Abstract
Nuclear power reactors are operating in 31 countries around the world. Along with reactor operations, activities like mining, fuel fabrication, fuel reprocessing and military operations are the major contributors to the nuclear waste. The presence of a large number of fission products along with multiple oxidation state long-lived radionuclides such as neptunium (237Np), plutonium (239Pu), americium (241/243Am) and curium (245Cm) make the waste streams a potential radiological threat to the environment. Commonly high concentrations of cesium (137Cs) and strontium (90Sr) are found in a nuclear waste. These radionuclides are capable enough to produce potential health threat due to their long half-lives and effortless translocation into the human body. Besides the radionuclides, heavy metal contamination is also a serious issue. Heavy metals occur naturally in the earth crust and in low concentration, are also essential for the metabolism of living beings. Bioaccumulation of these heavy metals causes hazardous effects. These pollutants enter the human body directly via contaminated drinking water or through the food chain. This issue has drawn the attention of scientists throughout the world to device eco-friendly treatments to remediate the soil and water resources. Various physical and chemical treatments are being applied to clean the waste, but these techniques are quite expensive, complicated and comprise various side effects. One of the promising techniques, which has been pursued vigorously to overcome these demerits, is phytoremediation. The process is very effective, eco-friendly, easy and affordable. This technique utilizes the plants and its associated microbes to decontaminate the low and moderately contaminated sites efficiently. Many plant species are successfully used for remediation of contaminated soil and water systems. Remediation of these systems turns into a serious problem due to various anthropogenic activities that have significantly raised the amount of heavy metals and radionuclides in it. Also, these activities are continuously increasing the area of the contaminated sites. In this context, an attempt has been made to review different modes of the phytoremediation and various terrestrial and aquatic plants which are being used to remediate the heavy metals and radionuclide-contaminated soil and aquatic systems. Natural and synthetic enhancers, those hasten the process of metal adsorption/absorption by plants, are also discussed. The article includes 216 references.
Similar content being viewed by others
References
Abdallah MA (2012) Phytoremediation of heavy metals from aqueous solutions by two aquatic macrophytes, Ceratophyllum demersum and lemna gibba L. Environ Technol 33:1609–1614
Aboudrar W, Schwartz C, Morel JL, Boularbah A (2013) Effect of nickel-resistant rhizosphere bacteria on the uptake of nickel by the hyperaccumulator Noccaea caerulescens under controlled conditions. J Soil Sediment 3:501–507
Ali MB, Vajpayee P, Tripathi RD, Rai UN, Singh SN, Singh SP (2003) Phytoremediation of lead, nickel, and copper by Salix acmophylla Boiss.: role of antioxidant enzymes and antioxidant substances. Bull Environ Contam Toxicol 70:462–469
Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soil. Bioresource Technol 79:273–276
Andreazza R, Bortolon L, Pieniz S, Camargo FAO, Bortolon ESO (2013) Copper phytoextraction and phytostabilization by Brachiaria decumbens Stapf. in vineyard soils and a copper mining waste. Open J Soil Sci 3:273–282
Anjum NA, Umar S, Iqbal M (2014) Assessment of cadmium accumulation, toxicity, and tolerance in Brassicaceae and Fabaceae plants—implications for phytoremediation. Environ Sci Pollut Res Int. doi:10.1007/s11356-014-2889-5
Arora M, Kiran B, Rani S, Rani A, Kaur B, Mittal N (2008) Heavy metal accumulation in vegetables irrigated with water from diff sources. Food Chem 111:811–815
Arriagada C, Pereira G, Garcıa-Romera I, Ocampo JA (2010) Improved zinc tolerance in Eucalyptus globulus inoculated with Glomus deserticola and Trametes versicolor or Coriolopsis rigida. Soil Biol Biochem 42:118–124
Awad F, Romheld V (2000) Mobilization of heavy metals from contaminated calcareous soils by plant born, microbial and synthetic chelators and their uptake by wheat plants. J Plant Nutr 23:1847–1855
Balarama Krishna MV, Arunachalam J, Murali MS, Kumar S, Manchanda VK (2004) Performance of immobilized moss in the removal of 137Cs and 90Sr from actual low level waste solution. J Radioanal Nucl Chem 261:551–557
Baldwin PR, Butcher DJ (2007) Phytoremediation of arsenic by two hyperaccumulators in a hyroponic environment. Microchem J 85:297–300
Bange GGJ, Overstreet R (1960) Some observation on absorption of cesium by excised barley roots. Plant Physiol 35:605–608
Barea J, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778
Barlow R, Bryant N, Andersland J, Sahi S (2000) Lead hyperaccumulation by Sesbania drummondii. Proceedings of the 2000 Conference on Hazardous Waste Research. 112–114
Barren F (2012) Chelate assisted phytoextraction using oilseed Brassicas. Plant Fam Brassicaceae 21:289–311
Bhatia NP, Walsh KB, Baker AJM (2005) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. J Exp Bot 56:1343–1349
Bidar G, Garcon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium Perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553
Boonyapookana B, Parkpian P, Techapinyawat S, Delaune RD, Juqsujinda A (2005) Phytoremediation of lead by sunflower (Helianthus annuus), tobacco (Nicotiana tabacum), and vetiver (Vetiveria zizanioides). J Environ Sci Health A Toxicol Hazard Subst Environ Eng 40:117–137
Brambilla M, Fortunati P, Carini F (2002) Foliar and root uptake of 134Cs, 85Sr and 65Zn in processing tomato plants (Lycopersicon esculentum Mill.). J Environ Radioact 60:351–363
Brings B (2010) Use of modern ion exchange resins for removing radionuclides using a German PWR reactor as an example. Therm Eng 57:538–542
Bruce SL, Noller BN, Grigg AH, Mullen BF, Mulligan DR, Ritchie PJ, Currey N, Ng JC (2003) A field study conducted at Kidston gold mine, to evaluate the impact of arsenic and zinc from mine tailing to grazing cattle. Toxicol Lett 137:23–34
Brunetti G, Farrag K, Rovira PS, Nigro F, Senesi N (2011) Greenhouse and field studies on Cr, Cu, Pb and Zn phytoextraction by Brassica napus from contaminated soils in the Apulia region, Southern Italy. Geoderma 160:517–523
Caldwell EF, Duff MC, Ferguson CE, Coughlin DP, Hicks RA, Dixon E (2012) Bio-monitoring for uranium using stream-side terrestrial plants and macrophytes. J Environ Monit 14:968–976
Carvalho FP, Oliveira JM, Malta M (2011) Radionuclides in plants growing on sludge and water from uranium mine water treatment. Ecol Eng 37:1058–1063
Chekol T, Vough LR, Chaney RL (2004) Phytoremediation of polychlorinated biphenyl-contaminated soils: the rhizosphere effect. Environ Int 30:799–804
Chen BD, Zhu YG, Smith FA (2006) Effects of arbuscular mycorrhizal inoculation on uranium and arsenic accumulation by Chinese brake fern (Pteris vittata L.) from a uranium mining-impacted soil. Chemosphere 62:1464–1473
Chen KF, Yeh TY, Lin CF (2012) Phytoextraction of Cu, Zn, and Pb enhanced by chelators with vetiver (Vetiveria zizanioides): hydroponic and pot experiments. International Scholarly Research Network ID 729693
Chiang PN, Wand MK, Wang JJ, Chih C (2005) Low-molecular-weight organic acids exudation of rape (Brassica campestris) roots in cesium-contaminated soils. Soil Sci 170:726–733
Chiang K, Wang Y, Wang M, Chiang P (2006) Low-molecular-weight organic acids and metal speciation in rhizosphere and bulk soils of a temperate rain forest in Chitou, Taiwan. Taiwan J Sci 21(3):327–337
Chinmayee MD, Mahesh B, Pradesh S, Mini I, Swapna TS (2012) The assessment of phytoremediation potential of invasive weed Amaranthus spinosus L. Appl Biochem Biotechnol 167:1550–1559
Chunilall V, Kindness A, Jonnalagadda SB (2005) Heavy metal uptake by two edible Amaranthus herbs grown on soils contaminated with lead, mercury, cadmium, and nickel. J Environ Sci Health 40:375–384
Citterio S, Santagostino A, Fumagalli P, Prato N, Ranalli P, Sgorbati S (2003) Heavy metal tolerance and accumulation of Cd, Cr and Ni by Cannabis sativa L. Plant Soil 256:243–252
Cobbett CS (2000) Phytochetins and their roles in heavy metal detoxification. Plant Physiol 123:825–832
Coinchelin D, Bartoli F, Robin C, Echevarria G (2012) Ecophysiology of nickel phytoremediation: a simplified biophysical approach. J Exp Bot. doi:10.1093/jxb/ers230
Conesa HM, Faz A, Arnaldos R (2006) Heavy metal accumulation and tolerance in plants from mine tailing of the semiarid Cartagena-La union mining district (SE Spain). Sci Total Environ 366:01–11
Cook LL, Inouye RS, McGonigle TP (2009) Evaluation of four grasses for use in phytoremediation of cs-contaminated arid land soil. Plant Soil 324:169–184
Couselo JL, Corredoira E, Vieitez AM, Ballester A (2012) Plant tissue culture of fast growing trees for phytoremediation research. Methods Mol Biol 877:247–263
Dahmani-Muller H, Oort FV, Gelle B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238
Danh LT, Truong P, Mammucari R, Tran T, Foster N (2009) Vetiver grass, Vetiveria zizanioides: a choice plant for phytoremediation of heavy metals and organic wastes. Int J Phytoremediation 11:664–691
De Souza Costa ET, Guilherme LR, De Melo EE, Ribeiro BT, Inácio EDSB, Severiano EC, Faquin V, Hale BA (2012) Assessing the tolerance of castor bean to Cd and Pb for phytoremediation purposes. Biol Trace Elem Res 145:93–100
Dellantonio A, Fitz WJ, Repmann F, Wenzel WW (2010) Disposal of coal compustion residues in terrestrial systems: contamination and risk management. J Environ Qual 13:761–775
Dong WQY, Cui Y, Liu X (2001) Instances of soil and crop heavy metal contamination in china. Soil Sediment Contam 10:497–510
Doumett S, Lamperi L, Checchni L, Azzarello E, Mugnai S, Mancuso S, Petruzzelli G, Bubba MD (2008) Heavy metal distribution between contaminated soil and Paulownia tomentosa, in a pilot-scale assisted phytoremediation study: influence of different complexing agents. Chemosphere 72:1481–1490
Dushenkov V, Kumar PBAN, Motto H, Raskin I (1995) Rhizofilteration: the use of plants to remove heavy metals from aqueous streams. Environ Sci Technol 29:1239–1245
Dushenkov S, Vasudev D, Kapulnik Y, Gleba D, Fleisher D, Ting KC, Ensley B (1997) Removal of uranium from water using terrestrial plants. Environ Sci Technol 31:3468–3474
Eapen S, Singh S, Thorat V, Kaushik CP, Raj K, D’Souza SF (2006) Phytoremediation of radiostrontium (90Sr) and radiocesium (137Cs) using giant milky weed (Calotropis gigantea R.Br.) plants. Chemosphere 65:2071–2073
Efroymson RA, Sample BE, Suter GW (2001) Uptake of inorganic chemicals from soil by plant leaves: regressions of field data. Environ Toxicol Chem 20:2561–2571
Endo S, Kimura S, Takatsuji T, Nanasawa K, Imanaka T, Shizuma K (2012) Measurement of soil contamination by radionuclides due to the Fukushima Dai-ichi nuclear power plant accident and associated estimated cumulative external dose estimation. J Environ Radioact 111:18–27
Entry JA, Watrud LS, Reeves M (1997) Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Environ Pollut 104:449–457
Epelde L, Becerril JM, Mijangos I, Garbisu C (2009) Evaluation of the efficiency of a phytostabilization process with biological indicators of soil health. J Environ Qual 38:2041–2049
Essa A, Abd-Alsalam E, Ali R (2012) Biogenic volatile compounds of activated sludge and their application for metal bioremediation. Afr J Biotechnol 11:9993–10001
Euliss K, Ho C, Schwab AP, Rock S, Banks MK (2008) Greenhouse and field assessment of phytoremediation for petroleum contaminants in a riparian zone. Biores Technol 99:1961–1971
Farid M, Ali S, Shakoor MB, Bharwana SA, Rizvi H, Ehsan S, Tauqer HM, Iftikhar U, Hannan F (2013) EDTA assisted phytoremediation of cadmium, lead and zinc. Int J Agron Plant Prod 4(1):283–2846
Fowler SW, Buat-Menard P, Yokoyama Y, Ballestra S, Holm E, Nguyen HV (1987) Rapid removal of Chernobyl fallout from mediterranean surface waters by biological activity. Nature 329:56–58
Frerot H, Lefebvre C, Gruber W, Collin C, Dos Santos A, Escarre J (2006) Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant Soil 282:53–65
Fuhrmann M, Lasat MM, Ebbs SD, Kochian LV, Cornish J (2002) Uptake of cesium-137 and strontium-90 from contaminated soil by three plant species; application to phytoremediation. J Environ Qual 31:904–909
Fulekar MH, Singh A, Thorat V, Kaushik CP, Eapen S (2010) Phytoremediation of 137Cs from low level nuclear waste using Catharanthus roseus. Indian J Pure Appl Phy 48:516–519
Gao Y, Miao C, Wang Y, Xia J, Zhou P (2012) Metal-resistant microorganisms and metal chelators synergistically enhance the phytoremediation efficiency of Solanum nigrum L. in Cd- andPb-contaminated soil. Environ Technol 33:1383–1389
Gekeler W, Grill E, Winnacker E, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Microbiology 150:197–202
Gerhardt KE, Huang X, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30
Gohre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis ton heavy metal phytoremediation. Planta 223:1115–1122
Gonzaga MS, Santos JAG, Ma LQ (2006) Arsenic chemistry in the rhizosphere of Pteris vittata L. and Nephrolepis exaltata L. Environ Pollut 143:254–260
Grill E, Winnacker E, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci U S A 84:439–443
Gunduz S, Uygur FN, Kahramanoglu I (2012) Heavy metal phytoremediation potentials of Lepidum sativum L., Lactuca sativa L., Spinacia oleracea L. and Raphanus sativus L. Agric Food Sci Res 1:01–05
Hamadouche NA, Aoumeur H, Djediai SM, Aoues A (2012) Phytoremediation potential of Raphanus sativus L. for lead contaminated soil. Acta Biol Szeged 56:43–49
Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88:01–03
Hoseini PS, Poursafa P, Moattar F, Amin MM, Rezaei AH (2012) Ability of phytoremediation for absorption of strontium and cesium from soils using Cannabis sativa. Int J Environ Health Eng 1:01–05
Hua J, Zhang C, Yin Y, Chen R, Wang X (2012) Phytoremediation potential of three aquatic macrophytes in manganese-contaminated water. Water Environ J 26:335–342
Huang J, Blaylock MJ, Kapulnik Y, Ensley BD (1998) Phytoremediation of uranium-contaminated soils: role of organic acids in triggering uranium hyperaccumulation in plants. Environ Sci Technol 32:2004–2008
Huang X, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) A multi-process phytoremediation system for removal of polycyclic aromatic hydrocarbons from contaminated soils. Environ Pollut 130:465–476
Huhle B, Heilmeier H, Merkel B (2008) Potential of Brassica juncea and Helianthus annuus in phytoremediation for uranium. Uranium, Mining and Hydrogeology 307–318
Huikuri P, Salonen L, Raff O (1998) Removal of natural redionuclides from drinking water by point of entry reverse osmosis. Desalination 119:01–03
Irshad M, Ahmad S, Pervez A, Inoue M (2014) Phytoaccumulation of heavy metals in natural plants thriving on wastewater effluent at hattar industrial estate, Pakistan. Int J Phytoremediation. doi:10.1080/15226514.2013.862208
Islam M, Ueno Y, Sikder M, Kurasaki M (2013) Phytofiltration of arsenic and cadmium from the water environment using Micranthemum umbrosum (J.F. Gmel) S.F. Blake as a hyperaccumulator. Int J Phytoremediation. doi:10.1080/15226514.2012.751356
Jacob D, Otte M (2003) Conflicting processes in the wetland plant rhizosphere: metal retention or mobilization? Water Air Soil Pollut 3:91–104
Jadia CD, Fulekar MH (2008) Phytoremediation: the application of vermicompost to remove zinc, cadmium, copper, nickel and lead by sunflower plant. Environ Eng Manag J 7:547–558
Jaffre T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580
Jagatheeswari D, Vedhanarayanan P, Ranganathan P (2013) Phytoaccumulation of mercuric chloride polluted soil using tomato plants (Lycopersicon esculentum Mill.). Int J Res Bot 3(2):30–33
Jankong P, Visoottiviseth P (2008) Effects of arbuscular mycorrhizal inoculation on plants growing on arsenic contaminated soil. Chemosphere 72:1092–1097
Javaid A (2011) Importance of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soil. Biomanagement Metal-Contaminated Soil 20:125–141
Jia L, Wang W, Li Y, Yang L (2010) Heavy metals in soil and crops of an intensively farmed area: a case study in Yucheng city, Shandong province, China. Int J Environ Res Public Health 7:395–412
Jia Y, Huang H, Sun G, Zhao F, Zhu Y (2012) Pathways and relative contributions to arsenic volatilization from rice plants and paddy soil. Environ Sci Technol 46:8090–8096
Jung MC, Thornton I (1996) Heavy metal contamination of soils and plants in the vicinity of a lead-zinc mine, Korea. Appl Geochem 11:53–59
Kachenko AG, Singh B (2006) Heavy metals contamination in vegetables grown in urban and metal smelter contaminated sites in Australia. Water Air Soil Pollut 169:101–123
Kala M, Khan TI (2009) Heavy metal contamination in Pisum sativum var. Azad P-1 grown in Sanganerarea, Rajasthan (India). J Environ Sci Eng 51:163–168
Kanter U, Hauser A, Michalke B, Draxl S, Schaffner AR (2010) Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J Exp Bot 61:3995–4009
Ke HY, Sun JG, Feng XZ, Czako M, Marton L (2001) Differential mercury volatilization by tobacco organs expressing a modified bacterial merA gene. Cell Res 11(3):231–236
Keeling SM, Stewart RB, Anderson CW, Robinson BH (2003) Nickel and cobalt phytoextraction by the hyperaccumulator Berkheya coddii: implications for polymetallic phytomining and phytoremediation. Int J Phytoremediation 5:235–244
Khan AG, Kuel C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207
Khandare RV, Rane NR, Waghmode TR, Govindwar SP (2012) Bacterial assisted phytoremediation for enhanced degradation of highly sulfonated diazo reactive dye. Environ Sci Pollut Res Int 19:1709–1718
Khilji S, Bareen F (2008) Rhizofilteration of heavy metals from the tannery sludge by the anchored hydrophyte, Hydrocotyle umbellate L. Afr J Biotechnol 7:2711–3717
Kozdroj J, Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417
Kubota H, Takenaka C (2003) Arabis gemmifera is a hyperaccumulator of Cd and Zn. Int J Phytoremediation 5:197–201
Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg JJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Int 17:06–15
Kumar B, Smita K, Flores LC (2014) Plant mediated detoxification of mercury and lead. Arab J Chem. doi:10.1016/j.arabjc.2013.08.010
Kumari A, Lal B, Pakade YB, Chand P (2011) Assessment of bioaccumulation of heavy metal by Ptesis vittata L. growing in the vicinity of fly ash. Int J Phytoremediation 13:779–787
Lee M, Yang M (2010) Rhizofilteration using sunflower (Helianthus annuus L.) and bean (Phaseolus vulgaris L. var. vulgaris) to remediate uranium contaminated groundwater. J Hazard Mater 173:589–596
Lee DA, Chen A, Schroeder JI (2003) Ars1, an arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J 35:637–646
Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54:805–815
Lewandowski I, Schmidt U, Londo M, Faaij A (2006) The economic value of the phytoremediation function – assessed by the example of cadmium remediation by willow (Salix ssp.). Agric Syst 89:68–89
Li G, Hu N, Ding D, Zheng Y, Liu Y, Wang Y, Nie X (2011) Screening of plant species for phytoremediation of uranium, thorium, barium, nickel, strontium and lead contaminated soils from a uranium mill tailing repository in south china. Bull Environ Contam Toxicol 86:646–652
Li H, Wei D, Shen M, Zhou Z (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18
Lin Q, Mendelssohn IA (2009) Potential of restoration and phytoremediation with Juncus Roemerianus for diesel-contaminated coastal wetlands. Ecol Eng 35:85–91
Liu Y, Zhang H, Zeng G, Huang B, Li X (2006) Heavy metal accumulation in plants in Mn mine tailing. Pedophere 16:131–136
Liu D, Islam E, Ma J, Wamg X, Mahmood Q, Jin X, Li T, Yang X, Gupta D (2008) Optimization of chelator-assisted phytoextraction, using EDTA, lead and Sedum alfredii hence as a model system. Bull Environ Contam Toxicol 81:30–35
Lu N, Kung S, Manson CFV, Triay IR, Cotter CR, Pappas AJ, Pappas MEG (1998) Removal of plutonium-239 and americium-241 from rocky flats soil by leaching. Environ Sci Technol 32:370–374
Luksiene B, Marciulioniene D, Gudeliene I, Schonhofer F (2013) Accumulation and transfer of 137Cs and 90Sr in the plants of the forest ecosystem near the Ignalina nuclear power plant. J Environ Radioact 116:01–09
Lv Y, Deng X, Quan L, Xia Y, Shen Z (2012) Metallothioneins BcMT1 and BcMT2 from Brassica campestris enhance tolerance to cadmium and copper and decrease production of reactive oxygen species in Arabidopsis thaliana. Plant Soil 10:1007
Lyman GH, Lyman CG, Johnson W (1985) Association of leukemia with radium groundwater contamination. J Am Med Assoc 254:621–626
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
Mahieu S, Frerot H, Vidal C, Galiana A, Heulin K, Lucette M, Brunel B, Lefebvre C, Escarre J, Cleyet-marel J (2011) Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn, Pb and Cd. Plant Soil 342:405–417
Malik M, Chaney RL, Brewer EP, Li Y, Angle S (2000) Phytoextraction of soil cobalt using hyperaccumulator plants. Int J Phytoremediation 2:319–329
Mangkoedihardjo S, Surahmaida A (2008) Jatropha curcas L. for phytoremediation of lead and cadmium polluted soil. World Appl Sci J 4:519–522
Mason CFV, Turney WRJR, Thomson BM, Lu N, Longmire PA, Chisholm-Brause CJ (1997) Carbonate leaching of uranium from contaminated soil. Environ Sci Technol 31:2707–2711
Mcgrath SP, Zhao F (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282
McLaughlin MJ, Smolders E, Merckx R, Maes A (1997) Plant uptake of Cd and Zn in chelator-buffered nutrient solution depends on ligand type. Dev Plant Soil Sci 78:113–118
Megateli S, Semsari S, Couderchet M (2009) Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba. Ecotoxicol Environ Saf 6:1774–1780
Miretzky P, Saralegui A, Cirelli AF (2004) Aquatic macrophytes potential for the simultaneous removal of heavy metals (Buenos Aires, Argentina). Chemosphere 57:997–1005
Mishra VK, Tripathi BD (2008) Concurrent removal and accumulation of heavy metals by the three aquatic macrophytes. Bioresource Technol 99:7091–7097
Mkandawire M, Dudel EG (2005) Accumulation of arsenic in Lemna gibba L. (duckweed) in tailing waters of two abandoned uranium mining sites in Saxony, Germany. Sci Total Environ 336:81–89
Mleczek M, Rutkowski P, Rissmanna I, Kaczmarekc Z, Golinski P, Szentner K, Strazynska K, Stachowiak A (2010) Biomass productivity and phytoremediation potential of Salix alba and Salix viminalis. Biomass Bioenergy 34:1410–1418
Mohebbi AH, Harutyunyan SS, Chorom M (2012) Phytoremediation potential of three plants grown in monoculture and intercropping with date palm in contaminated soil. Int J Agricul Crop Sci 4:1523–1530
Mok H, Majumder R, Laidlaw WS, Gregory D, Baker AJM, Arndt SK (2012) Native Australian species are effective in extracting multiple heavy metals from biosolids. Int J Phytoremediation 15:615–632
Moogouei R, Borghei M, Arjmandi R (2011) Phytoremediation of stable Cs from solutions by Calendula alata, Amaranthus chlorostachys and Chenopodium album. Ecotoxicol Environ Saf 74:2036–2039
Muchuweti M, Birkett JW, Chiyanga E, Zvauya R, Scrimshaw MD, Lester JN (2006) Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agric Ecosyst Environ 112:41–48
Muratova A, Hubner T, Tischer S, Turkovskaya MM, Kuschk P (2003) Plant- rhizoflora association during phytoremediation of PAH contaminated soil. Int J Phytoremediation 5:137–151
Nanda S, Abraham J (2011) Impact of heavy metals on the rhizosphere microflora of Jatropha multifida and their effective remediation. Afr J Biotechnol 10:11948–11955
Neumann D, Nieden U (2001) Silicon and heavy metal tolerance of higher plants. Phytochem 556:685–692
Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23:06–08
Niazi NK, Singh B, Zwieten LV, Kachenko AG (2012) Phytoremediation of an arsenic-contaminated site using Pteris vittata L. and Pityrogramma calomelanos var. austroamericana: a long-term study. Environ Sci Pollut Res 19:3506–3515
Odjegba VJ, Fasidi IO (2004) Accumulation of trace elements by Pistia stratiotes: implications for phytoremediation. Ecotoxicology 13:637–646
Odjegba VJ, Fasidi IO (2007) Phytoremediation of heavy metals by Eichornia crassipes. Environmentalist 27:349–355
Olson PE, Castro A, Joern M, Duteau NM, Pilon-Smits E, Reardon KF (2008) Effects of agronomic practices on phytoremediation of an aged PAH-contaminated soil. J Environ Qual 37:1439–1446
Palmer CE, Warwick S, Keller W (2001) Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. Int J Phytoremediation 3:245–287
Pandey SN (2006) Accumulation of heavy metals (Cd, Cr, Cu, Ni and Zn) in Raphanus sativus L. and Spinacia oleracea L. plants irrigated with industrial effluent. J Environ Biol 27:381–384
Pandey J, Shubhashish K, Pandey R (2010) Heavy metal contamination of Ganga river at Varanasi in relation to atmospheric deposition. Trop Ecol 51:365–373
Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823
Parkyn SM, Davies-Colley RJ, Halliday NJ, Costley KJ, Croker GF (2003) Planted riparian buffer zones in New Zealand: do they live up to expectations? Restor Ecol 11:436–447
Parra LM, Torres G, Arenas AD, Sanchez E, Rodriguez K (2012) Phytoremediation of low levels of heavy metals using duckweed (Lemna minor). Abiotic Stress Responses in Plants 451–463
Pitre FE, Teodorescu TI, Labrecque M (2010) Brown field phytoremediation of heavy metals using Brassica and Salix supplemented with EDTA:results of the first growing season. J Environ Sci Eng 4:51–59
Poniedzialek M, Sekara A, Jedrszczyk E, Ciura J (2010) Phytoremediation efficiency of crop plants in removing cadmium, lead and zinc from soil. Folia Hortic 22:25–31
Prasad MNV (2007) Sunflower (Helianthus annuus L.) -a potential crop for environmental industry. Helia 46:167–174
Prasad MNV, Freitas HM (2003) Metal hyperaccumulation in plants –biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6:285–305
Rai PK (2008) Phytoremediation of Hg and Cd from industrial effluents using an aquatic free floating macrophyte Azolla pinnata. Int J Phytoremediation 10:430–439
Rai PK (2010) Microcosm investigation on phytoremediation of Cr using Azolla pinnata. Int J Phytoremediation 12:96–104
Ramaswami A, Carr P, Burkhardt M (2001) Plant-uptake of uranium: hydroponic and soil system studies. Int J Phytoremediation 3:189–201
Rathi V, Sambyal SS, Kulshreshtha H, Satvat PS (2011) Heavy metal bioaccumulation by Eisenia fetida, Cynodon dactylon and Vigna radiata in single, bi and tri-metal soil systems. Int J Technol Eng Syst 2:252–257
Rauret G, Vallejo VR, Cancio D, Real J (1995) Transfer of radionuclides in soil-plant systems following aerosol simulation of accidental release: design and first results. J Environ Radioact 29:163–184
Reboreda R, Cacador I (2008) Enzymatic activity in the rhizosphere of Spartina maritime: potential contribution for phytoremediation of metals. Mar Environ Res 65:77–84
Reichenauer TG, Germida JJ (2008) Phytoremediation of organic contaminants in soil and ground water. Chem Sus Chem 1:708–717
Ribeiro de Souza SC, López A, de Andrade S, Anjos de Souza L, Schiavinato MA (2012) Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage. J Environ Manage 110:299–307
Rizzi L, Petruzzelli G, Poggio G, Guidi GV (2004) Soil physical changes and plant availability of Zn and Pb in a treatability test of phytostabilization. Chemosphere 57:1039–1046
Robinson BH, Brooks RR, Howes AW, Kirkman GPEH (1997a) The potential of the high-biomass nickel hyperaccumulation Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126
Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, De Dominicis V (1997b) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86
Robinson BH, Brooks RR, Clothier BE (1999) Soil amendments effecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot 84:689–694
Rodriguez L, Rincon J, Asencio I, Rodriguez-Castellanos L (2007) Capability of selected crop plants for shoot mercury accumulation from polluted soil: phytoremediation perspectives. Int J Phytoremediation 9:01–13
Roongtanakiat N, Sudsawad P, Sudsawad N (2010) Uranium absorption ability of sunflower, vetiver and purple guinea grass. Kasetsart J: Nat Sci 44:182–190
Ruttenber AJ, Kreiss K, Douglas RL, Buhl TE, Millard J (1984) The assessment of human exposure to radionuclides from a uranium mill tailings release and mine dewatering effluent. Health Phys 47:21–35
Ruttens A, Colpaert JV, Mench M, Boisson J, Carleer R, Vangronsveld J (2006) Phytostabilization of a metal contaminated sandy soil. II: influence of compost and/or inorganic metal immobilizing soil amendments on metal leaching. Environ Pollut 144:553–559
Sahi SV, Natalie LB, Sharma NC, Singh SR (2002) Characterization of a lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Technol 36:4676–4680
Sakakibara M, Watanabe V, Sano S, Inoue M, Kaise T (2007) Phytoextraction and phytovolatilization of arsenic from As-contaminated soils by Pteris vittata. Proceedings of the annual international conference on soils, sediments, water and energy 12
Sampanpanish P, Pongsapich W, Khaodhiar S, Khan E (2006) Chromium removal from soil by phytoremediation with weed plant species in Thailand. Water Air Soil Pollut: Focus 6:191–206
Sandermann H (1992) Plant metabolism of xenobiotics. Trends Biochem Sci 17:82–84
Santos EA, Ladeira ACQ (2011) Recovery of uranium from mine wastes by leaching with carbonate-based reagents. Environ Sci Technol 45:3591–3597
Sarin V, Pant KK (2006) Removal of chromium from industrial waste by using eucalyptus bark. Bioresource Technol 97:15–20
Sasmaz A, Sasmaz M (2009) The phytoremediation potential for strontium of indigenous plants growing in a mining area. Environ Exp Bot 67:139–144
Sas-Nowosielskaa A, Kucharski R, Malkowski E, Pogrzeba M, Kuperberg JM, Krynski K (2004) Phytoextraction crop disposal—an unsolved problem. Environ Poll 128:373–379
Schuller P, Bunzi K, Voigt G, Krarup A, Castillo A (2004) Seasonal variation of the radiocaesium transfer soil-to-swiss chard (Beta vulgaris var. cicla L.) in allophonic soils from the lake region, Chile. J Environ Radioact 78:21–23
Sekabira K, Oryem-Origa H, Mutumba G, Kakudidi E, Basamba TA (2011) Heavy metal phytoremediation by Commelina benghalensis (L) and Cynodon dactylon (L) growing in urban stream sediments. Int J Plant Physiol Biochem 3:133–142
Seth CS, Misra V, Chauhan LK (2012) Accumulation, detoxification, and genotoxicity of heavy metals in Indian mustard (Brassica juncea L.). Int J Phytoremediation 14:01–13
Shaw LJ, Burns RG (2003) Biodegradation of organic pollutants in the rhizosphere. Adv Appl Microbiol 53:01–60
Shibamoto T, Yasuhara A, Katami T (2007) Dioxin formation from waste incineration. Rev Environ Contam Toxicol 190:01–41
Shivakumar CK, Hemavani C, Thippeswamy B, Krishnappa M (2011) Effect of inoculation with arbuscular mycorrhizal fungi on green gram grown in soil containing heavy metal zinc. J Exp Sci 2:17–21
Shivhare L, Sharma S (2012) Effects of toxic heavy metal contaminated soil on an ornamental plant Georgina wild (Dahlia). Environ Anal Toxicol 2
Shoji R, Yajima R, Yano Y (2008) Arsenic speciation for the phytoremediation by the Chinese brake fern, Pteris vittata. J Environ Sci 20:1463–1468
Simon L, Tamás J, Kovács E, Kovács B, Biró B (2006) Stabilisation of metals in mine spoil with amendments and growth of red fescue in symbiosis with mycorrhizal fungi. Plant Soil Environment 52:385–391
Singh S, Eapen S, Thorat V, Kaushik CP, Raj K, D’Souza SF (2008) Phytoremediation of cesium and strontium from solutions and low-level nuclear waste by Vetiveria zizanoides. Ecotoxicol Environ Saf 69:306–311
Singh S, Thorat V, Kaushik CP, Raj K, Eapen S, D’Souza SF (2009) Potential of chromolaena odorata for phytoremediation of 137Cs from solution and low level nuclear waste. J Hazard Mater 162:743–745
Singh S, Singh DP, Kumar N, Bhargava SK, Barman SC (2010) Accumulation and translocation of heavy metals in soil and plants from fly ash contaminated area. J Environ Biol 31:421–430
Singh D, Tiwari A, Gupta R (2012) Phytoremediation of lead from wastewater using aquatic plants. J Agric Sci Technol 8:01–11
Sinhal VK, Srivastava A, Singh VP (2010) EDTA and citric acid mediated phytoextraction of Zn, Cu, Pb and Cd through marigold (Tagetes erecta). J Environ Biol 31:255–259
Souza MP, Chu D, Zhao M, Zayed AM, Ruzin SE, Schichnes D, Terry N (1999a) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol 119:565–573
Souza MP, Huang CPA, Chee N, Terry N (1999b) Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta 209:259–263
Sun WH, Lo JB, Robert FM, Ray C, Tang CS (2004) Phytoremediation of petroleum hydrocarbons in tropical coastal soils. I. Selection of promising woody plants. Environ Sci Pollut Res Int 11:260–266
Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647–658
Tang S, Willey NJ (2003) Uptake of 134Cs by four species from the Asteraceae and two varieties from the Chenopodiaceae grown in two types of Chinese soil. Plant Soil 250:75–81
Taylor GJ, Crowder AA (1983) Uptake and accumulation of heavy metals by Typha latifolia in wetlands of the Sudbury, Ontario region. Can J Bot 61:63–73
Terry N, Zayed AM, De Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432
Tjahaja PI, Sukmabuana P, Roosmini D (2013) 123The EDTA amendment in phytoextraction of 134Cs from soil by Indian Mustard (Brassica juncea). Int J Phytoremediation. doi:10.1080/15226514.2013.783554
Turgut C, Pepe MK, Cutright TJ (2004) The effect of EDTA and citric acid on phytoremediation of Cd, Cr, and Ni from soil using Helianthus annuus. Environ Pollut 131:147–154
Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultramafic soils in South Africa. Mycorrhiza 13:185–190
Ucer A, Uyanik A, Kutbay HG (2013) Removal of heavy metals using Myriophyllum verticillatum (whorl-leaf watermilfoil) in a hydroponic system. Ekoloji 22(87):01–09
Venkatesan S, Kirithika M, Rajapriya R, Ganesan R, Muthuchelian K (2011) Improvement of economic phytoremediation with heavy metals tolerant rhizosphere bacteria. Int J Environ Sci 01:07
Vervaeke P, Tack FMG, Navez F, Martin J, Verloo MG, Lust N (2006) Fate of heavy metals during fixed bed downdraft gasification of willow wood harvested from contaminated sites. Biomass Bioenergy 30:58–65
Volkle H, Murith C, Surbeck H (1989) Fallout from atmospheric bomb tests and releases from nuclear installations. Radiat Phys Chem 34:261–277
Wang G, Li Q, Luo B, Chen X (2004) Ex planta phytoremediation of trichlorophenol and phenolics allelochemicals via an engineered secretory laccase. Nat Biotechnol 22:7
Wang F, Lin X, Yin R (2005) Heavy metal uptake by arbuscular mycorrizas of Elsholtzia splendens and the potential for phytoremediation of contaminated soil. Plant Soil 269:225–232
Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408
Wu CH, Wood TK, Mulchandani A, Chen W (2006) Engineering plant-microbe symbiosis for rhizoremediation of heavy metals. Appl Environ Microbiol 72:1129–1134
Wu L, Li Z, Akahane I, Liu L, Han C, Makino T, Luo Y, Christie P (2012) Effects of organic amendments on Cd, Zn and Cu bioavailability in soil with repeated phytoremediation by Sedum plumbizincicola. Int J Phytoremediation 14:1024–1038
Xiaomei L, Qitang W, Banks MK (2005) Effect of simultaneous establishment of Sedum alfredii and Zea mays on heavy metal accumulation in plants. Int J Phytoremediation 7:43–53
Xie W, Huang Q, Li G, Rensing C, Zhu Y (2013) Cadmium accumulation in the rootless macrophyte Wolffia globosa and its potential for phytoremediation. Int J Phytoremediation 15:385–397
Ximenez-Embun P, Madrid-Albarrán Y, Camara C, Cuadrado C, Burbano C, Muzquiz M (2001) Evaluation of Lupinus species to accumulate heavy metals from waste waters. Int J Phytoremediation 3:369–379
Xing W, Wu H, Hao B, Huang W, Liu G (2013) Bioaccumulation of heavy metals by submerged macrophytes: looking for hyperaccumulators in eutrophic lakes. Environ Sci Technol 47:4695–4703
Yadav BK, Siebei MA, Bruggen JJ (2011) Rhizofilteration of a heavy metal (lead) containing wastewater using the wetland plant Carex pendula. Soil Air Water 39:467–474
Yang XE, Ye HB, Long XX, He B, He ZI, Stoffella PJ, Calvert DV (2004) Uptake and accumulation of cadmium and zinc by Sedum alfredii Hance at different Cd/Zn supply levels. J Plant Nutrition 27:1963–1977
Yang S, Liang S, Yi L, Xu B, Cao J, Guo Y, Zhou Y (2014) Heavy metal accumulation and phytostabilization potential of dominant plant species growing on manganese mine tailings. Front Environ Sci Eng 8(3):394–404
Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464
Yoshida N, Kanda J (2012) Tracking the Fukushima radionuclides. Science 336:1115–1116
Zaier H, Ghnaya T, Rejeb K, Lakhdar A, Rejeb S, Jema F (2010) Effects of EDTA on phytoextraction of heavy metals (Zn, Mn and Pb) from sludge-amended soil with Brassica napus. Bioresource Technol 101:3978–3983
Zhang X, Hu Y, Liu Y, Chen B (2011) Arsenic uptake, accumulation and phytofilteration by duckweed (Spirodela polyrhiza L.). J Environ Sci 23:601–606
Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559
Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–885
Zhu YG, Shaw G (2000) Soil contamination with radionuclides and potential remediation. Chemosphere 41:121–128
Zhuang P, Yang QW, Wang HB, Shu WS (2007) Phytoextraction of heavy metals by eight plant species in the field. Water Air Soil Pollut 184:234–242
Acknowledgments
Authors are thankful to the Director of IHBT, Palampur, for providing necessary facilities. Thanks are also due to DAE-BRNS Mumbai, India, for financial assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Elena Maestri
Rights and permissions
About this article
Cite this article
Sharma, S., Singh, B. & Manchanda, V.K. Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environ Sci Pollut Res 22, 946–962 (2015). https://doi.org/10.1007/s11356-014-3635-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-014-3635-8