Hairy Roots and Phytoremediation

  • Anrini Majumder
  • Smita Ray
  • Sumita JhaEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


Contamination of the environment arises either from natural geological processes or due to human activities and has created an alarming situation worldwide. Biological strategies for cleaning up contaminated biosphere have gained much importance in recent years and are preferred over other conventional physical and chemical methods because these are environmentally friendly and cost-effective. Phytoremediation is an ecologically compatible approach using plants to remediate polluted environment. Currently hairy roots have emerged as a notably competent research tool for phytoremediation among the various biological systems investigated for this purpose. Infection of certain plants caused by Agrobacterium rhizogenes is expressed in the form of hairy root disease. The disease is characterized by adventitious roots with copious root hairs developing elaborately from or next to the infection site. The plant genome receives a set of genes from a segment of the large root inducing (Ri) plasmid of A. rhizogenes. Under the effect of these genes, the inherent hormonal balance of the plant is altered resulting in the development of hairy roots. In nature, plant roots are the primary organs having contact with the environmental contaminants. Thus, hairy roots have been used in phytoremediation research as physiologically they resemble the normal roots of the mother plants. Several studies demonstrate the potentiality of hairy roots in removing a vast array of both organic and inorganic pollutants from the environment. In addition, microorganisms colonizing the rhizosphere of hairy roots have also proved to improve the efficacy of hairy roots in eliminating contaminants. The purpose of this review is to summarize the applications of hairy roots in different phytoremediation strategies and provide examples and prospects of the use of hairy roots in the removal of organic and inorganic contaminants from the environment.


Agrobacterium rhizogenes Hairy roots Inorganic pollutants Organic pollutants Phytoremediation 





Arbuscular mycorrhizal fungus








Deoxyribonucleic acid


Fourier transform infrared spectroscopy


Gas chromatography–mass spectrometry




High-performance liquid chromatography





NADH–DCIP reductase

Nicotinamide adenine dinucleotide reduced–dichlorophenolindophenol reductase






Polychlorinated biphenyl






Transferred DNA








  1. 1.
    Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780PubMedCrossRefGoogle Scholar
  2. 2.
    Freitas H, Prasad MNV, Pratas J (2004) Plant community tolerant to trace elements growing on the degraded soils of Sao Domingos mine in the south east of Portugal: environmental implications. Environ Int 30:65–72PubMedCrossRefGoogle Scholar
  3. 3.
    Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation–an overview. Crit Rev Plant Sci 24:109–122CrossRefGoogle Scholar
  4. 4.
    Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manag 105:103–120CrossRefGoogle Scholar
  5. 5.
    Zhou ML, Tang YX, Wu YM (2013) Plant hairy roots for remediation of aqueous pollutants. Plant Mol Biol Report 31:1–8CrossRefGoogle Scholar
  6. 6.
    López-Molina D, Hiner ANP, Tudela J, Garćıa-Cánovas F, Rodŕıguez-López JN (2003) Enzymatic removal of phenols from aqueous solution by artichoke (Cynara scolymus L.) extracts. Enzym Microb Technol 33:738–742CrossRefGoogle Scholar
  7. 7.
    Khaitan S, Kalainesan S, Erickson LE, Kulakow P, Martin S, Karthikeyan R, Hutchinson S, Davis L, Illangasekare TH, Nģoma C (2006) Remediation of sites contaminated by oil refinery operations. Environ Prog 25:20–31CrossRefGoogle Scholar
  8. 8.
    Doran PM (2009) Application of plant tissue cultures in phytoremediation research: incentives and limitations. Biotechnol Bioeng 103:60–76PubMedCrossRefGoogle Scholar
  9. 9.
    Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17(1):6–15PubMedCrossRefGoogle Scholar
  10. 10.
    Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333PubMedCrossRefGoogle Scholar
  11. 11.
    Majumder A, Jha S (2012) Hairy roots: a promising tool for phytoremediation. In: Satyanarayana T et al (eds) Microorganisms in environmental management: microbes and environment. Springer, Dordrecht, pp 607–629CrossRefGoogle Scholar
  12. 12.
    Sadowsky MJ (1999) Phytoremediation: past promises and future practices. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Microbial biosystems: new frontiers. Proceedings of the 8th international symposium on microbial ecology, Atlantic Canada Society for Microbial Ecology, HalifaxGoogle Scholar
  13. 13.
    Van Aken B (2009) Transgenic plants for enhanced phytoremediation of toxic explosives. Curr Opin Biotechnol 20:231–236PubMedCrossRefGoogle Scholar
  14. 14.
    Agostini E, Talano MA, González PS, Wevar Oller AL, Medina MI (2013) Application of hairy roots for phytoremediation: what makes them an interesting tool for this purpose? Appl Microbiol Biotechnol 97:1017–1030PubMedCrossRefGoogle Scholar
  15. 15.
    Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39PubMedCrossRefGoogle Scholar
  16. 16.
    Abhilash PC, Jamil S, Singh N (2009) Transgenic plants for enhanced biodegradation and phytoremediation of organic xenobiotics. Biotechnol Adv 27:474–488PubMedCrossRefGoogle Scholar
  17. 17.
    Suthersan SS (1999) Phytoremediation. In: Suthersan SS (ed) Remediation engineering: design concepts. CRC Press LLC, Boca RatonGoogle Scholar
  18. 18.
    Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362CrossRefGoogle Scholar
  19. 19.
    Baker AJM, Whiting SN (2002) In search of the Holy Grail – a further step in understanding metal hyperaccumulation? New Phytol 155:1–7CrossRefGoogle Scholar
  20. 20.
    Rascio N, Navari-Izzo F (2011) Heavy metal accumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181PubMedCrossRefGoogle Scholar
  21. 21.
    Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Plant Soil 184:105–126Google Scholar
  22. 22.
    Al-Shalabi Z, Doran PM (2013) Metal uptake and nanoparticle synthesis in hairy root cultures. Adv Biochem Eng Biotechnol 134:135–153PubMedGoogle Scholar
  23. 23.
    Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30(10):528–537PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Suresh B, Ravishankar GA (2004) Phytoremediation – a novel and promising approach for environmental clean-up. Crit Rev Biotechnol 24(2–3):97–124PubMedCrossRefGoogle Scholar
  25. 25.
    Schröder P, Daubner D, Maier H, Neustifter J, Debus R (2008) Phytoremediation of organic xenobiotics – glutathione dependent detoxification in Phragmites plants from European treatment sites. Bioresour Technol 99:7183–7191PubMedCrossRefGoogle Scholar
  26. 26.
    Newman L, Strand S, Choe N, Duffy J, Ekuan G, Ruszaj M, Shurtleff BB, Wilmoth J, Heilman P, Gordon MP (1997) Uptake and biotransformation of trichloroethylene by hybrid poplars. Environ Sci Technol 31:1062–1067CrossRefGoogle Scholar
  27. 27.
    Gordon MP, Choe N, Duffy J, Ekuan G, Heilman P, Muiznieks I, Ruszaj M, Shurtleff BB, Strand SE, Wilmoth J, Newman LA (1998) Phytoremediation of trichloroethylene with hybrid poplars. Environ Health Perspect 106:1001–1004PubMedPubMedCentralGoogle Scholar
  28. 28.
    Doty SL, Shang QT, Wilson AM, Moore AL, Newman LA, Strand SE, Gordon MP (2003) Metabolism of the soil and groundwater contaminants, ethylene dibromide and trichloroethylene, by the tropical leguminous tree, Leucaena leucocephala. Water Res 37:441–449PubMedCrossRefGoogle Scholar
  29. 29.
    González PS, Ontañon OM, Armendariz AL, Talano MA, Paisio CE, Agostini E (2013) Brassica napus hairy roots and rhizobacteria for phenolic compounds removal. Environ Sci Pollut R 20:1310–1317CrossRefGoogle Scholar
  30. 30.
    Ontañon OM, González PS, Ambrosio LF, Paisio CE, Agostini E (2014) Rhizoremediation of phenol and chromium by the synergistic combination of a native bacterial strain and Brassica napus hairy roots. Int Biodeter Biodegr 88:192–198CrossRefGoogle Scholar
  31. 31.
    Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540Google Scholar
  32. 32.
    Sevón N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868PubMedCrossRefGoogle Scholar
  33. 33.
    Zhou ML, Zhu XM, Shao JR, Tang YX, Wu YM (2011) Production and metabolic engineering of bioactive substances in plant hairy root culture. Appl Microbiol Biotechnol 90:1229–1239PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Armitage P, Walden R, Draper J (1988) Vectors for the transformation of plant cells using Agrobacterium. In: Draper J, Scott R, Armitage P, Walden R (eds) Plant genetic transformation and gene expression – a laboratory manual. Blackwell, Oxford, pp 3–67Google Scholar
  35. 35.
    Riva GA, González-Cabrera J, Vázquez-Padrón R, Ayra-Pardo C (1998) Agrobacterium tumefaciens: a natural tool for plant transformation. Electron J Biotechnol 1(3):1–16Google Scholar
  36. 36.
    Pacurar DI, Thordal-Christensen H, Pacurar ML, Pamfil D, Botez C, Bellini C (2011) Agrobacterium tumefaciens: from crown gall tumors to genetic transformation. Physiol Mol Plant P 76:76–81CrossRefGoogle Scholar
  37. 37.
    Chandra S (2012) Natural plant genetic engineer Agrobacterium rhizogenes: role of T-DNA in plant secondary metabolism. Biotechnol Lett 34:407–415PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17:147–154PubMedCrossRefGoogle Scholar
  39. 39.
    Alvarez MA, Talou JR, Paniego NB, Giulietti AM (1994) Solasodine production in transformed organ cultures (roots and shoots) of Solanum elaeagnifolium Cav. Biotechnol Lett 16(4):393–396CrossRefGoogle Scholar
  40. 40.
    Lorence A, Medina-Bolivar F, Nessler CL (2004) Campothecin and 10-hydroxycamptothecin from Camptotheca acuminata hairy roots. Plant Cell Rep 22:437–441PubMedCrossRefGoogle Scholar
  41. 41.
    Woods RR, Geyer BC, Mor TS (2008) Hairy-root organ cultures for the production of human acetylcholinesterase. BMC Biotechnol 8:95PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Georgiev MI, Pavlov AI, Bley T (2007) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185CrossRefPubMedGoogle Scholar
  43. 43.
    Georgiev MI, Ludwig-Müller J, Bley T (2010) Hairy root culture: copying nature in new bioprocesses. In: Arora R (ed) Medicinal plant b. CAB International, Wallingford, pp 156–175Google Scholar
  44. 44.
    Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Harnessing the potential of hairy roots: dawn of a new era. Trends Biotechnol 24:403–409PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 9:341–346PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395CrossRefGoogle Scholar
  47. 47.
    Ono NN, Tian L (2011) The multiplicity of hairy root cultures: prolific possibilities. Plant Sci 180:439–446PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Banerjee S, Singh S, Rahman LU (2012) Biotransformation studies using hairy root cultures–a review. Biotechnol Adv 30(3):461–468PubMedCrossRefGoogle Scholar
  49. 49.
    Huang TK, McDonald KA (2012) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol Adv 30(2):398–409PubMedCrossRefGoogle Scholar
  50. 50.
    Roychowdhury D, Majumder A, Jha S (2013) Agrobacterium rhizogenes-mediated transformation in medicinal plants: prospects and challenges. In: Chandra S et al (eds) Biotechnology for medicinal plants. Springer, Berlin/Heidelberg, pp 29–68CrossRefGoogle Scholar
  51. 51.
    Banerjee S, Shang TQ, Wilson AM, Moore AL, Strand SE, Gordon MP, Doty SL (2002) Expression of functional mammalian P450 2E1 in hairy root cultures. Biotechnol Bioeng 77(4):462–466PubMedCrossRefGoogle Scholar
  52. 52.
    Flocco CG, Giulietti AM (2007) In vitro hairy root cultures as a tool for phytoremediation research. In: Willey N (ed) Methods in biotechnology 23: phytoremediation: methods and reviews series. Humana Press, Totowa, pp 161–173Google Scholar
  53. 53.
    Nepovím A, Podlipná R, Soudek P, Schröder P, Vaněk T (2004) Effects of heavy metals and nitroaromatic compounds on horseradish glutathione S-transferase and peroxidase. Chemosphere 57:1007–1015PubMedCrossRefGoogle Scholar
  54. 54.
    Agostini E, Coniglio MS, Milrad SR, Tigier HA, Giulietti AM (2003) Phytoremediation of 2,4-dichlorophenol by Brassica napus hairy root cultures. Biotechnol Appl Biochem 37:139–144PubMedCrossRefGoogle Scholar
  55. 55.
    Talano MA, Frontera S, González P, Medina MI, Agostini E (2010) Removal of 2,4-diclorophenol from aqueous solutions using tobacco hairy root cultures. J Hazard Mater 176(1–3):784–791PubMedCrossRefGoogle Scholar
  56. 56.
    Angelini VA, Orejas J, Medina MI, Agostini E (2011) Scale up of 2,4-dichlorophenol removal from aqueous solutions using Brassica napus hairy roots. J Hazard Mater 185(1):269–274PubMedCrossRefGoogle Scholar
  57. 57.
    Sosa Alderete LG, Agostini E, Medina MI (2011) Antioxidant response of tobacco (Nicotiana tabacum) hairy roots after phenol treatment. Plant Physiol Biochem 49:1020–1028PubMedCrossRefGoogle Scholar
  58. 58.
    Suza W, Harris RS, Lorence A (2008) Hairy roots: from high-value metabolite production to phytoremediation. Electron J Integr Biosci 3(1):57–65Google Scholar
  59. 59.
    Doran PM (2011) Hairy root studies in phytoremediation and phytomining. In: Golubev IA (ed) Handbook of phytoremediation. Nova Science, New York, pp 591–612Google Scholar
  60. 60.
    Miland E, Smyth MR, Fágáin C (1996) Phenol removal by modified peroxidases. J Chem Technol Biotechnol 67:227–236CrossRefGoogle Scholar
  61. 61.
    Singh S, Melo JS, Eapen S, D’Souza SF (2006) Phenol removal using Brassica juncea hairy roots: role of inherent peroxidase and H2O2. J Biotechnol 123:43–49PubMedCrossRefGoogle Scholar
  62. 62.
    Araujo BS, Dec J, Bollag JM, Pletsch M (2006) Uptake and transformation of phenols and chlorophenols by hairy root cultures of Daucus carota, Ipomoea batatas and Solanum aviculare. Chemosphere 63:642–651PubMedCrossRefGoogle Scholar
  63. 63.
    González PS, Capozucca C, Tigier HA, Milrad SR, Agostini E (2006) Phytoremediation of phenol from wastewater, by peroxidases of tomato hairy root cultures. Enzym Microb Technol 39:647–653CrossRefGoogle Scholar
  64. 64.
    Coniglio MS, Busto VD, González PS, Medina MI, Milrad S, Agostini E (2008) Application of Brassica napus hairy root cultures for phenol removal from aqueous solutions. Chemosphere 72:1035–1042PubMedCrossRefGoogle Scholar
  65. 65.
    Huang Q, Tang J, Webet WJ Jr (2005) Precipitation of enzyme-catalyzed phenol oxidative coupling products: background ion and pH effects. Water Res 39:3021–3027PubMedCrossRefGoogle Scholar
  66. 66.
    Prpich GP, Daugulis AJ (2005) Enhanced biodegradation of phenol by a microbial consortium in a solid-liquid two-phase partitioning bioreactor. Biodegradation 16:329–339PubMedCrossRefGoogle Scholar
  67. 67.
    Nair CI, Jayachandran K, Shashidha S (2008) Biodegradation of phenol: a review. Afr J Biotechnol 7(25):4951–4958Google Scholar
  68. 68.
    Wevar Oller AL, Agostini E, Talano MA, Capozucca C, Milrad SR, Tigier HA, Medina MI (2005) Overexpression of a basic peroxidase in transgenic tomato (Lycopersicon esculentum Mill. cv. Pera) hairy roots increases phytoremediation of phenol. Plant Sci 169:1102–1111CrossRefGoogle Scholar
  69. 69.
    Jha P, Jobby R, Kudale S, Modi N, Dhaneshwar A, Desai N (2013) Biodegradation of phenol using hairy roots of Helianthus annuus L. Int Biodeter Biodegr 77:106–113CrossRefGoogle Scholar
  70. 70.
    Mazaheri H, Piri K (2015) Removal of phenol by A. belladonna L. hairy root. Int J Phytoremediation 17:1212–1219PubMedCrossRefGoogle Scholar
  71. 71.
    Harvey PJ, Campanella BF, Castro PML, Harms H, Lichtfouse E, Schäffner AR, Smrcek S, Werck-Reichhart D (2002) Phytoremediation of polyaromatic hydrocarbons, anilines and phenols. Environ Sci Pol 9(1):29–47CrossRefGoogle Scholar
  72. 72.
    Edwards R, Santillo D (1996) The stranger; the chlorine industry in India. In: Kellett R (ed) Uses of elemental chlorine. Greenpeace International, Amsterdam, pp 23–41Google Scholar
  73. 73.
    Rezek J, Macek T, Mackova M, Tříska J (2007) Plant metabolites of polychlorinated biphenyls in hairy root culture of black nightshade Solanum nigrum SNC-9O. Chemosphere 69:1221–1227PubMedCrossRefGoogle Scholar
  74. 74.
    Skaare JU, Larsen HJ, Lie E, Bernhoft A, Derocher AE, Norstrom R, Ropstad E, Lunn NF, Wiig O (2002) Ecological risk assessment of persistent organic pollutants in the arctic. Toxicology 181–182:193–197PubMedCrossRefGoogle Scholar
  75. 75.
    Petrik J, Drobna B, Pavuk M, Jursa S, Wimmerova S, Chovancova J (2006) Serum PCBs and organochlorine pesticides in Slovakia: age, gender and residents as determinants of organochlorine concentrations. Chemosphere 65:410–418PubMedCrossRefGoogle Scholar
  76. 76.
    Van Aken JM, Correa PA, Schnoor JL (2010) Phytoremediation of polychlorinated biphenyls: new trends and promises. Environ Sci Technol 44:2767–2776PubMedCentralCrossRefGoogle Scholar
  77. 77.
    Rezek J, Macek T, Doubsky J, Macková M (2012) Metabolites of 2,20-dichlorobiphenyl and 2,6-dichlorobiphenyl in hairy root culture of black nightshade Solanum nigrum SNC-9O. Chemosphere 89:383–388PubMedCrossRefGoogle Scholar
  78. 78.
    Morita M, Yamazaki T, Kamiya T, Takano H, Fuse O, Manabe E, Maruta T (2001) Method of decontaminating medium containing polychlorinated biphenyls or dioxins. US20016303844Google Scholar
  79. 79.
    Kučerová P, Macková M, Chromá L, Burkhard J, Tříska J, Demnerová K, Macek T (2000) Metabolism of polychlorinated biphenyls by Solanum nigrum hairy root clone SNC-90 and analysis of transformation products. Plant Soil 225:109–115CrossRefGoogle Scholar
  80. 80.
    Rezek J, Macek T, Macková M, Tříska J, Ruzickova K (2008) Hydroxy-PCBs, methoxy-PCBs and hydroxy–methoxy-PCBs: metabolites of polychlorinated biphenyls formed in vitro by tobacco cells. Environ Sci Technol 42:5746–5751PubMedCrossRefGoogle Scholar
  81. 81.
    Gujarathi NP, Haney BJ, Park HJ, Wickramasinghe SR, Linden JC (2005) Hairy roots of Helianthus annuus: a model system to study phytoremediation of tetracycline and oxytetracycline. Biotechnol Prog 21:775–780PubMedCrossRefGoogle Scholar
  82. 82.
    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. Environ Sci Pollut Res 16:206–213CrossRefGoogle Scholar
  83. 83.
    Hughes JB, Shanks J, Vanderford M, Lauritzen J, Bhadra R (1997) Transformation of TNT by aquatic plants and plant tissue cultures. Environ Sci Technol 31:266–271CrossRefGoogle Scholar
  84. 84.
    Bhadra R, Wayment DG, Hughes JB, Shanks JV (1999) Confirmation of conjugation processes during TNT metabolism by axenic plant roots. Environ Sci Technol 33:446–452CrossRefGoogle Scholar
  85. 85.
    Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110:125–128PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Suresh B, Sherkhane PD, Kale S, Eapen S, Ravishankar GA (2005) Uptake and degradation of DDT by hairy root cultures of Cichorium intybus and Brassica juncea. Chemosphere 61:1288–1292PubMedCrossRefGoogle Scholar
  87. 87.
    Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80PubMedCrossRefGoogle Scholar
  88. 88.
    Nigam R, Srivastava S, Prakash S, Srivastava MM (2001) Cadmium mobilisation and plant availability- the impact of organic acids commonly exuded from roots. Plant Soil 230:107–113CrossRefGoogle Scholar
  89. 89.
    Banat IM, Nigam P, Singh D, Marchant R (1996) Microbial decolorization of textile-dye containing effluents: a review. Bioresour Technol 58:217–227CrossRefGoogle Scholar
  90. 90.
    Khandare RV, Kabra AN, Tamboli DP, Govindwar SP (2011) The role of Aster amellus Linn. in the degradation of a sulfonated azo dye Remazol Red: a phytoremediation strategy. Chemosphere 82:1147–1154PubMedCrossRefGoogle Scholar
  91. 91.
    Patil P, Desai N, Govindwar S, Jadhav JP, Bapat V (2009) Degradation analysis of Reactive Red 198 by hairy roots of Tagetes patula L. (Marigold). Planta 230:725–735PubMedCrossRefGoogle Scholar
  92. 92.
    Telke AA, Kagalkar AN, Jagtap UB, Desai NS, Bapat VA, Govindwar SP (2011) Biochemical characterization of laccase from hairy root culture of Brassica juncea L. and role of redox mediators to enhance its potential for the decolorization of textile dyes. Planta 234:1137–1149PubMedCrossRefGoogle Scholar
  93. 93.
    Ghodake GS, Telke AA, Jadhav JP, Govindwar SP (2009) Potential of Brassica juncea in order to treat textile effluent contaminated sites. Int J Phytoremediation 11:297–312CrossRefGoogle Scholar
  94. 94.
    Kagalkar AN, Jagatap UB, Jadhav JP, Bapat VA, Govindwar SP (2009) Biotechnological strategies for phytoremediation of the sulphonated azo dye Direct Red 5B using Blumea malcolmii Hook. Bioresour Technol 100:4104–4110PubMedCrossRefGoogle Scholar
  95. 95.
    Kagalkar AN, Jagatap UB, Jadhav JP, Govindwar SP, Bapat VA (2010) Studies on phytoremediation potentiality of Typhonium flagelliforme for the degradation of Brilliant Blue R. Planta 232:271–285PubMedCrossRefGoogle Scholar
  96. 96.
    Lokhande VH, 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. Biosci Rep 8:56–63Google Scholar
  97. 97.
    Al-Salhi R, Abdul-Sada A, Lange A, Tyler CR, Hill EM (2012) The xenometabolome and novel contaminant markers in fish exposed to a wastewater treatment works effluent. Enviro Sci Technol 46:9080–9088CrossRefGoogle Scholar
  98. 98.
    Blüthgen N, Zucchi S, Fent K (2012) Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol Appl Pharmacol 263:184–194PubMedCrossRefGoogle Scholar
  99. 99.
    Coronado M, De Haro H, Deng X, Rempel MA, Lavado R, Schlenk D (2008) Estrogenic activity and reproductive effects of the UV-filter oxybenzone (2-hydroxy-4-methoxyphenyl-methanone) in fish. Aquat Toxicol 90:182–187PubMedCrossRefGoogle Scholar
  100. 100.
    Fent K, Kunz PY, Gomez E (2008) UV filters in the aquatic environment induce hormonal effects and affect fertility and reproduction in fish. Chimia 62:368–375CrossRefGoogle Scholar
  101. 101.
    Richardson SD, Ternes TA (2014) Water analysis: emerging contaminants and current issues. Anal Chem 86(6):2813–2848PubMedCrossRefGoogle Scholar
  102. 102.
    Chen F, Huber C, May R, Schröder P (2016) Metabolism of oxybenzone in a hairy root culture: perspectives for phytoremediation of a widely used sunscreen agent. J Hazard Mater 306:230–236PubMedCrossRefGoogle Scholar
  103. 103.
    Gratao PL, Prasad MNV, Cardoso PF, Lea PJ, Azevedo RA (2005) Phytoremediation: green technology for the clean up of toxic metals in the environment. Braz J Plant Physiol 17:53–64CrossRefGoogle Scholar
  104. 104.
    Rajkumar M, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160PubMedCrossRefGoogle Scholar
  105. 105.
    Nedelkoska TV, Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67(5):607–615PubMedCrossRefGoogle Scholar
  106. 106.
    Wu S, Zu Y, Wu M (2001) Cadmium response of the hairy root culture of the endangered species Adenophora lobophylla. Plant Sci 160(3):551–562PubMedCrossRefGoogle Scholar
  107. 107.
    Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnol Bioeng 83(2):158–167PubMedCrossRefGoogle Scholar
  108. 108.
    Godbold DL, Horst WJ, Collins JC, Thurman DA, Marschner H (1984) Accumulation of zinc and organic acids in roots of zinc tolerant and non-tolerant ecotypes of Deschampsia caespitosa. J Plant Physiol 116:59–69PubMedCrossRefGoogle Scholar
  109. 109.
    Krotz RM, Evangelou BP, Wagner GJ (1989) Relationships between cadmium, zinc, Cd-peptide and organic acid in tobacco suspension cells. Plant Physiol 91:780–787PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Tolrà RP, Poschenrieder C, Barceló J (1996) Zinc hyperaccumulation in Thlaspi caerulescens II. Influence on organic acids. J Plant Nutr 19:1541–1550CrossRefGoogle Scholar
  111. 111.
    Yang XE, Baligar VC, Foster JC, Martens DC (1997) Accumulation and transport of nickel in relation to organic acids in ryegrass and maize grown with different nickel levels. Plant Soil 196:271–276CrossRefGoogle Scholar
  112. 112.
    Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47(3:339–347CrossRefGoogle Scholar
  113. 113.
    Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717CrossRefGoogle Scholar
  114. 114.
    Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514CrossRefGoogle Scholar
  115. 115.
    Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefGoogle Scholar
  116. 116.
    Boominathan R, Doran PM (2003) Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J Biotechnol 101:131–146PubMedCrossRefGoogle Scholar
  117. 117.
    Nedelkoska TV, Doran PM (2001) Hyperaccumulation of nickel by hairy roots of Alyssum species: comparison with whole regenerated plants. Biotechnol Prog 17(4):752–759PubMedCrossRefGoogle Scholar
  118. 118.
    Vinterhalter B, Savić J, Platisă 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 Tiss Org 94:299–303CrossRefGoogle Scholar
  119. 119.
    Eapen S, Suseelan KN, Tivarekar S, Kotwal SA, Mitra R (2003) Potential for rhizofiltration of uranium using hairy root cultures of Brassica juncea and Chenopodium amaranticolor. Environ Res 91:127–133PubMedCrossRefGoogle Scholar
  120. 120.
    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 1:15–28Google Scholar
  121. 121.
    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. Environ Exp Bot 65:82–89CrossRefGoogle Scholar
  122. 122.
    Nedelkoska TV, Doran PM (2000) Characteristics of heavy metal uptake by plant species with potential for phytoremediation and phytomining. Miner Eng 13(5):549–561CrossRefGoogle Scholar
  123. 123.
    Subroto MA, Priambodo S, Indrasti NS (2007) Accumulation of zinc by hairy root cultures of Solanum nigrum. Biotechnology 6(3):344–348CrossRefGoogle Scholar
  124. 124.
    Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374PubMedCrossRefGoogle Scholar
  125. 125.
    Gerhardt KE, Dong Huang X, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30CrossRefGoogle Scholar
  126. 126.
    Patil SS (2014) Biodegradation study of phenol by Burkholderia sp. PS3 and Bacillus pumilus OS1 isolated from contaminated soil. Thesis, National Institute of Technology, RourkelaGoogle Scholar
  127. 127.
    Kowalska M, Bodzek M, Bohdziewicz J (1998) Biodegradation of phenols and cyanides using membranes with immobilized micro-organisms. Process Biochem 33:189–197CrossRefGoogle Scholar
  128. 128.
    Caballero-Mellado J, Onofre Lemus J, Estrada de los Santos P (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ibáñez SG, Medina MI, Agostini E (2011) Phenol tolerance, changes of antioxidative enzymes and cellular damage in transgenic tobacco hairy roots colonized by arbuscular mycorrhizal fungi. Chemosphere 83(5):700–705PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre of Advanced Study, Department of BotanyUniversity of CalcuttaKolkataIndia
  2. 2.Bethune CollegeKolkataIndia

Personalised recommendations