. (2002). Performance of hairy root cultures of Cichorium intybus l. in bioreactors of different configurations. In Vitro Cellular & Developmental Biology. Plant, 38, 573–580.
Article CAS Google Scholar
Bálványos, L., Kursinszki, L., & Szõke, E. (2001). The effect of plant growth regulators on biomass formation and lobeline production of Lobelia inflata L. hairy root cultures. Plant Growth Regulation, 34, 339–345.
Article Google Scholar
Banerjee, S., Naqvil, A. A., Mandalt, S., & Ahuja, P. S. (1994). Transformation of Withania somnifera (L) Dunal by Agrobacterium rhizogenes: infectivity and phytochemical studies. Phytotherapy Research, 8, 452–455.
Google Scholar
Banerjee, S., Shang, T. Q., Wilson, A. M., Moore, A. L., Strand, S. E., Gordon, M. P., & Doty, S. L. (2002). Expression of functional mammalian P450 2E1 in hairy root cultures. Biotechnology and Bioengineering, 77(4), 462–466.
Article PubMed CAS Google Scholar
Banerjee, S., Madhusudanan, K. P., Chattopadhyay, S. K., Rahman, L. U., & Khanuja, S. P. S. (2008). Expression of tropane alkaloids in the hairy root culture of Atropa acuminata substantiated by DART mass spectrometric technique. Biomedical Chromatography, 22, 830–834.
Article PubMed CAS Google Scholar
Bányai, P., Bálványos, I., Kursinszki, L., & Szőke, É. (2003). Cultivation of Lobelia inflata L. hairy root culture in bioreactor. Acta Horticulturae, (597), 253–256.
Google Scholar
Baskaran, P., & Jayabalan, N. (2009). Psoralen production in hairy roots and adventitious roots cultures of Psoralea corylifolia. Biotechnology Letters, 31, 1073–1077. https://doi.org/10.1007/s10529-009-9957-9.
Belabbassi, O., Khelifi-Slaoui, M., Zaoui, D., Benyammi, R., Khalfallah, N., Malik, S., Makhzoum, A., & Khelifi, L. (2016). Synergistic effects of polyploidization and elicitation on biomass and hyoscyamine content in hairy roots of Datura stramonium. Biotechnologie, Agronomie, Société et Environnement, 20, 408–416.
CAS Google Scholar
Bhadra, R., Vani, S., & Shank, J. V. (1993). Production of indole alkaloids by selected hairy root lines of Catharanthus roseus. Biotechnology and Bioengineering, 41, 581–592.
Google Scholar
Boominathan, R., & Doran, P. M. (2003). Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnology and Bioengineering, 83, 158–167.
Article PubMed CAS Google Scholar
Boominathan, R., Saha-Chaudhury, N. M., Sahajwalla, V., & Doran, P. M. (2004). Production of nickel bio-ore from hyperaccumulator plant biomass: applications in phytomining. Biotechnology and Bioengineering, 86, 243–250.
Article PubMed CAS Google Scholar
Borkataky, M., Kakoti, B. B., & Saikia, L. R. (2014). Analysis of primary and secondary metabolite profile of Costus speciosus (Koen Ex.Retz.) Sm. rhizome. Journal of Natural Product and Plant Resources, 4(3), 71–76.
Google Scholar
Brooks, R. R., & Robinson, B. H. (1998). The potential use of hyperaccumulators and other plants for phytomining. In R. R. Brooks (Ed.), Plants that hyperaccumulate heavy metals (pp. 327–356). Wallingford: CAB International.
Google Scholar
Buitelaar, R. M., Langenhoff, A. A. M., Heidstra, R., & Tramper, J. (1991). Growth and thiophene production by hairy root cultures of Tagetes patula in various two-liquid-phase bioreactors. Enzyme and Microbial Technology, 13, 487–494.
Article CAS Google Scholar
Bulgakov, V. P., Khodakovskaya, M. V., Labetskaya, N. V., Chernoded, G. K., & Zhuravle, Y. N. (1998). The impact of plant rolC oncogene on ginsenoside production by Ginseng hairy root cultures. Phytochemistry, 49(7), 1929–1934.
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 hyoscyamine production by Brugmansia candida hairy root cultures in bioreactors. Process Biochemistry, 45, 1577–1581.
Article CAS Google Scholar
Carrizo, C. N., Pitta-Alvareza, S. I., Koganb, M. J., Giuliettia, A. M., & Tomaro, M. L. (2001). Occurrence of cadaverine in hairy roots of Brugmansia candida. Phytochemistry, 57, 759–763.
Article PubMed CAS Google Scholar
Caspeta, L., Quintero, R., & Villarreal, M. L. (2005). Novel airlift reactor fitting for hairy root cultures: Developmental and performance studies. Biotechnology Progress, 21, 735–740.
Google Scholar
Celma, C. R., Palazon, J., Cusido, R. M., Pinol, M. T., & Keil, M. (2001). Decreased scopolamine yield in field-grown Duboisia plants regenerated from hairy roots. Planta Medica, 67(7), 249–253.
Google Scholar
Chashmi, N. A., Sharifi, M., Karimi, F., & Rahnama, H. (2010). Differential production of tropane alkaloids in hairy roots and in vitro cultured two accessions of Atropa belladonna L under nitrate treatments. Zeitschrift für Naturforschung. Section C, 65, 373–379.
Google Scholar
Chaudhury, A., & Pal, M. (2010). Induction of shikonin production in hairy root cultures of Arnebia hispidissima via Agrobacterium rhizogenes-mediated genetic transformation. Journal of Crop Science and Biotechnology, 13(2), 99–106.
Article Google Scholar
Chen, H., Chen, F., Zhang, Y. L., & Song, J. Y. (1999). Production of lithospermic acid B and rosmarinic acid in hairy root cultures of Salvia miltiorrhiza. Journal of Industrial Microbiology & Biotechnology, 22, 133–138.
Article CAS Google Scholar
Chen, S. L., Yu, H., Luo, H. M., Wu, Q., Li, C. F., & Steinmetz, A. (2016). Conservation and sustainable use of medicinal plants: problems, progress, and prospects. Chinese Medicine, 11, 37. https://doi.org/10.1186/s13020-016-0108-7.
Article PubMed PubMed Central Google Scholar
Cheruvathur, M. K., Jose, B., & Thomas, T. D. (2015). Rhinacanthin production from hairy root cultures of Rhinacanthus nasutus (L.) Kurz. In Vitro Cellular & Developmental Biology. Plant, 51, 420–427. https://doi.org/10.1007/s11627-015-9694-9.
Article CAS Google Scholar
Christen, P., Aoki, T., & Shimomura, K. (1992). Characteristics of growth and tropane alkaloid production in Hyoscyamus albus hairy roots transformed with Agrobacterium rhizogenes A4. Plant Cell Reports, 11, 597–600.
Article PubMed CAS Google Scholar
Condori, J., Sivakumar, G., Hubstenberger, J., Dolan, M. C., Sobolev, V. S., & Medina-Bolivar, 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.
Article PubMed CAS Google Scholar
Constabel, C. P., & Towers, G. H. N. (1988). Thiarubrine accumulation in hairy root cultures of Chaenactis douglasii. Plant Physiology, 133, 67–72.
Article CAS Google Scholar
Deno, H., Yamagata, H., Emoto, T., Yoshioka, T., Yamada, Y., & Fujita, Y. (1987). Scopolamine production by root cultures of Duboisia myoporoides: II. Establishment of a hairy root culture by infection with Agrobacterium rhizogenes. Journal of Plant Physiology, 131, 315–313.
Google Scholar
Drake, P. M. W., Madeira, L. M., Szeto, T. H., & Ma, J. K. C. (2013). Transformation of Althaea officinalis L. by Agrobacterium rhizogenes for the production of transgenic roots expressing the anti-HIV microbicide cyanovirin-N. Transgenic Research, 22, 1225–1229. https://doi.org/10.1007/s11248-013-9730-7.
Article PubMed CAS Google Scholar
Du, M., Wu, X. J., Ding, J., Hu, Z. B., White, K. N., & Branford-White, C. J. (2003). Astragaloside IV and polysaccharide production by hairy roots of Astragalus membranaceus in bioreactors. Biotechnology Letters, 25, 1853–1856.
Article PubMed CAS Google Scholar
Dupraz, J. M., Christen, P., & Kapetanidis, I. (1994). Tropane alkaloids in transformed roots of Datura quercifolia. Planta Medica, 60(2), 158–162.
Google Scholar
Eapen, S., Suseelan, K. N., Tivarekar, S., Kotwal, S. A., & Mitra, R. (2003). Potential for rhizofiltration of uranium using hairy root cultures of Brassica juncea and Chenopodium amaranticolor. Environmental Research, 91, 127–133.
Article PubMed CAS Google Scholar
EMBO course (1982) The use of Ti plasmid as cloning vector for genetic engineering in plants, August 4–23; pp 109
Google Scholar
Fang, J., Reichelt, M., Hidalgo, W., Agnolet, S., & Schneider, B. (2012). Tissue-specific distribution of secondary metabolites in rapeseed (Brassica napus L.). PLoS One, 7(10), e48006.
Article PubMed PubMed Central CAS Google Scholar
Frankfater, C. R., Dowd, M. K., & Triplett, B. A. (2009). Effect of elicitors on the production of gossypol and methylated gossypol in cotton hairy roots. Plant Cell, Tissue and Organ Culture, 98, 341–349.
Article CAS Google Scholar
Fu, C. X., Xu, Y., Zhao, D. X., & Shan, M. F. (2006). A comparison between hairy root cultures and wild plants of Saussurea involucrata in phenylpropanoids production. Plant Cell Reports, 24, 750–754.
Article PubMed CAS Google Scholar
Fu, X., Yin, Z. P., Chen, J. G., Shangguan, X. C., Wang, X., Zhang, Q. F., & Peng, D. Y. (2015). Production of chlorogenic acid and its derivatives in hairy root cultures of Stevia rebaudiana. Journal of Agricultural and Food Chemistry, 63, 262–268. https://doi.org/10.1021/jf504176r.
Article PubMed CAS Google Scholar
Gai, Q. Y., Jiao, J., Luo, M., Wei, Z. F., Zu, Y. G., Ma, W., & Fu, Y. J. (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. https://doi.org/10.1371/journal.pone.0119022.
Gamborg, O. L., Miller, R. A., & Ojima, O. (1968). Nutrient requirements of suspension cultures of soybean root cell. Experimental Cell Research, 50, 151–158.
Article PubMed 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(6), 706–710.
Article PubMed CAS Google Scholar
Gaume, A., Komarnytsky, S., Borisjuk, N., & Raskin, I. (2003). Rhizosecretion of recombinant proteins from plant hairy roots. Plant Cell Reports, 21, 1188–1193.
Article PubMed CAS Google Scholar
Ge, X. C., & Wu, J. Y. (2005). Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag⁺ and yeast elicitor. Plant Science, 168, 487–491.
Google Scholar
Geerlings, A., Hallard, D., Caballero, A. M., Cardoso, I. L., Heijden, R., & Verpoorte, R. (1999). Alkaloid production by a Cinchona officinalis ‘Ledgeriana’ hairy root culture containing constitutive expression constructs of tryptophan decarboxylase and strictosidine synthase cDNAs from Catharanthus roseus. Plant Cell Reports, 19, 191–196.
Article CAS PubMed Google Scholar
González, P. S., Capozucca, C. E., Tigier, H. A., Milrad, S. R., & Agostini, E. (2006). Phytoremediation of phenol from wastewater, by peroxidases of tomato hairy root cultures. Enzyme and Microbial Technology, 39, 647–653.
Article CAS Google Scholar
González, P. S., Maglione, G. A., Giordana, M., Paisio, C. E., Talano, M. A., & Agostini, E. (2012). Evaluation of phenol detoxification by Brassica napus hairy roots, using Allium cepa test. Environmental Science and Pollution Research, 19, 482. https://doi.org/10.1007/s11356-011-0581-6.
Article PubMed CAS Google Scholar
Grzegorczyk, I., & Wysokinska, H. (2010). Antioxidant compounds in Salvia officinalis L. shoot and hairy root cultures in the nutrient sprinkle bioreactor. Acta Societatis Botanicorum Poloniae, 79(1–7), 7–10.
CAS Google Scholar
Gujarathi, N. P., Haney, B. J., Park, H. J., Wickramasinghe, S. R., & Linden, J. C. (2005). Hairy roots of Helianthus annuus: a model system to study phytoremediation of tetracycline and oxytetracycline. Biotechnology Progress, 21, 775–780.
Article PubMed CAS Google Scholar
Gupta, S. K., Liu, R. B., Liaw, S. Y., Chan, H. S., & Tsay, H. S. (2011). Enhanced tanshinone production in hairy roots of ‘Salvia miltiorrhiza Bunge’ under the influence of plant growth regulators in liquid culture. Botanical Studies, 52, 435–443.
CAS Google Scholar
Gurusamy, P. D., Schaefer, H., Ramamoorthy, S., & Wink, M. (2017). Biologically active recombinant human erythropoietin expressed in hairy root cultures and regenerated plantlets of Nicotiana tabacum L. PLoS One. https://doi.org/10.1371/journal.pone.018236.
Ha, N. T., Sakakibara, M., & Sano, S. (2011). Accumulation of indium and other heavy metals by Eleocharis acicularis: An option for phytoremediation and phytomining. Bioresource Technology, 102(3), 2228–2234.
Google Scholar
Ha, L. T., Pawlicki-Jullian, N., Pillon-Lequart, M., Boitel-Conti, M., Duong, H. X., & Gontier, E. (2016). Hairy root cultures of Panax vietnamensis, a promising approach for the production of ocotillol-type ginsenosides. Plant Cell, Tissue and Organ Culture, 126, 93–103.
Article CAS Google Scholar
Habibi, P., Piri, K., Deljo, A., Moghadam, Y. A., & Ghiasvand, T. (2015). Increasing scopolamine content in hairy roots of Atropa belladonna using bioreactor. Brazilian Archives of Biology and Technology, 58(2), 166–174.
Google Scholar
Häggman, H. M., & Aronen, T. S. (2000). Agrobacterium rhizogenes for rooting recalcitrant woody plants. In S. M. Jain & S. C. Minocha (Eds.), Molecular biology of woody plants. Forestry sciences (Vol. 66). Dordrecht: Springer.
Google Scholar
Häkkinen, S. T., Raven, N., Henquet, M., Laukkanen, M. L., Anderlei, T., Pitkänen, J. P., Twyman, R. M., Bosch, D., Oksman-Caldentey, K. M., Schillberg, S., & Ritala, A. (2014). Molecular farming in tobacco hairy roots by triggering the secretion of a pharmaceutical antibody. Biotechnology and Bioengineering, 111(2), 336–346.
Article PubMed CAS Google Scholar
Hamill, J. D., Parr, A. J., Robins, R. J., & Rhodes, M. J. C. (1986). Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed with Agrobacterium rhizogenes. Plant Cell Reports, 5, 111–114.
Article PubMed CAS Google Scholar
Hamill, J. D., Robins, R. J., & Rhodes, M. J. C. (1989). Alkaloid production by transformed root cultures of Cinchona ledgeriana. Planta Medica, 55, 354–357.
Article PubMed CAS Google Scholar
Heller, R. (1953). Studies on mineral nutrition of in vitro plant tissue cultures. Annals Scientific and Natural Botany Biology of Vegetables. 11^th Ser. 14, 1–223.
Google Scholar
Hilton, M. G., & Rhodes, M. J. C. (1990). Growth and hyoscyamine production of 'hairy root' cultures of Datura stramonium in a modified stirred tank reactor. Applied Microbiology and Biotechnology, 33, 132–138.
Article PubMed CAS Google Scholar
Hitaka, Y., Kino-oka, M., Taya, M., & Tone, S. (1997). Effect of liquid flow on culture of red beet hairy roots in single column reactor. J Chem Eng Jpn, 30(6), 1070–1075.
Google Scholar
Huang, S. H., Vishwakarma, R. K., Lee, T. T., Chan, H. S., & Tsay, H. S. (2014). Establishment of hairy root lines and analysis of iridoids and secoiridoids in the medicinal plant Gentiana scabra. Botanical Studies, 55, 17.
Article PubMed PubMed Central Google Scholar
Huber, C., Bartha, B., Harpaintner, R., & Schröder, P. (2009). Metabolism of acetaminophen (paracetamol) in plants-two independent pathways result in the formation of a glutathione and a glucose conjugate. Environemental Science and Pollution Research, 16, 206–213.
Article CAS Google Scholar
Huet, Y., Ekouna, J. P. E., Caron, A., Mezreb, K., Boitel-Conti, M., & Guerineau, F. (2014). Production and secretion of a heterologous protein by turnip hairy roots with superiority over tobacco hairy roots. Biotechnology Letters, 36, 181–190.
Article PubMed CAS Google Scholar
Hwang, H. H., Yu, M., & Lai, E. M. (2017). Agrobacterium-mediated plant transformation: Biology and applications. The Arabidopsis Book, 15, e0186. https://doi.org/10.1199/tab.0186.
Ishimaru, K., & Shimomura, K. (1991). Tannin production in hairy root culture of Geranium thunbergii. Phytochemistry, 30(3), 825–828.
Article CAS Google Scholar
Ishimaru, K., Sudo, H., Satake, M., & Shimomura, K. (1990). Phenyl glucosides from a hairy root culture of Swertia japonica. Phytochemistry, 29(12), 3823–3825.
Article CAS Google Scholar
Jaremicz, Z., Luczkiewicz, M., Kokotkiewicz, A., Krolicka, A., & Sowinski, P. (2014). Production of tropane alkaloids in Hyoscyamus niger (black henbane) hairy roots grown in bubble-column and spray bioreactors. Biotechnology Letters, 36, 843–853.
Article PubMed CAS Google Scholar
Jaziri, M., Legros, M., Homes, J., & Vanhaelen, M. (1988). Tropine alkaloids production by hairy root cultures of Datura stramonium and Hyoscyamus niger. Phytochemistry, 27(2), 419–420.
Article CAS Google Scholar
Jaziri, M., Homes, J., & Shimomura, K. (1994). An unusual root tip formation in hairy root culture of Hyoscyamus muticus. Plant Cell Reports, 13, 349–352.
Article PubMed CAS Google Scholar
Jeong, G. T., & Park, D. H. (2006). Enhanced secondary metabolite biosynthesis by elicitation in transformed plant root system: Effect of abiotic elicitors. Applied Biochemistry and Biotechnology, 129(132), 436–446.
Google Scholar
Jeong, G. T., Park, D. H., Hwang, B., Park, K., Kim, S. W., & Woo, J. C. (2002). Studies on mass production of transformed Panax ginseng hairy roots in bioreactor. In M. Finkelstein, J. D. McMillan, & B. H. Davison (Eds.), Biotechnology for fuels and chemicals. Appl Biochem Biotechnol (pp. 1115–1127). Totowa: Humana Press.
Chapter Google Scholar
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(12), 3754–3762.
Article CAS Google Scholar
Jung, G., & Tepfer, D. (1987). Use of genetic-transformation by the Ri T-DNA of Agrobacterium rhizogenes to stimulate biomass and tropane alkaloid production in Atropa belladonna and Calystegia sepium roots grown-in vitro. Plant Science, 50(2), 145–151.
Google Scholar
Jung, K. H., Kwak, S. S., Choi, C. Y., & Liu, J. R. (1995). An interchangeable system of hairy root and cell suspension cultures of Catharanthus roseus for indole alkaloid production. Plant Cell Reports, 15, 51–54.
Article PubMed CAS Google Scholar
Kang, S., Ajjappala, H., Seo, H. H., Sim, J. S., Yoon, S. H., Koo, B. S., Kim, Y. H., Lee, S., & Hahn, B. S. (2011). Expression of the human tissue-plasminogen activator in hairy roots of oriental melon (Cucumis melo). Plant Molecular Biology Reporter, 29, 919–926.
Article CAS Google Scholar
Kayser, O., & Quax, W. G. (2007). Medicinal plant biotechnology (Vol. 1, p. 604). Weinheim: WILEY-VCH Verlag GmbH & Co..
Google Scholar
Khalili, G. M., Hasanloo, T., & Tabar, S. K. K. (2010). Ag⁺ enhanced silymarin production in hairy root cultures of Silybum marianum L. Plant. OMICS, 3, 109–114.
Google Scholar
Khanna, P., & Staba, J. (1968). Antimicrobials from plant tissue cultures. Lloydia, 31, 180–189.
Google Scholar
Kim, Y. H., & Yoo, Y. J. (1996). Peroxidase production from carrot hairy root cell culture. Enzyme and Microbial Technology, 18, 531–535.
Article CAS Google Scholar
Kim, Y. J., Weathers, P. J., & Wyslouzil, B. E. (2002). Growth of Artemisia annua hairy roots in liquid- and gas-phase reactors. Biotechnology and Bioengineering, 80(4), 454–464.
Article PubMed CAS Google Scholar
Kim, O. T., Manickavasagm, M., Kim, Y. J., Jin, M. R., Kim, K. S., Seong, N. S., & Hwang, B. (2005). Genetic transformation of Ajuga multiflora Bunge with Agrobacterium rhizogenes and 20-hydroxyecdysone production in hairy roots. Journal of Plant Biology, 48, 258–262. https://doi.org/10.1007/BF03030416.
Article CAS Google Scholar
Kim, O. T., Bang, K. H., Shin, Y. S., Lee, M. J., Jung, S. J., Hyun, D. Y., Kim, Y. C., Seong, N. S., Cha, S. W., & Hwang, B. (2007). Enhanced production of asiaticoside from hairy root cultures of Centella asiatica (L.) Urban elicited by methyl jasmonate. Plant Cell Reports, 26, 1941–1949.
Google Scholar
Kim, O. T., Bang, K. H., Kim, Y. C., Hyun, D. Y., Kim, M. Y., & Cha, S. W. (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, 9, 25–33.
Article CAS Google Scholar
Kim, S. R., Sim, J. S., Ajjappala, H., Kim, Y. H., & Hahn, B. S. (2012). Expression and large-scale production of the biochemically active human tissue-plasminogen activator in hairy roots of Oriental melon (Cucumis melo). Journal of Bioscience and Bioengineering, 113(1), 106–111.
Article PubMed CAS Google Scholar
Kim, O. T., Yoo, N. H., Kim, G. S., Kim, Y. C., Bang, K. H., Hyun, D. Y., Kim, S. H., & Kim, M. Y. (2013). Stimulation of Rg3 ginsenoside biosynthesis in Ginseng hairy roots elicited by methyl jasmonate. Plant Cell, Tissue and Organ Culture, 112, 87–93.
Article CAS Google Scholar
Kino-oka, M., Hongo, Y., Taya, M., & Tone, S. (1992). Culture of red beet hairy root in bioreactor and recovery of pigment released from the cells by repeated treatment of oxygen starvation. J Chem Eng Jpn, 25(5), 490–495.
Google Scholar
Kintzios, S., Makri, O., Pistola, E., Matakiadis, T., Shi, H. P., & Economou, A. (2004). Scale-up production of puerarin from hairy roots of Pueraria phaseoloides in an airlift bioreactor. Biotechnology Letters, 26, 1057–1059.
Article PubMed CAS Google Scholar
Kisiel, W., Stojakowska, A., Malarz, J., & Kohlmunzer, S. (1995). Sesquiterpene lactones in Agrobacterium rhizogenes-transformed hairy root culture of Lactuca virosa. Phytochemistry, 40(4), 1139–1140.
Article 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.
Google Scholar
Kochan, E., Królicka, A., & Chmiel, A. (2012). Growth and ginsenoside production in Panax quinquefolium hairy roots cultivated in flasks and nutrient sprinkle bioreactor. Acta Physiologiae Plantarum, 34, 1513–1518.
Article CAS Google Scholar
Kochan, E., Szymańska, G., & Szymczyk, P. (2014). Effect of sugar concentration on ginsenoside biosynthesis in hairy root cultures of Panax quinquefolium cultivated in shake flasks and nutrient sprinkle bioreactor. Acta Physiologiae Plantarum, 36, 613–619.
Article CAS Google Scholar
Kochan, E., Szymczyk, P., Kuźma, Ł., & Szymańska, G. (2016). Nitrogen and phosphorus as the factors affecting ginsenoside production in hairy root cultures of Panax quinquefolium cultivated in shake flasks and nutrient sprinkle bioreactor. Acta Physiologiae Plantarum, 38, 149.
Google Scholar
Kochan, E., Szymczyk, P., Kuźma, Ł., Lipert, A., & Szymańska, G. (2017). Yeast extract stimulates ginsenoside production in hairy root cultures of American ginseng cultivated in shake flasks and nutrient sprinkle bioreactors. Molecules, 22(6), 880. https://doi.org/10.3390/molecules22060880.
Komarnytsky, S., Gaume, A., Garvey, A., Borisjuk, N., & Raskin, I. (2004). A quick and efficient system for antibiotic-free expression of heterologous genes in tobacco roots. Plant Cell Reports, 22, 765–773.
Article PubMed CAS Google Scholar
Kondo, O., Honda, H., Taya, M., & Kobayashi, T. (1989). Comparison of growth properties of carrot hairy root in various bioreactors. Applied Microbiology and Biotechnology, 32, 291–294.
Article CAS Google Scholar
Körner C (2016) Plant adaptation to cold climates. F1000Research 2016, 5(F1000 Faculty Rev):2769
Google Scholar
Królicka, A., Staniszewska, I. I., Bielawski, K., Maliński, E., Szafranek, J., & Łojkowska, E. (2001). Establishment of hairy root cultures of Ammi majus. Plant Science: An International Journal of Experimental Plant Biology, 160(2), 259–264.
Google Scholar
Kucerova, P., Mackova, M., Chroma, L., Burkhard, J., Triska, J., Demnerova, K., & Macek, T. (2000). Metabolism of polychlorinated biphenyls by Solanum nigrum hairy root clone SNC-9O and analysis of transformation products. Plant and Soil, 225, 109–115.
Article CAS Google Scholar
Kumar, G. B. S., Ganapathi, T. R., Srinivas, L., Revathi, C. J., & Bapat, V. A. (2006). Expression of hepatitis B surface antigen in potato hairy roots. Plant Science, 170(5), 918–925.
Article CAS Google Scholar
Kumar, V., Rajauria, G., Sahai, V., & Bisaria, V. S. (2012). Culture filtrate of root endophytic fungus Piriformospora indica promotes the growth and lignan production of Linum album hairy root cultures. Process Biochemistry, 47, 901–907.
Article CAS Google Scholar
Kuzma, Ł., Skrzypek, Z., & Wysokinska, H. (2006). Diterpenoids and triterpenoids in hairy roots of Salvia sclarea. Plant Cell, Tissue and Organ Culture, 84, 171–179.
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
Lee, L. Y., & Gelvin, S. B. (2008). T-DNA binary vectors and systems. Plant Physiology, 146(2), 325–332. https://doi.org/10.1104/pp.107.113001.
Article PubMed PubMed Central CAS Google Scholar
Lee, K. T., Suzuki, T., Yamakawa, T., Kodama, T., Igarashi, Y., & Shimomura, K. (1999). Production of tropane alkaloids by transformed root cultures of Atropa belladonna in stirred bioreactors with a stainless steel net. Plant Cell Reports, 18, 567–571.
Google Scholar
Lee, S. Y., Cho, S. I., Park, M. H., Kim, Y. K., Choi, J. E., & Park, S. U. (2007). Growth and rutin production in hairy root cultures of buckwheat (Fagopyrum esculentum M.). Preparative Biochemistry & Biotechnology, 37(3), 239–246.
Article CAS Google Scholar
Lee, K. S. Y., Xu, H., Kim, Y. K., & Park, S. U. (2008). Rosmarinic acid production in hairy root cultures of Agastache rugosa Kuntze. World Journal of Microbiology and Biotechnology, 24, 969–972.
Article Google Scholar
Linsmaier, E. M., & Skoog, F. (1965). Organic growth factor requirements of tobacco tissue culture. Plant Physiology, 21, 487–492.
Article Google Scholar
Liu, C. Z., Wang, Y. C., Ouyang, F., Ye, H. C., & Li, G. F. (1998a). Production of artemisinin by hairy root cultures of Artemisia annua L in bioreactor. Biotechnology Letters, 20(3), 265–268.
Article CAS Google Scholar
Liu, C., Wang, Y., Guo, C., Ouyang, F., Ye, H., & Li, G. (1998b). Enhanced production of artemisinin by Artemisia annua L hairy root cultures in a modified inner-loop airlift bioreactor. Bioprocess Engineering, 19, 389–392.
Google Scholar
Liu, C., Towler, M. J., Medrano, G., Cramer, C. L., & Weathers, P. J. (2009). Production of mouse interleukin-12 is greater in tobacco hairy roots grown in a mist reactor than in an airlift reactor. Biotechnology and Bioengineering, 102(4), 1074–1086.
Article PubMed CAS Google Scholar
Lloyd, G., & McCown, B. (1981). Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Combined Proceedings, International Plant Propagators’ Society, 30, 421–427.
Google Scholar
Lokhande, V. H., Kudale, S., Nikalje, G., Desai, N., & Suprasanna, P. (2015). Hairy root induction and phytoremediation of textile dye, Reactive green 19A-HE4BD, in a halophyte, Sesuvium portulacastrum (L.) L. Biotechnology Reports, 28, 56–63.
Article Google Scholar
Lonoce, C., Salem, R., Marusic, C., Jutras, P. V., Scaloni, A., Salzano, A. M., Lucretti, S., Steinkellner, H., Benvenuto, E., & Donini, M. (2016). Production of a tumour-targeting antibody with a human-compatible glycosylation profile in N. benthamiana hairy root cultures. Biotechnology Journal, 11(9), 1209–1220. https://doi.org/10.1002/biot.201500628.
Article PubMed CAS Google Scholar
Lopez, E. G., Ramarez, E. G. R., Guzman, O. G., & Calva, G. C. (2014). MALDI-TOF characterization of hGH1 produced by hairy root cultures of Brassica oleracea var. italica grown in an airlift with mesh bioreactor. Biotechnology Progress, 30(1), 161–171. https://doi.org/10.1002/btpr.1829.
Luchakivskaya, Y. S., Olevinskaya, Z. M., Kishchenko, E. M., NYA, S., & Kuchuk, N. V. (2012). Obtaining of hairy root, callus and suspension cell cultures of carrot (Daucus carota L.) able to accumulate human interferon alpha-2b. Cytology and Genetics, 46(1), 15–20.
Google Scholar
Ludwig-Müller, J., Georgiev, M., & Bley, T. (2008). Metabolite and hormonal status of hairy root cultures of Devil’s claw (Harpagophytum procumbens) in flasks and in a bubble column bioreactor. Process Biochemistry, 43, 15–23.
Article CAS Google Scholar
Macek, T., Kotbra, P., Suchova, M., Skacel, F., Demnerova, K., & Ruml, T. (1994). Accumulation of cadmium by hairy-root cultures of Solanum nigrum. Biotechnology Letters, 16, 621–624.
Article CAS Google Scholar
Macková, M., Macek, T., Kučerová, P., Burkhard, J., Pazlarová, J., & Demnerová, K. (1997). Degradation of polychlorinated biphenyls by hairy root culture of Solanum nigrum. Biotechnology Letters, 19, 787–790.
Article Google Scholar
Madhusudanan, K. P., Banerjee, S., Khanuja, S. P. S., & Chattopadhyay, S. K. (2008). Analysis of hairy root culture of Rauvolfia serpentina using direct analysis in real time mass spectrometric technique. Biomedical Chromatography, 22, 596–600.
Article PubMed CAS Google Scholar
Magnotta, M., Murata, J., Chen, J., & Luca, V. D. (2007). Expression of deacetylvindoline-4-O-acetyltransferase in Catharanthus roseus hairy roots. Phytochemistry, 68, 1922–1931.
Article PubMed CAS Google Scholar
Maheswari, U. R., Selvamurugan, C., Jayabarath, J., & Lakshmi, P. A. (2011). Hairy root culture of an important medicinal plant: Coleus forskohlii. International Journal of Agricultural Science, 3(2), 82–89.
Google Scholar
Mai, N. T. P., Boitel-Conti, M., & Guerineau, F. (2016). Arabidopsis thaliana hairy roots for the production of heterologous proteins. Plant Cell, Tissue and Organ Culture, 127, 489–496. https://doi.org/10.1007/s11240-016-1073-7.
Article CAS Google Scholar
Malarz, J., & Kisiel, W. (1999). Effect of methyl jasmonate on the production of sesquiterpene lactones in the hairy root culture of Lactuca virosa L. Acta Societatis Botanicorum Poloniae, 68(2), 119–121.
Article CAS Google Scholar
Malarz, J., Stojakowska, A., & Kisiel, W. (2002). Sesquiterpene lactones in a hairy root culture of Cichorium intybus. Zeitschrift für Naturforschung, 57, 994–997.
Article PubMed CAS Google Scholar
Mallol, A., Cusido, R. M., Palazon, J., Bonfill, M., Morales, C., & Pinol, M. T. (2001). Ginsenoside production in different phenotypes of Panax ginseng transformed roots. Phytochemistry, 57, 365–371.
Article PubMed CAS Google Scholar
Mannan, A., Shaheen, N., Arshad, W., Qureshi, R. A., Zia, M., & Mirza, B. (2008). Hairy roots induction and artemisinin analysis in Artemisia dubia and Artemisia indica. African Journal of Biotechnology, 7(18), 3288–3292.
CAS Google Scholar
Mano, Y., Ohkawa, H., & Yamada, Y. (1989). Production of tropane alkaloids by hairy root cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes. Plant Science, 59, 191–201.
Article CAS Google Scholar
Marsh, Z., Yang, T., Nopo-olazabal, W. S., Ingle, T., Joshee, N., & Medina-bolivar, M. (2014). Effect of light, methyl jasmonate and cyclodextrin on production of phenolic compounds in hairy root cultures of Scutellaria lateriflora. Phytochemistry, 107, 50–60.
Article PubMed CAS Google Scholar
Martin, K. P., Sabovljevic, A., & Madassery, J. (2011). High-frequency transgenic plant regeneration and plumbagin production through methyl jasmonate elicitation from hairy roots of Plumbago indica L. Journal of Crop Science and Biotechnology, 14, 205–212.
Article Google Scholar
Martínez, C., Petruccelli, S., Giulietti, A. M., & Alvarez, M. A. (2005). Expression of the antibody 14D9 in Nicotiana tabacum hairy roots. Electronic Journal of Biotechnology, 8(2), 170–176.
Article Google Scholar
Matsuda, Y., Toyoda, H., Sawabe, A., Maeda, K., Shimizu, N., Fujita, N., Fujita, T., Nonomura, T., & Ouchi, S. (2000). A hairy root culture of melon produces aroma compounds. Journal of Agricultural and Food Chemistry, 48, 1417–1420.
Article PubMed CAS Google Scholar
Matsumoto, T., & Tanaka, N. (1991). Production of phytoecdysteroids by hairy root cultures of Ajuga reptans var. atropurpurea. Agricultural and Biological Chemistry, 55(4), 1019–1025.
Google Scholar
Medina-Bolívar, F., & Cramer, C. (2004). Production of recombinant proteins by hairy roots cultured in plastic sleeve bioreactors. In P. Balbás & A. Lorence (Eds.), Recombinant gene expression: Reviews and protocols. Methods in Molecular Biology (pp. 351–363). Totowa: Humana Press Inc.
Chapter Google Scholar
Medina-Bolivar, F., Condori, J., Rimando, A. M., Hubstenberger, J., Shelton, K., O'Keefe, S. F., Bennett, S., & Dolan, M. C. (2007). Production and secretion of resveratrol in hairy root cultures of peanut. Phytochemistry, 68, 1992–2003.
Article PubMed CAS Google Scholar
Mehrotra, S., Kukreja, A. K., Khanuja, S. P. S., & Mishra, B. N. (2008). Genetic transformation studies and scale up of hairy root culture of Glycyrrhiza glabra in bioreactor. Electronic Journal of Biotechnology, 11(2), 1–7.
Article CAS Google Scholar
Metzger, L., Fouchault, I., Glad, C., Prost, R., & Tepfer, D. (1992). Estimation of cadmium availability using transformed roots. Plant and Soil, 143, 249–257.
Article CAS Google Scholar
Mishra, B. N., & Ranjan, R. (2008). Growth of hairy-root cultures in various bioreactors for the production of secondary metabolites. Biotechnology and Applied Biochemistry, 49(1), 1–10.
Article PubMed CAS Google Scholar
Mishra, J., Bhandari, H., Singh, M., Rawat, S., Agnihotri, R. K., Mishra, S., & Purohit, S. (2011). Hairy root culture of Picrorhiza kurroa Royle ex Benth.: a promising approach for the production of picrotin and picrotoxinin. Acta Physiologiae Plantarum, 33, 1841–1846.
Article CAS Google Scholar
Mišić, D., Šiler, B., Skorić, M., Djurickovic, M. S., Živković, J. N., Jovanović, V., & Giba, Z. (2013). Secoiridoid glycosides production by Centaurium maritimum (L.) Fritch hairy root cultures in temporary immersion bioreactor. Process Biochemistry, 48, 1587–1591.
Article CAS Google Scholar
Moghadam, A., Niazi, A., Afsharifar, A., & Taghavi, S. M. (2016). Expression of a recombinant anti-HIV and anti-tumor protein, MAP 30, in Nicotiana tobacum hairy roots: a pH-stable and thermophilic antimicrobial protein. PLoS One. https://doi.org/10.1371/journal.pone.0159653.
Momčilović, I., Grubišić, D., Kojić, M., & Nešković, M. (1997). Agrobacterium rhizogenes-mediated transformation and plant regeneration of four Gentiana species. Plant Cell, Tissue and Organ Culture, 50, 1–6.
Article Google Scholar
Moreno-Valenzuela, O., Coello-Coello, J., Loyola-Vargas, V. M., & Vázquez-Flota, F. (1999). Nutrient consumption and alkaloid accumulation in a hairy root line of Catharanthus roseus. Biotechnology Letters, 21, 1017–1021.
Article CAS Google Scholar
Mukundan, U., Bhagwat, V., Singh, G., & Curtis, W. (2001). Integrated recovery of pigments released from red beet hairy roots exposed to acidic medium. Journal of Plant Biochemistry and Biotechnology, 10, 67–69.
Article CAS Google Scholar
Muranaka, T., Ohkawa, H., & Yamada, Y. (1993). Continuous production of scopolamine by a culture of Duboisia leichhardtii hairy root clone in a bioreactor system. Applied Microbiology and Biotechnology, 40, 219–223.
Article CAS Google Scholar
Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.
Article 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
Nagakari, M., Kushiro, T., Matsumoto, T., Tanaka, N., Kakinuma, K., & Fujimoto, Y. (1994). Incorporation of acetate and cholesterol into 20-hydroxyecdysone by hairy root clone of Ajuga reptans var. atropurpurea. Phytochemistry, 36(4), 907–914.
Article CAS Google Scholar
Nanasato, Y., Namiki, S., Oshima, M., Moriuchi, R., Konagaya, K., Seike, N., Otani, T., Nagata, Y., Tsuda, M., & Tabei, Y. (2016). Biodegradation of γ-hexachlorocyclohexane by transgenic hairy root cultures of Cucurbita moschata that accumulate recombinant bacterial LinA. Plant Cell Reports, 35, 1963–1974. https://doi.org/10.1007/s00299-016-2011-1.
Article PubMed CAS Google Scholar
Neagoe, A., Tenea, G., N, C., Ion, S., & Iordache, V. (2017). Coupling Nicotiana tabaccum transgenic plants with Rhizophagus irregularis for phytoremediation of heavy metal polluted areas. Revista de Chimie -Bucharest, 68, 789–795.
CAS Google Scholar
Nedelkoska, T. V., & Doran, P. M. (2000). Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnology and Bioengineering, 67, 607–615.
Article PubMed CAS Google Scholar
Nedelkoska, T. V., & Doran, P. M. (2001). Hyperaccumulation of nickel by hairy roots of Alyssum species: Comparison with whole regenerated plants. Biotechnology Progress, 17, 752–759.
Google Scholar
Neelwarne, B., & Thimmaraju, R. (2009). Bioreactor for cultivation of red beet hairy roots and in situ recovery of primary and secondary metabolites. Engineering in Life Sciences, 9(3), 227–238.
Article CAS Google Scholar
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.
Google Scholar
Noda, T., Tanaka, N., Mano, Y., Nabeshima, S., Ohkawa, H., & Matsui, C. (1987). Regeneration of horseradish hairy roots incited by Agrobacterium rhizogenes infection. Plant Cell Reports, 6, 283–286.
Article PubMed CAS Google Scholar
Novo, L. A. B., Castro, P. M. L., Alvarenga, P., & Silva, E. F. (2017). Phytomining of rare and valuable metals. In A. A. Ansari, S. S. Gill, R. Gill, G. R. Lanza, & L. Newman (Eds.), Phytoremediation : Management of Enviornmental Contaminants (Vol. 5, pp. 469–486), Cham: Springer International Publishing.
Google Scholar
Nuutila, A. M., Toivonen, L., & Kauppinen, V. (1994). Bioreactor studies on hairy root cultures of Catharanthus roseus: comparison of three bioreactor types. Biotechnology Techniques, 8(1), 61–66.
Article CAS Google Scholar
Nuutila, A. M., Lindqvist, A. S., & Kauppinen, V. (1997). Growth of hairy root cultures of strawberry (Fragaria x ananassa Duch.) in three different types of bioreactors. Biotechnology Techniques, 11, 363–366.
Google Scholar
Oksman-Caldentey, K. M., Park, O., Joki, E., & Hiltunen, R. (1989). Increased production of tropane alkaloids by conventional and transformed root cultures of Hyoscyamus muticus. Planta Medica, 55, 682.
Article Google Scholar
Ondrej, M., & Protiva, J. (1987). In vitro culture of crown gall and hairy root tumors of Atropa belladonna: Differentiation and alkaloid production. Biologia Plantarum, 29(4), 241–246.
Google Scholar
Pala, Z., Shukla, V., Alok, A., Kudale, S., & Desai, N. (2016). Enhanced production of an anti-malarial compound artesunate by hairy root cultures and phytochemical analysis of Artemisia pallens Wall. 3 Biotech, 6, 182. https://doi.org/10.1007/s13205-016-0496-5.
Article PubMed PubMed Central Google Scholar
Palazón, J., Cusidó, R. M., Bonfill, M., Mallol, A., Moyano, E., Morales, C., & Piñol, M. T. (2003a). Elicitation of different Panax ginseng transformed root phenotypes for an improved ginsenoside production. Plant Physiology and Biochemistry, 41, 1019–1025.
Article CAS Google Scholar
Palazón, J., Mallol, A., Eibl, R., Lattenbauer, C., Cusidó, R. M., & Piñol, M. T. (2003b). Growth and ginsenoside production in hairy root cultures of Panax ginseng using a novel bioreactor. Planta Medica, 69, 344–349.
Article PubMed Google Scholar
Park, S. U., Kim, Y. K., & Lee, S. Y. (2009). Establishment of hairy root culture of Rubia akane Nakai for alizarin and purpurin production. Scientific Research and Essays, 4(2), 094–097.
Google Scholar
Parr, A. J., & Hamill, J. D. (1987). Relationship between Agrobacterium rhizogenes transformed hairy roots and intact, uninfected Nicotiana plants. Phytochemistry, 26(12), 3241–3245.
Article CAS Google Scholar
Patel, D. K. (2015). Diversity of underground medicinal and aromatic plants and their regeneration for further ex situ conservation in herbal garden. Journal of Biodiversity and Endangered Species, 3(1). https://doi.org/10.4172/2332-2543.1000152.
Patial, V., Devi, K., Sharma, M., Bhattacharya, A., & Ahuja, P. S. (2012). Propagation of Picrorhiza kurroa Royle ex Benth: an important medicinal plant of western Himalaya. Journal of Medicinal Plants Research, 6, 4848–4860.
Article CAS Google Scholar
Patra, N., & Srivastava, A. K. (2014). Enhanced production of artemisinin by hairy root cultivation of Artemisia annua in a modified stirred tank reactor. Applied Biochemistry and Biotechnology, 174, 2209–2222. https://doi.org/10.1007/s12010-014-1176-8.
Article PubMed CAS Google Scholar
Patra, N., & Srivastava, A. K. (2015). Use of model-based nutrient feeding for improved production of artemisinin by hairy roots of Artemisia annua in a modified stirred tank bioreactor. Applied Biochemistry and Biotechnology, 177, 373–388. https://doi.org/10.1007/s12010-015-1750-8.
Article PubMed CAS Google Scholar
Patra, N., Srivastava, A. K., & Sharma, S. (2013). Study of various factors for enhancement of artemisinin in Artemisia annua hairy roots. IJCEA, 4(3), 157–160.
Article CAS Google Scholar
Pavlov, A., & Bley, T. (2006). Betalains biosynthesis by Beta vulgaris L. hairy root culture in a temporary immersion cultivation system. Process Biochemistry, 41, 848–852.
Article CAS Google Scholar
Pavlov, A., Kovatcheva, P., Georgiev, V., Koleva, I., & Ilieva, M. (2002). Biosynthesis and radical scavenging activity of betalains during the cultivation of red beet (Beta vulgaris) hairy root cultures. Zeitschrift für Naturforschung. Section C, 57, 640–644.
Google Scholar
Pavlov, A., Georgiev, M., & Bley, T. (2007). Batch and fed-batch production of betalains by red beet (Beta vulgaris) hairy roots in a bubble column reactor. Zeitschrift für Naturforschung, 62c, 439–446.
Google Scholar
Pavlova, O. A., Matveyeva, T. V., & Lutova, L. A. (2014). Rol-Genes of Agrobacterium rhizogenes. Russian Journal of Genetics: Applied Research, 4(2), 137–145.
Article Google Scholar
Payne, J., Hamill, J. D., Robins, R., & Rhodes, M. J. C. (1987). Production of hyoscyamine by 'hairy root' cultures of Datura stramonium. Planta Medica, 53, 474–478.
Article PubMed CAS Google Scholar
Perassolo, M., Cardillo, A. B., Mugasc, M. L., Montoyac, S. C. N., Giuliettia, A. M., & Taloua, J. R. (2017). Enhancement of anthraquinone production and release by combination of culture medium selection and methyl jasmonate elicitation in hairy root cultures of Rubia tinctorum. Industrial Crops and Products, 105, 124–132.
Article CAS Google Scholar
Peraza-Luna, F., Rodríguez-Mendiola, M., Arias-Castro, C., Bessiere, J. M., & Calva-Calva, G. (2001). Sotolone production by hairy root cultures of Trigonella foenum-graecum in airlift with mesh bioreactors. Journal of Agricultural and Food Chemistry, 49, 6012–6019.
Google Scholar
Pham, N. B., Schäfer, H., & Wink, M. (2012). Production and secretion of recombinant thaumatin in tobacco hairy root cultures. Biotechnology Journal, 7, 537–545. https://doi.org/10.1002/biot.201100430.
Article PubMed CAS Google Scholar
Phongprueksapattana, S., Putalun, W., Keawpradub, N., & Wungsintaweekul, J. (2008). Mitragyna speciosa: hairy root culture for triterpenoid production and high yield of mitragynine by regenerated plants. Zeitschrift für Naturforschung, 63c, 691–698.
Article Google Scholar
Pillai, D. B., Jose, B., Satheeshkumar, K., & Krishnan, P. N. (2015). Optimization of inoculum density in hairy root culture of Plumbago rosea L. for enhanced growth and plumbagin production towards scaling-up in bioreactor. Indian Journal of Biotechnology, 14(2), 264–269.
CAS Google Scholar
Pirian, K., Piri, K., & Ghiyasvand, T. (2012). Hairy roots induction from Portulaca oleracea using Agrobacterium rhizogenes to Noradrenaline’s production. International Research Journal of Applied and Basic Sciences, 3(3), 642–649.
CAS Google Scholar
Pitta-Alvarez, S. I., & Giulietti, A. M. (1995). Advantages and limitations in the use of hairy root cultures for the production of tropane alkaloids: use of anti-auxins in the maintenance of normal root morphology. In Vitro Cellular & Developmental Biology. Plant, 31, 215–220.
Article Google Scholar
Pitta-Alvarez, S. I., & Giulietti, A. M. (1998). Novel biotechnological approaches to obtain scopolamine and hyoscyamine: the influence of biotic elicitors and stress agents on cultures of transformed roots of Brugmansia candida. Phytotherapy Research, 12, S18–S20.
Article CAS Google Scholar
Putalun, W., Taura, F., Qing, W., Matsushita, H., Tanaka, H., & Shoyama, Y. (2003). Anti-solasodine glycoside single-chain Fv antibody stimulates biosynthesis of solasodine glycoside in plants. Plant Cell Reports, 22, 344–349. https://doi.org/10.1007/s00299-003-0689-3.
Article PubMed CAS Google Scholar
Putalun, W., Luealon, W., De-Eknamkul, W., Tanaka, H., & Shoyama, Y. (2007). Improvement of artemisinin production by chitosan in hairy root cultures of Artemisia annua L. Biotechnology Letters, 29, 1143–1146.
Article PubMed CAS Google Scholar
Rahimi, S., Hasanloo, T., Najafi, F., & Khavari-Nejad, R. A. (2012). Methyl jasmonate influence on silymarin production and plant stress responses in Silybum marianum hairy root cultures in a bioreactor. Natural Product Research, 26(18), 1662–1667. https://doi.org/10.1080/14786419.2011.593518.
Article PubMed CAS Google Scholar
Rao, S. R., Tripathi, U., Suresh, B., & Ravishankar, G. A. (2001). Enhancement of secondary metabolite production in hairy root cultures of Beta vulgaris and Tagetes patula under the influence of microalgal elicitors. Food Biotechnology, 15(1), 35–46. https://doi.org/10.1081/FBT-100103893.
Rezek, J., Macek, T., Mackova, M., & Triska, J. (2007). Plant metabolites of polychlorinated biphenyls in hairy root culture of black nightshade Solanum nigrum SNC-90. Chemosphere, 69, 1221–1227.
Article PubMed 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 trees. Journal of Agricultural Research, 41, 507–540.
Google Scholar
Ritala, A., Dong, L., Imseng, N., Seppänen-Laakso, T., Vasilev, N., Krol, S., Rischer, H., Maaheimo, H., Virkki, A., Brändli, J., Schillberg, S., Eibl, R., Bouwmeester, H., & Oksman-Caldentey, K. M. (2014). Evaluation of tobacco (Nicotiana tabacum L. cv. Petit Havana SR1) hairy roots for the production of geraniol, the first committed step in terpenoid indole alkaloid pathway. Journal of Biotechnology, 176, 20–28.
Article PubMed CAS Google Scholar
Robins, R. J., Hamill, J. D., Parr, A. J., Smith, K., Walton, N. J., & Rhodes, M. J. C. (1987). Potential for use of nicotinic acid as a selective agent for isolation of high nicotine -producing lines of Nicotiana rustica hairy root cultures. Plant Cell Reports, 6(2), 122–126.
PubMed CAS Google Scholar
Rosić, N., Momčilović, I., Kovačević, N., & Grubišić, D. (2006). Genetic transformation of Rhamnus fallax and hairy roots as a source of anthraquinones. Biologia Plantarum, 50(4), 514–518.
Article Google Scholar
Ru, M., An, Y., Wang, K., Peng, L., li, B., Bai, Z., Wang, B., & Liang, Z. (2016). Prunella vulgaris L. hairy roots: Culture, growth, and elicitation by ethephon and salicylic acid. Engineering in Life Sciences, 16, 494–502.
Article CAS Google Scholar
Rudrappa, T., Neelwarne, B., Kumar, V., Lakshmanan, V., Venkataramareddy, S. R., & Aswathanarayana, R. G. (2005). Peroxidase production from hairy root cultures of red beet (Beta vulgaris). Electronic Journal of Biotechnology, 8(2), 185–196.
Article CAS Google Scholar
Saito, K., Sudo, H., Yamazaki, M., Koseki-Nakamura, M., Kitajima, M., Takayama, H., & Aimi, N. (2001). Feasible production of camptothecin by hairy root culture of Ophiorrhiza pumila. Plant Cell Reports, 20, 267–271. https://doi.org/10.1007/s002990100320.
Article CAS Google Scholar
Sajjalaguddam, R. R., & Paladugu, A. (2016). Influence of Agrobacterium rhizogenes strains and elicitation on hairy root induction and glycyrrhizin production from Abrus precatorius. Journal of Pharmaceutical Sciences and Research, 8(12), 1353–1357.
Google Scholar
Sakamoto, S., Putalun, W., Pongkitwitoon, B., Juengwatanatrakul, T., Shoyama, Y., Tanaka, H., & Morimoto, S. (2012). Modulation of plumbagin production in Plumbago zeylanica using a single-chain variable fragment antibody against plumbagin. Plant Cell Reports, 31, 103–110. https://doi.org/10.1007/s00299-011-1143-6.
Article PubMed CAS Google Scholar
Sampaio, B. L., Edrada-Ebel, R. A., & Da Costa, F. B. (2016). Effect of the environment on the secondary metabolic profile of Tithonia diversifolia: a model for environmental metabolomics of plants. Scientific Reports, 6, 29265.
Article PubMed PubMed Central Google Scholar
Sasaki, K., Udagawa, A., Ishimaru, H., Hayashi, T., Alfermann, A. W., Nakanishi, F., & Shimomura, K. (1998). High forskolin production in hairy roots of Coleus forskohlii. Plant Cell Reports, 17, 457–459.
Article CAS PubMed 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, 281–289.
Article PubMed CAS Google Scholar
Sauerwein, M., Yamazaki, T., & Shimomura, K. (1991). Hernandulcin in hairy root cultures of Lippia dulcis. Plant Cell Reports, 9, 579–581.
Google Scholar
Savitha, B. C., Thimmaraju, R., Bhagyalakshmi, N., & Ravishankar, G. A. (2006). Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor. Process Biochemistry, 41(1), 50–60.
Article CAS Google Scholar
Schenk, R. V., & Hildebrandt, A. C. (1972). Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Canadian Journal of Botany, 50, 199–204.
Article CAS Google Scholar
Sharp, J. M., & Doran, P. M. (1990). Characteristics of growth and tropane alkaloid synthesis in Atropa belladonna roots transformed by Agrobacterium rhizogenes. Journal of Biotechnology, 16, 171–186.
Article CAS Google Scholar
Sheoran, V., Sheoran, A. S., & Poonia, P. (2013). Phytomining of gold: a review. Journal of Geochemical Exploration, 128, 42–50.
Article CAS Google Scholar
Shi, H. P., & Lindemann, P. (2006). Expression of recombinant Digitalis lanata EHRH. Cardenolide 16′-O-glucohydrolase in Cucumis sativus L. hairy roots. Plant Cell Reports, 25, 1193–1198. https://doi.org/10.1007/s00299-006-0183-9.
Article PubMed CAS Google Scholar
Shi, M., Kwok, K. W., & Wu, J. Y. (2007). Enhancement of tanshinone production in Salvia miltiorrhiza Bunge (red or Chinese sage) hairy-root culture by hyperosmotic stress and yeast elicitor. Biotechnology and Applied Biochemistry, 46, 191–196.
Article PubMed CAS Google Scholar
Shimomura, K., Suda, H., Saga, K., & Kamada, H. (1991). Shikonin production and secretion by hairy root cultures of Lithospermum erythrorhizon. Plant Cell Reports, 10, 282–285.
Article PubMed CAS Google Scholar
Shimon-Kerner, N., Mills, D., & Merchuk, J. C. (2000). Sugar utilization and invertase activity in hairy-root and cell-suspension cultures of Symphytum officinale. Plant Cell, Tissue and Organ Culture, 62, 89–94.
Article CAS Google Scholar
Shin, K. S., Murthy, H. N., Ko, J. Y., & Paek, K. Y. (2002). Growth and betacyanin production by hairy roots of Beta vulgaris in airlift bioreactors. Biotechnology Letters, 24, 2067–2069.
Article CAS Google Scholar
Shinde, A. N., Malpathak, N., & Fulzele, D. P. (2009). Enhanced production of phytoestrogenic isoflavones from hairy root cultures of Psoralea corylifolia L. using elicitation and precursor feeding. Biotechnology and Bioprocess Engineering, 14, 288–294. https://doi.org/10.1007/s12257-008-0238-6.
Article CAS Google Scholar
Sim, S. J., & Chang, H. N. (1993). Increased shikonin production by hairy roots of Lithospermum erythrorhizon in two phase bubble column reactor. Biotechnology Letters, (2), 145–150.
Google Scholar
Singh, S., Melo, J. S., Eapen, S., & D’Souza, S. F. (2006). Phenol removal using Brassica juncea hairy roots: Role of inherent peroxidase and H₂O₂. Journal of Biotechnology, 123, 43–49.
Article PubMed CAS Google Scholar
Singh, A., Srivastava, S., Chouksey, A., Panwar, B. S., Verma, P. C., Roy, S., Singh, P. K., Saxena, G., & Tuli, R. (2015). Expression of rabies glycoprotein and ricin toxin b chain (RGP–RTB) fusion protein in tomato hairy roots: A step towards oral vaccination for rabies. Molecular Biotechnology, 57, 359–370. https://doi.org/10.1007/s12033-014-9829-y.
Article PubMed CAS Google Scholar
Sirikantaramas, S., Morimoto, S., Shoyama, Y., Ishikawa, Y., Wada, Y., Shoyama, Y., & Taura, F. (2004). The gene controlling marijuana psychoactivity: molecular cloning and heterologous expression of delta1-tetrahydrocannabinolic acid synthase from Cannabis sativa L. The Journal of Biological Chemistry, 279(38), 39767–39774.
Article PubMed CAS Google Scholar
Sivakumar, G., Liu, C., Towler, M. J., & Weathers, P. J. (2010). Biomass production of hairy roots of Artemisia annua and Arachis hypogaea in a scaled-up mist bioreactor. Biotechnology and Bioengineering 1, 107(5), 802–813. https://doi.org/10.1002/bit.22892.
Article CAS Google Scholar
Sivanandhan, G., Dev, K. G., Jeyaraj, M., Rajesh, M., Arjunan, A., Muthuselvam, M., Manickavasagam, M., & Ganapathi, A. (2013). Increased production of withanolide A withanone and withaferin A in hairy root cultures of Withania somnifera (L.) Dunal elicited with methyl jasmonate and salicylic acid. Plant Cell, Tissue and Organ Culture, 114, 121–129.
Article CAS Google Scholar
Siwach, P., Gill, A. R., & Sethi, K. (2013). Hairy root cultures of medicinal trees: A viable alternative for commercial production of high-value secondary metabolites. In R. K. Salar, S. Gahlawat, P. Siwach, J. Duhan (Eds.), Biotechnology: Prospects and applications (pp. 67–78), New Delhi: Springer.
Google Scholar
Skorupińska-Tudek, K., Hung, V. S., Olszowska, O., Furmanowa, M., Chojnacki, T., & Swiezewska, E. (2000). Polyprenols in hairy roots of Coluria geoides. Biochemical Society Transactions, 28(6), 790–791.
Article PubMed Google Scholar
Smigocki, A. C., Puthoff, D. P., Zuzga, S., & Ivic-Haymes, S. D. (2009). Low efficiency processing of an insecticidal Nicotiana proteinase inhibitor precursor in Beta vulgaris hairy roots. Plant Cell, Tissue and Organ Culture, 97, 167–174. https://doi.org/10.1007/s11240-009-9512-3.
Article CAS Google Scholar
Soudek, P., Petrova, S., Benesova, D., & Vanek, T. (2011). Uranium uptake and stress responses of in vitro cultivated hairy root culture of Armoracia rusticana. Agrochimica Pisa, 55(1), 15–28.
CAS Google Scholar
Souret, F. F., Kim, Y., Wyslouzil, B. E., Wobbe, K. K., & Weathers, P. J. (2003). Scale up of Artemisia annuaL. hairy root cultures produces complex patterns of terpenoid gene expression. Biotechnology and Bioengineering, 83, 653–667.
Google Scholar
Spano, L., Mariotti, D., Pezzotti, M., Damjani, F., & Arcioni, S. (1987). Hairy root transformation in alfalfa (Medicago sativa L.). Theoretical and Applied Genetics, 73(4), 523–530.
Article PubMed CAS Google Scholar
Spollansky, T. C., Pitta-Alvarez, S. I., & Giulietti, A. M. (2000). Effect of jasmonic acid and aluminum on production of tropane alkaloids in hairy root cultures of Brugmansia candida. Electronic Journal of Biotechnology, 3(1). https://doi.org/10.2225/vol3-issue1-fulltext-6.
Srivastava, S., & Srivastava, A. K. (2012). Azadirachtin production by hairy root cultivation of Azadirachta indica in a modified stirred tank reactor. Bioprocess and Biosystems Engineering. https://doi.org/10.1007/s00449-012-0745-x.
Srivastava, S., & Srivastava, A. K. (2013). Production of the biopesticide azadirachtin by hairy root cultivation of Azadirachta indica in liquid-phase bioreactors. Applied Biochemistry and Biotechnology, 171, 1351–1361. https://doi.org/10.1007/s12010-013-0432-7.
Article PubMed CAS Google Scholar
Stewart, F. C., Rolf, F. M., & Hall, F. H. (1900). A fruit disease survey of western New York in 1900. New York State Agricultural Experiment Station, 191, 291–331.
Google Scholar
Stojakowska, A., Burczyk, J., Kisel, W., Zych, M., Banaś, A., & Duda, T. (2008). Effect of various elicitors on the accumulation and secretion of spiroketal enol ether diacetylenes in feverfew hairy root culture. Acta Societatis Botanicorum Poloniae, 77, 17–21.
Article CAS Google Scholar
Straczek, A., Wannijn, J., Van Hees, M., Thijs, H., & Thiry, Y. (2009). Tolerance of hairy roots of carrots to U chronic exposure in a standardized in vitro device. Environmental and Experimental Botany, 65(1), 82–89.
Article CAS Google Scholar
Streatfield, S. J. (2007). Approaches to achieve high-level heterologous protein production in plants. Plant Biotechnology Journal, 5, 2–15.
Article PubMed CAS Google Scholar
Subroto, M. A., Priambodo, S., & Indrasti, N. S. (2007). Accumulation of zinc by hairy root cultures of Solanum nigrum. Biotechnology, 6, 344–348.
Article CAS Google Scholar
Sudo, H., Yamakawa, T., Yamazaki, M., Aimi, N., & Saito, K. (2002). Bioreactor production of camptothecin by hairy root cultures of Ophiorrhiza pumila. Biotechnology Letters, 24, 359–363.
Article CAS Google Scholar
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), 441–449.
Article PubMed CAS Google Scholar
Suresh, B., Thimmaraju, R., Bhagyalakshmi, N., & Ravishankar, G. A. (2004). Polyamine and methyl jasmonate-influenced enhancement of betalaine production in hairy root cultures of Beta vulgaris grown in a bubble column reactor and studies on efflux of pigments. Process Biochemistry, 39(12), 2091–2096.
Article CAS Google Scholar
Suresh, B., Sherkhane, P. D., Kale, S., Eapen, S., & Ravishankar, G. A. (2005). Uptake and degradation of DDT by hairy root cultures of Cichorium intybus and Brassica juncea. Chemosphere, 61, 1288–1292.
Article PubMed CAS Google Scholar
Suza, W., Harris, R. S., & Lorence, A. (2008). Hairy roots: from high-value metabolite production to phytoremediation. Electronic Journal of Integrative Biosciences, 3(1), 57–65.
Google Scholar
Tada, H., Murakam, Y., Omoto, T., Shimomura, K., & Ishimaru, K. (1996). Rosmarinic acid and related phenolics in hairy root cultures of Ocimum basilicum. Phytochemistry, 42(2), 431–434.
Article CAS Google Scholar
Talamond, P., Verdeil, J. L., & Conéjéro, G. (2015). Secondary metabolite localization by autofluorescence in living plant cells. Molecules, 20, 5024–5037. https://doi.org/10.3390/molecules20035024.
Article PubMed CAS PubMed Central Google Scholar
Taya, M., Yoyama, A., Kondo, O., Kobayashi, T., & Matsui, C. (1989). Growth characteristics of plant hairy roots and their cultures in bioreactors. Journal of Chemical Engineering of Japan, 22(1), 84–89.
Article Google Scholar
Thakore, D., Srivastava, A. K., & Sinha, A. K. (2017). Mass production of ajmalicine by bioreactor cultivation of hairy roots of Catharanthus roseus. Biochemical Engineering Journal, 119, 84–91. https://doi.org/10.1016/j.bej.2016.12.010.
Theboral, J., Sivanandhan, G., Subramanyam, K., Arun, M., Selvaraj, N., Manickavasagam, M., & Ganapathi, A. (2014). Enhanced production of isoflavones by elicitation in hairy root cultures of soybean. Plant Cell, Tissue and Organ Culture, 117(3), 477–481. https://doi.org/10.1007/s11240-014-0450-3.
Tikhomiroff, C., Allais, S., Klvana, M., Hisiger, S., & Jolicoeur, M. (2002). Continuous selective extraction of secondary metabolites from Catharanthus roseus hairy roots with silicon oil in a two-liquid-phase bioreactor. Biotechnology Progress, 18(5), 1003–1009.
Article PubMed CAS Google Scholar
Tokmakov, A. A., Kurotani, A., Takagi, T., Toyama, M., Shirouzu, M., Fukami, Y., & Yokoyama, S. (2012). Multiple post-translational modifications affect heterologous protein synthesis. The Journal of Biological Chemistry, 287(32), 27106–27116.
Article PubMed PubMed Central CAS Google Scholar
Trotin, F., Moumou, Y., & Vasseur, J. (1993). Flavanol production by Fagopyrum esculentum hairy and normal root cultures. Phytochemistry, 32, 929–931.
Article CAS Google Scholar
Uchimiya, H., & Murashige, T. (1974). Evaluation of parameters in the isolation of viable protoplasts from cultured tobacco cells. Plant Physiology, 54(6), 936–944. https://doi.org/10.1104/pp.54.6.936.
Urbańska, N., Giebułtowicz, J., Olszowska, O., & Szypuła, W. J. (2014). The growth and saponin production of Platycodon grandiflorum (Jacq.) A. DC. (Chinese bellflower) hairy roots cultures maintained in shake flasks and mist bioreactor. Acta Societatis Botanicorum Poloniae, 83(3), 229–237. https://doi.org/10.5586/asbp.2014.017.
Article Google Scholar
Verma, P. C., Rahman, L. U., Nagi, A. S., Jain, D. C., Khanuja, S. P. S., & Banerjee, S. (2007). Agrobacterium rhizogenes-mediated transformation of Picrorhiza kurroa Royle ex Benth.: establishment and selection of superior hairy root clone. Plant Biotechnology Reports, 1, 169–174.
Article Google Scholar
Verma, P., Mathur, A. K., & Shanker, K. (2012). Growth, alkaloid production, rol genes integration, bioreactor up-scaling and plant regeneration studies in hairy root lines of Catharanthus roseus. Plant Biosystems – An International Journal Dealing with all Aspects of Plant Biology, 146(sup1), 27–40. https://doi.org/10.1080/11263504.2011.649797.
Verma, P., Khan, S. A., Mathur, A. K., Shanker, K., & Lal, R. K. (2014). Regulation of vincamine biosynthesis and associated growth promoting effects through abiotic elicitation, cyclooxygenase inhibition, and precursor feeding of bioreactor grown Vinca minor hairy roots. Applied Biochemistry and Biotechnology, 173, 663–672.
Article PubMed CAS Google Scholar
Verma, P. C., Singh, H., Negi, A. S., Saxena, G., Rahman, L., & Banerjee, S. (2015). Yield enhancement strategies for the production of picroliv from hairy root culture of Picrorhiza kurroa Royle ex Benth. Plant Signaling & Behavior, 10(5), e1023976. https://doi.org/10.1080/15592324.2015.1023976.
Article CAS Google Scholar
Vinterhalter, B., Savić, J., Platiša, J., Raspor, M., Ninković, S., Mitić, N., & Vinterhalter, D. (2008). Nickel tolerance and hyperaccumulation in shoot cultures regenerated from hairy root cultures of Alyssum murale Waldst et Kit. Plant Cell, Tissue and Organ Culture, 94, 299–303.
Article CAS Google Scholar
Walton, N. J., & Belshaw, N. J. (1988). The effect of cadaverine on the formation of anabasine from lysine in hairy root cultures of Nicotiana hesperis. Plant Cell Reports, 7(2), 115–118.
Article PubMed CAS Google Scholar
Walton, N. J., Robin, R. J., & Rhodes, M. J. C. (1988). Peturbation of alkaloid production by cadaverine in hairy root culture of Nicotina rustica. Plant Science, 54, 125–131.
Article CAS Google Scholar
Wang, J. W., Zhang, Z., & Tan, R. X. (2001). Stimulation of artemisinin production in Artemisia annua hairy roots by the elicitor from the endophytic Colletotrichum sp. Biotechnology Letters, 23, 857–860.
Article CAS Google Scholar
Wang, B., Zhang, G., Zhua, L., Chena, L., & Zhang, Y. (2006a). Genetic transformation of Echinacea purpurea with Agrobacterium rhizogenes and bioactive ingredient analysis in transformed cultures. Colloid Surface B, 53, 101–104.
Article CAS Google Scholar
Wang, J. W., Zheng, L. P., & Tan, R. X. (2006b). The preparation of an elicitor from a fungal endophyte to enhance artemisinin production in hairy root cultures of Artemisia annua L. Chinese Journal of Biotechnology, 22(5), 829–834.
PubMed CAS Google Scholar
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 & Developmental Biology. Plant, 41, 4753.
Article CAS Google Scholar
Wevar-Oller, A. L., Agostini, E., Talano, M. A., Capozucca, C., Milrad. S.R., Tigier, H. A., & Medina, M. I. (2005). Overexpression of a basic peroxidase in transgenic tomato (Lycopersicon esculentum Mill. cv. Pera) hairy roots increases phytoremediation of phenol. Plant Science, 169, 1102–1111.
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
Wilczańska-Barska, A., Królicka, A., Głód, D., Majdan, M., Kawiak, A., & Krauze Baranowska, M. (2012). Enhanced accumulation of secondary metabolites in hairy root cultures of Scutellaria lateriflora following elicitation. Biotechnology Letters, (9), 1757–1763.
Google Scholar
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.), International conference on bioreactors and biotransformations (pp. 38–51). London: Elsevier.
Google Scholar
Wongsamuth, R., & Doran, P. M. (1997). Production of monoclonal antibodies by tobacco hairy roots. Biotechnology and Bioengineering, 54(5), 401–415.
Article PubMed CAS Google Scholar
Wongwicha, W., Tanaka, H., Shoyama, Y., & Putalun, W. (2011). Methyl jasmonate elicitation enhances glycyrrhizin production in Glycyrrhiza inflata hairy roots cultures. Zeitschrift für Naturforschung. Section C, 66(7–8), 423–428.
Article CAS Google Scholar
Woods, R. R., Geyer, B. C., & Mor, T. S. (2008). Hairy-root organ cultures for the production of human acetylcholinesterase. BMC Biotechnology, 8(95), 1–7.
Google Scholar
Wu, S. J., & Wu, J. Y. (2008). Extracellular ATP-induced NO production and its dependence on membrane Ca²⁺ flux in Salvia miltiorrhiza hairy roots. Journal of Experimental Botany, 59(14), 4007–4016. https://doi.org/10.1093/jxb/ern242.
Article PubMed PubMed Central CAS Google Scholar
Wu, J. Y., Ng, J., Shi, M., & Wu, S. J. (2007). Enhanced secondary metabolite (tanshinone) production of Salvia miltiorrhiza hairy roots in a novel root-bacteria coculture process. Applied Microbiology and Biotechnology, 77, 543–550.
Article PubMed CAS Google Scholar
Xie, D., Wang, L., Ye, H., & Le, G. (2000). Isolation and production of artimisinin and stigma sterol in hairy root cultures of Artemisia annua. Plant Cell, Tissue and Organ Culture, 63, 161–166.
Article CAS Google Scholar
Yamazaki, Y., Sudo, H., Yamazaki, M., Aimi, N., & Saito, K. (2003). Camptothecin biosynthetic genes in hairy roots of Ophiorrhiza pumila: cloning, characterization and differential expression in tissues and by stress compounds. Plant & Cell Physiology, 44(4), 395–403.
Google Scholar
Yan, Q., Hu, Z. D., Tan, R. X., & Wu, J. Y. (2005). Efficient production and recovery of diterpenoid tanshinones in Salvia miltiorrhiza hairy root cultures with in situ adsorption, elicitation and semi-continuous operation. Journal of Biotechnology, 119, 416–424.
Article PubMed 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, H. J., He, M., Huang, W. J., Li, D., & Yu, X. (2016). Induction of hairy roots and plant regeneration from the medicinal plant Pogostemon cablin. Pharmacognosy Journal, 8(1), 50–55.
Google Scholar
Yang, C., Chen, M., Zeng, L., Zhang, L., Liu, X., Lan, X., Tang, K., & Liao, Z. (2011). Improvement of tropane alkaloids production in hairy root cultures of Atropa belladonna by overexpressing pmt and h6h genes. Plant Omics, 4(1), 29–33.
CAS Google Scholar
Yazawa, M., Suginuma, C., Ichikawa, K., & Akihama, T. (1995). Regeneration of transgenic plants from hairy root of kiwi fruit (Actinidia deliciosa) induced by Agrobacterium rhizogenes. Breeding Science, 45, 241–244.
Google Scholar
Yonemitsu, H., Shimomura, K., Satake, M., Mochida, S., Tanaka, M., Endo, T., & Kaji, A. (1990). Lobeline production by hairy root culture of Lobelia inflata L. Plant Cell Reports, 9, 307–310.
Article PubMed CAS Google Scholar
Yoshikawa, T., & Furuya, T. (1987). Saponin production by cultures of Panax ginseng transformed with Agrobacterium rhizogenes. Plant Cell Reports, 6, 449–453.
PubMed CAS Google Scholar
Yu, K. W., Gao, W. Y., Son, S. H., & Paek, K. Y. (2000). Improvement of ginsenoside production by jasmonic acid and some other elicitors in hairy root culture of ginseng (Panax ginseng C.A. Meyer). In Vitro Cellular & Developmental Biology. Plant, 36, 424–428.
Article CAS Google Scholar
Yu, K. W., Hahn, E. J., & Paek, K. Y. (2003). Ginsenoside production by hairy root cultures of Panax ginseng C.A. Meyer in bioreactors. Acta Horticulturae, (597), 237–243.
Google Scholar
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. (2004a). Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. PNAS, 101(17), 6786–6791.
Article PubMed CAS PubMed Central Google Scholar
Zhang, C., Yan, Q., Cheuk, W., & Wu, J. (2004b). Enhancement of tanshinone production in Salvia miltirrhiza hairy root culture by Ag⁺ elicitation and nutrient feeding. Planta Medica, 70, 147–151.
Google Scholar
Zhang, L., Yang, B., Lu, B., Kai, G., Wang, Z., Xia, Y., Ding, R., Zhang, H., Sun, X., Chen, W., & Tang, K. (2007). Tropane alkaloids production in transgenic Hyoscyamus niger hairy root cultures over-expressing putrescine N-methyltransferase is methyl jasmonate-dependent. Planta, 225, 887–896.
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, B., Zou, T., Yan Hua, L. Y. H., & Wang, J. W. (2010). Stimulation of artemisinin biosynthesis in Artemisia annua hairy roots by oligogalacturonides. African Journal of Biotechnology, 9, 3437–3442.
Article CAS Google Scholar
Zhao, J. L., Zhou, L. G., & Wu, J. Y. (2010). Promotion of Salvia miltiorrhiza hairy root growth and tanshinone production by polysaccharide-protein fractions of plant growth-promoting rhizobacterium Bacillus cereus. Process Biochemistry, 45, 1517–1522.
Article CAS Google Scholar
Zhao, J. L., Zou, L., Zhang, C. Q., Li, Y. Y., Peng, L. X., Xiang, D. B., & Zhao, G. (2014). Efficient production of flavonoids in Fagopyrum tataricum hairy root cultures with yeast polysaccharide elicitation and medium renewal process. Pharmacognosy Magazine, 10, 234–240.
Article PubMed PubMed Central CAS Google Scholar
Zheng, L. P., Zhang, B., Zou, T., Chen, Z. H., & Wang, J. W. (2010). Nitric oxide interacts with reactive oxygen species to regulate oligosaccharide-induced artemisinin biosynthesis in Artemisia annua hairy roots. Journal of Medicinal Plants Research, 4, 758–765.
CAS Google Scholar
Zhou, L. G., Zhu, H. T., Hu, H., & Yang, C. R. (1999). Hairy root culture of Panax japonicus var. major and its saponin formation. In C. R. Yang, O. Tanaka (Eds.), Advances in Plant Glycosides. Chemistry and Biology,(Vol. 6, pp. 91-98), Studies in Plant Science, Elsevier Science Ltd., The Netherlands: Amsterdam
Google Scholar
Zhou, X., Wu, Y., Wang, X., Liu, B., & Xu, H. (2007a). Salidroside production by hairy roots of Rhodiola sachalinensis obtained after transformation with Agrobacterium rhizogenes. Biological & Pharmaceutical Bulletin, 30(3), 439–442.
Article CAS Google Scholar
Zhou, L., Cao, X., Zhang, R., Peng, Y., Zhao, S., & Wu, J. (2007b). Stimulation of saponin production in Panax ginseng hairy roots by two oligosaccharides from Paris polyphylla var. yunnanensis. Biotechnology Letters, 29, 631–634.
Article PubMed CAS Google Scholar
Zhou, M. L., Zhu, X. M., Shao, J. R., Wu, Y. M., & Tang, Y. X. (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.
Google Scholar
Zid, S. A., & Orihara, Y. (2005). Polyacetylenes accumulation in Ambrosia maritima hairy root and cell cultures after elicitation with methyl jasmonate. Plant Cell, Tissue and Organ Culture, 81, 65–75. https://doi.org/10.1007/s11240-004-2776-8.
Article CAS Google Scholar
Zlatić, N. M., & Stanković, M. S. (2017). Variability of secondary metabolites of the species Cichorium intybus L. from different habitats. Plants (Basel), 6(3), 38.
Google Scholar
Zubrická, D., Mišianiková, A., Henzelyová, J., Valletta, A., de Angelis, G., D’Auria, F. D., Simonetti, G., Pasqua, G., & Cellárová, E. (2015). Xanthones from roots, hairy roots and cell suspension cultures of selected Hypericum species and their antifungal activity against Candida albicans. Plant Cell Reports, 34, 1953–1962.
Article PubMed CAS Google Scholar

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Acknowledgements

The authors thank the Director, CSIR-IHBT, Palampur for providing the necessary infrastructure. ND thanks the University Grants Commission, Govt. of India for providing Senior Research Fellowship. VP thanks the Council of Scientific and Industrial Research (CSIR) for providing her fellowship. ND and VP also acknowledge the Academy of Scientific and Innovative Research (AcSIR), New Delhi, India. The CSIR-IHBT communication number for the present article is 4227.

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Authors Nisha Dhiman and Vanita Patial have contributed equally to this chapter.

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Academy of Scientific and Innovative Research, New Delhi, India
Nisha Dhiman, Vanita Patial & Amita Bhattacharya
Division of Biotechnology, CSIR-Institute of Himalayan Bioresource Technology, Palampur-176061, Himachal Pradesh, India
Nisha Dhiman, Vanita Patial & Amita Bhattacharya

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Nisha Dhiman
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Vanita Patial
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Amita Bhattacharya
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Correspondence to Amita Bhattacharya .

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Department of Biotechnology, Central University of South Bihar, Panchanpur, Gaya, Bihar, India
Nitish Kumar

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Dhiman, N., Patial, V., Bhattacharya, A. (2018). The Current Status and Future Applications of Hairy Root Cultures. In: Kumar, N. (eds) Biotechnological Approaches for Medicinal and Aromatic Plants. Springer, Singapore. https://doi.org/10.1007/978-981-13-0535-1_5

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DOI: https://doi.org/10.1007/978-981-13-0535-1_5
Published: 12 September 2018
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Online ISBN: 978-981-13-0535-1
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Hairy Root Culture for the Production of Useful Secondary Metabolites

Hairy Root Culture: Secondary Metabolite Production in a Biotechnological Perspective

Advances in Transformed Root Cultures for Root Biofactory and Phytoremediation Research

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The Current Status and Future Applications of Hairy Root Cultures

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Hairy Root Culture for the Production of Useful Secondary Metabolites

Hairy Root Culture: Secondary Metabolite Production in a Biotechnological Perspective

Advances in Transformed Root Cultures for Root Biofactory and Phytoremediation Research

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