Abstract
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.
Similar content being viewed by others
Abbreviations
- 2,4-DCP:
-
2,4-dichlorophenol
- AMF:
-
Arbuscular mycorrhizal fungus
- Cd:
-
Cadmium
- cv:
-
Cultivar
- DDT:
-
1,1,1-trichloro-2,2-bis-(4´-chlorophenyl)ethylene
- DNA:
-
Deoxyribonucleic acid
- FTIR:
-
Fourier transform infrared spectroscopy
- GC–MS:
-
Gas chromatography–mass spectrometry
- h:
-
Hour
- HPLC:
-
High-performance liquid chromatography
- kb:
-
Kilobase
- min:
-
Minute
- NADH–DCIP reductase:
-
Nicotinamide adenine dinucleotide reduced–dichlorophenolindophenol reductase
- Ni:
-
Nickel
- OBZ:
-
Oxybenzone
- PCB:
-
Polychlorinated biphenyl
- Px:
-
Peroxidase
- TCE:
-
Trichloroethylene
- T-DNA:
-
Transferred DNA
- TNT:
-
2,4,6-trinitrotoluene
- U:
-
Uranium
- UV:
-
Ultraviolet
References
Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780
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 30:65–72
Arthur EL, Rice PJ, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation–an overview. Crit Rev Plant Sci 24:109–122
Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manag 105:103–120
Zhou ML, Tang YX, Wu YM (2013) Plant hairy roots for remediation of aqueous pollutants. Plant Mol Biol Report 31:1–8
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 33:738–742
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 25:20–31
Doran PM (2009) Application of plant tissue cultures in phytoremediation research: incentives and limitations. Biotechnol Bioeng 103:60–76
Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17(1):6–15
Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333
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 607–629
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, Halifax
Van Aken B (2009) Transgenic plants for enhanced phytoremediation of toxic explosives. Curr Opin Biotechnol 20:231–236
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 97:1017–1030
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39
Abhilash PC, Jamil S, Singh N (2009) Transgenic plants for enhanced biodegradation and phytoremediation of organic xenobiotics. Biotechnol Adv 27:474–488
Suthersan SS (1999) Phytoremediation. In: Suthersan SS (ed) Remediation engineering: design concepts. CRC Press LLC, Boca Raton
Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362
Baker AJM, Whiting SN (2002) In search of the Holy Grail – a further step in understanding metal hyperaccumulation? New Phytol 155:1–7
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 180:169–181
Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyperaccumulation metals in plants. Plant Soil 184:105–126
Al-Shalabi Z, Doran PM (2013) Metal uptake and nanoparticle synthesis in hairy root cultures. Adv Biochem Eng Biotechnol 134:135–153
Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30(10):528–537
Suresh B, Ravishankar GA (2004) Phytoremediation – a novel and promising approach for environmental clean-up. Crit Rev Biotechnol 24(2–3):97–124
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 99:7183–7191
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 31:1062–1067
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 106:1001–1004
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 37:441–449
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 20:1310–1317
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 88:192–198
Riker AJ (1930) Studies on infectious hairy root of nursery apple trees. J Agric Res 41:507–540
Sevón N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868
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 90:1229–1239
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 3–67
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):1–16
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 76:76–81
Chandra S (2012) Natural plant genetic engineer Agrobacterium rhizogenes: role of T-DNA in plant secondary metabolism. Biotechnol Lett 34:407–415
Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17:147–154
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):393–396
Lorence A, Medina-Bolivar F, Nessler CL (2004) Campothecin and 10-hydroxycamptothecin from Camptotheca acuminata hairy roots. Plant Cell Rep 22:437–441
Woods RR, Geyer BC, Mor TS (2008) Hairy-root organ cultures for the production of human acetylcholinesterase. BMC Biotechnol 8:95
Georgiev MI, Pavlov AI, Bley T (2007) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185
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 156–175
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 24:403–409
Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 9:341–346
Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395
Ono NN, Tian L (2011) The multiplicity of hairy root cultures: prolific possibilities. Plant Sci 180:439–446
Banerjee S, Singh S, Rahman LU (2012) Biotransformation studies using hairy root cultures–a review. Biotechnol Adv 30(3):461–468
Huang TK, McDonald KA (2012) Bioreactor systems for in vitro production of foreign proteins using plant cell cultures. Biotechnol Adv 30(2):398–409
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 29–68
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):462–466
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 161–173
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 57:1007–1015
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 37:139–144
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):784–791
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):269–274
Sosa Alderete LG, Agostini E, Medina MI (2011) Antioxidant response of tobacco (Nicotiana tabacum) hairy roots after phenol treatment. Plant Physiol Biochem 49:1020–1028
Suza W, Harris RS, Lorence A (2008) Hairy roots: from high-value metabolite production to phytoremediation. Electron J Integr Biosci 3(1):57–65
Doran PM (2011) Hairy root studies in phytoremediation and phytomining. In: Golubev IA (ed) Handbook of phytoremediation. Nova Science, New York, pp 591–612
Miland E, Smyth MR, Fágáin C (1996) Phenol removal by modified peroxidases. J Chem Technol Biotechnol 67:227–236
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 123:43–49
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 63:642–651
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 39:647–653
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 72:1035–1042
Huang Q, Tang J, Webet WJ Jr (2005) Precipitation of enzyme-catalyzed phenol oxidative coupling products: background ion and pH effects. Water Res 39:3021–3027
Prpich GP, Daugulis AJ (2005) Enhanced biodegradation of phenol by a microbial consortium in a solid-liquid two-phase partitioning bioreactor. Biodegradation 16:329–339
Nair CI, Jayachandran K, Shashidha S (2008) Biodegradation of phenol: a review. Afr J Biotechnol 7(25):4951–4958
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 169:1102–1111
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 77:106–113
Mazaheri H, Piri K (2015) Removal of phenol by A. belladonna L. hairy root. Int J Phytoremediation 17:1212–1219
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):29–47
Edwards R, Santillo D (1996) The stranger; the chlorine industry in India. In: Kellett R (ed) Uses of elemental chlorine. Greenpeace International, Amsterdam, pp 23–41
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 69:1221–1227
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 181–182:193–197
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 65:410–418
Van Aken JM, Correa PA, Schnoor JL (2010) Phytoremediation of polychlorinated biphenyls: new trends and promises. Environ Sci Technol 44:2767–2776
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 89:383–388
Morita M, Yamazaki T, Kamiya T, Takano H, Fuse O, Manabe E, Maruta T (2001) Method of decontaminating medium containing polychlorinated biphenyls or dioxins. US20016303844
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 225:109–115
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 42:5746–5751
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 21:775–780
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 16:206–213
Hughes JB, Shanks J, Vanderford M, Lauritzen J, Bhadra R (1997) Transformation of TNT by aquatic plants and plant tissue cultures. Environ Sci Technol 31:266–271
Bhadra R, Wayment DG, Hughes JB, Shanks JV (1999) Confirmation of conjugation processes during TNT metabolism by axenic plant roots. Environ Sci Technol 33:446–452
Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110:125–128
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 61:1288–1292
Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80
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 230:107–113
Banat IM, Nigam P, Singh D, Marchant R (1996) Microbial decolorization of textile-dye containing effluents: a review. Bioresour Technol 58:217–227
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 82:1147–1154
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 230:725–735
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 234:1137–1149
Ghodake GS, Telke AA, Jadhav JP, Govindwar SP (2009) Potential of Brassica juncea in order to treat textile effluent contaminated sites. Int J Phytoremediation 11:297–312
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 100:4104–4110
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 232:271–285
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 8:56–63
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 46:9080–9088
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 263:184–194
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 90:182–187
Fent K, Kunz PY, Gomez E (2008) UV filters in the aquatic environment induce hormonal effects and affect fertility and reproduction in fish. Chimia 62:368–375
Richardson SD, Ternes TA (2014) Water analysis: emerging contaminants and current issues. Anal Chem 86(6):2813–2848
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 306:230–236
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 17:53–64
Rajkumar M, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160
Nedelkoska TV, Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol Bioeng 67(5):607–615
Wu S, Zu Y, Wu M (2001) Cadmium response of the hairy root culture of the endangered species Adenophora lobophylla. Plant Sci 160(3):551–562
Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnol Bioeng 83(2):158–167
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 116:59–69
Krotz RM, Evangelou BP, Wagner GJ (1989) Relationships between cadmium, zinc, Cd-peptide and organic acid in tobacco suspension cells. Plant Physiol 91:780–787
Tolrà RP, Poschenrieder C, Barceló J (1996) Zinc hyperaccumulation in Thlaspi caerulescens II. Influence on organic acids. J Plant Nutr 19:1541–1550
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 196:271–276
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(3:339–347
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 33:713–717
Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
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 101:131–146
Nedelkoska TV, Doran PM (2001) Hyperaccumulation of nickel by hairy roots of Alyssum species: comparison with whole regenerated plants. Biotechnol Prog 17(4):752–759
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 94:299–303
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 91:127–133
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 1:15–28
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 65:82–89
Nedelkoska TV, Doran PM (2000) Characteristics of heavy metal uptake by plant species with potential for phytoremediation and phytomining. Miner Eng 13(5):549–561
Subroto MA, Priambodo S, Indrasti NS (2007) Accumulation of zinc by hairy root cultures of Solanum nigrum. Biotechnology 6(3):344–348
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374
Gerhardt KE, Dong Huang X, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30
Patil SS (2014) Biodegradation study of phenol by Burkholderia sp. PS3 and Bacillus pumilus OS1 isolated from contaminated soil. Thesis, National Institute of Technology, Rourkela
Kowalska M, Bodzek M, Bohdziewicz J (1998) Biodegradation of phenols and cyanides using membranes with immobilized micro-organisms. Process Biochem 33:189–197
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 73:5308–5319
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):700–705
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing AG
About this entry
Cite this entry
Majumder, A., Ray, S., Jha, S. (2016). Hairy Roots and Phytoremediation. In: Pavlov, A., Bley, T. (eds) Bioprocessing of Plant In Vitro Systems. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-32004-5_22-1
Download citation
DOI: https://doi.org/10.1007/978-3-319-32004-5_22-1
Received:
Accepted:
Published:
Publisher Name: Springer, Cham
Online ISBN: 978-3-319-32004-5
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences