Abstract
Due to their immutable nature, metals are a group of pollutants of much concern. As a result of human activities such as mining and smelting of metalliferous ores, electroplating, gas exhaust, energy and fuel production, fertilizer and pesticide application, etc., metal pollution has become one of the most serious environmental problems today. Phytoremediation, an emerging cost-effective, non-intrusive, and aesthetically pleasing technology, that uses the remarkable ability of plants to concentrate elements and compounds from the environment and to metabolize various molecules in their tissues, appears very promising for the removal of pollutants from the environment. Within this field of phytoremediation, the utilization of plants to transport and concentrate metals from the soil into the harvestable parts of roots and above-ground shoots, i.e., phytoextraction, may be, at present, approaching commercialization. Improvement of the capacity of plants to tolerate and accumulate metals by genetic engineering should open up new possibilities for phytoremediation. The lack of understanding pertaining to metal uptake and translocation mechanisms, enhancement amendments, and external effects of phytoremediation is hindering its full scale application. Due to its great potential as a viable alternative to traditional contaminated land remediation methods, phytoremediation is currently an exciting area of active research.
Similar content being viewed by others
References
Ager FJ, Ynsa MD, Domínguez-Solís JR, Gotor C, Respaldiza MA & Romero LC (2002) Cadmium localization and quanti cation in the plant A. thaliana using micro-PIXE. Nuclear Instr. Methods in Phy. Res. Section B. Beam Interactions with Mat. and Atoms 189: 494–498
Alkorta I & Garbisu C (2001) Phytoremediation of organic contaminants. Bioresource Technol. 79: 273–276
Arazi T, Sunkar R, Kaplan B & Fromm H (1999) A tobacco plasma membrane calmodulin-binding transporter confers Ni2+ tolerance and Pb2+ hypersensitivity in transgenic plants. Plant J. 20: 171–182
Assunçço AGL, Martins PD, De Folter S, Vooijs R, Schat H & Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 24: 217–226
Baghour M, Moreno DA, Hernçndez J, Castilla N & Romero L (2001) Influence of root temperature on phytoaccumulation of As, Ag, Cr, and Sb in potato plants (Solanum tuberosum L. var. Spunta). J. Environ. Sci. Health Part A Tox. Hazard Subst. Environ. Eng. 36: 1389–1401
Baker AJM (1981) Accumulators and excluders-Strategies in the response of plants toheavy metals. J. Plant Nutr. 3: 643–654
Baker AJM & Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1: 81–126
Baker AJM & Whiting SN (2002) In search of the Holy Grail-a further step in understanding metal hyperaccumu-lation? New Phytol. 155: 1–7
Baker AJM, McGrath SP, Reeves RD & Smith JAC (2000) Metal hyperaccumulator plants: A review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G & Vangronsveld J (Eds), Phytoremediation of contaminated soil and water (pp 85–107). Lewis Publisher, Boca Raton, FL, USA
Baker AJM, McGrath SP, Sidoli CMD & Reeves RD (1994a) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resour. Conser. Recycl. 11: 41–49
Baker AJM, Reeves RD & Hajar ASM (1994b) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol. 127: 61–68
Bennet LE, Burkhead JL, Hale KL, Terry N, Pilon M & Pilon-Smits EA (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal-contaminated mine tailings. J. Environ. Qual. 32: 432–440
Bert V, Macnair MR, de Laguerie P, Saumitou-Laprade P & Petit D (2000) Zinc tolerance and accumulation in metallic-olous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol. 146: 225–233
Bizily SP, Kim T, Kandasamy MK & Meagher RB (2003) Subcellular targeting of methylmercury lyase enhances its speci c activity for organic mercury detoxi cation in plants. Plant Physiol. 131: 463–471
Bolan NS, Adriano DC, Mani PA & Duraisamy A (2003a) Immobilization and phytoavailability of cadmium in variable charge soils. II. E. ect of lime addition. Plant Soil 251: 187–198
Bolan NS, Adriano DC & Naidu R (2003b) Role of phosphorus in (im) mobilization and bioavailability of heavy metals in the soil-plant system. Rev. Environ. Contam. Toxicol. 177: 1–44
Boominathan R & Doran PM (2003a) Organic acid complexation, heavy metal distribution and the e. ects of ATPase inhibition in hairy roots of hyperaccumulator plant species. J. Biotechnol. 101: 131–146
Boominathan R & Doran PM (2003b) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyper-accumulator, Thlaspi caerulescens. Biotechnol. Bioengineer. 20: 158–167
Boyajian GE & Carreira LH (1997) Phytoremediation: a clean transition from laboratory to marketplace. Nat. Biotechnol. 15: 127–128
Brennan MA & Shelley ML (1999) A model of the uptake, translocation, and accumulation of lead (Pb) by maize for the purpose of phytoextraction. Ecol. Engineer. 12: 271–297
Brewer EP, Saunders JA, Angle JS, Chaney RL & McIntosh MS (1999) Somatic hybridization between the zinc accumu-lator Thlaspi caer ulescens and Brassica napous. Theore. Appl. Gen. 9: 761–771
Briat JF & Lebrun M (1999) Plant responses to metal toxicity. Comptes Rendus de l'Académie des Sciences-Series III-Sciences de la Vie 322: 43–54
Brooks RR (1988) (Ed) Plants that Hyperaccumulate Heavy Metals. CAB International, Oxon, UK, 356 pp
Brooks RR, Lee J, Reeves RD & Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium species of indicator plants. J. Geochem. Explor. 7: 49–57
Brown SL, Chaney RL, Angle JS & Baker AJ (1995) Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci. Soc. Am. J. 59: 125–133
Chaney RL, Li YM, Brown SL, Homer FA, Malik M, Angle JS, Baker AJM, Reeves RD & Chin M (2000) Improving metal hyperaccumulator wild plant to commercial phytoex-traction systems: Approaches and progress. In: Terry N, Bañuelos G & Vangronsveld J (Eds), Phytoremediation of contaminated soil and water (pp 129–158). Lewis Publisher, Boca Raton, FL, USA
Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS & Baker AJ (1997) Phytoremediation of metals. Curr. Opin. Biotechnol. 8: 279–284
Chaudhry TM, Hayes WJ, Khan AG & Khoo CS (1998) Phytoremediation-Focusing on accumulator plants that remediate metal-contaminated soils. Australasian J. Ecotoxicol. 4: 37–51
Chen B, Christie P & Li X (2001) A modi ed glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42: 185–192
Chen HM, Zheng CR, Tu C & Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41: 229–234
Chen YX, He YF, Yang Y, Yu YL, Zheng SJ, Tian GM, Luo YM & Wong MH (2003) Effect of cadmium on nodulation and N2-xation of soybean in contaminated soils. Chemosphere 50: 781–787
Clemens S (2001) Developing tools for phytoremediation: towards a molecular understanding of plant metal tolerance and accumulation. Int. J. Occup. Med. Environ. Health 14: 235–239
Clemens S, Palmgren MG & Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci. 7: 309–315
Cobbett C, May MJ, Howden R & Rolls B (1998) The glutathione-de cient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is de cient in c glutamilcysteine synthetase. Plant J. 16: 73–78
Cobbett C & Goldsbrough P (2002) Phytochelatins and metallothioneins: Roles in heavy metal detoxi cation and homeostasis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 53: 159–182
Collins YE & Stotzky G (1989) Factors a. ecting the toxicity of heavy metals to microbes. In: Beveridge TJ & Doyle RJ (Eds), Metal Ions and Bacteria (pp 31–90). Wiley, Toronto, Canada
Cunningham SD & Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol. 110: 715–719
Dahmani-Muller H, van Oort F, Gélie B & Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ. Pollut. 109: 231–238
Dahmani-Muller H, van Oort F & Balabane M (2001) Metal extraction by Arabidopsis halleri grown on an unpolluted soil amended with various metal-bearing solids: a pot experiment. Environ. Pollut. 114: 77–84
De Knecht JA, van Dillen M, Koevoets PLM, Schat H, Verkleij JAC & Ernst WHO (1994) Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris. Plant Physiol. 104: 255–261
Delhaize E. A (1996) A metal-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 111: 849–855
Delorme TA, Gagliardi JV, Angle JS & Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J. & C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can. J. Microbiol. 47: 773–776
Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Seneco. JF, Sashti NA & Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arse-nate reductase and c glutamylcysteine synthetase expression. Nat. Biotechnol. 20: 1140–1145
Diels N, van der Lelie D & Bastiaens L (2002) New developments in treatment of heavy metal contaminated soils. Re/Views in Environ. Sci. & Bio/Technol. 1: 75–82
Doucleff M & Terry N (2002) Pumping out the arsenic. Nat. Biotechnol. 20: 1094–1095
Dushenkov S, Skarzhinskaya M, Glimelius K, Gleba D & Raskin I (2002) Bioengineering of a phytoremediation plant by means of somatic hybridization. Int. J. Phytoremediation 4: 117–126
Ebbs S, Lau I, Ahner B & Kochian L (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214: 635–640
Elmayan T & Tepfer M (1994) Synthesis of a bifunctional metallothionein/b-glucuronidase fusion protein in transgenic tobacco plants as a means of reducing leaf cadmium levels. Plant J. 6: 433–440
Entry JA, Rygiewicz PT, Watrud LS & Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv. Environ. Res. 7: 123–138
Evans KM, Gatehouse JA, Lindsay WP, Shi J, Tommey AM & Robinson NJ (1992) Expression of the pea metallothionein-like gene PsMTA in Escherichia coli and Arabidopsis thaliana and analysis of trace metal ion accumulation: Implications for PsMTA function. Plant Mol. Biol. 20: 1019–1028
Evans LD (2002) The dirt on phytoremediation. J. Soil & Water Conservation 57: 12A–15A
Francesconi K, Visoottiviseth P, Sridokchan W & Goessler W (2002) Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci. Total Environ. 284: 27–35
Gabbrielli R, Pandolfini T, Vergnano O & Palandri MR (1990) Comparison of two serpentine species with different nickel tolerance strategies. Plant Soil. 122: 271–277
Garbisu C & Alkorta I (1997) Bioremediation: principles and future. J. Clean Technol. Environ. Toxic. & Occup. Med. 6: 351–366
Garbisu C & Alkorta I (2001) Phytoextraction: a cost-e. ective plant-based technology for the removal of metals from the environment. Bioresource Technol. 77: 229–236
Garbisu C & Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Eur. J. Min. Proc. & Environ. Protect. 3: 58–66
Garbisu C, Hernández-Allica J, Barrutia O, Alkorta I & Becerril JM (2002) Phytoremediation: A technology using green plants to remove contaminants from polluted areas. Rev. Environ. Health 17: 75–90
Gisbert C, Ros R, de Haro A, Walker DJ, Bernal MP, Serrano R & Navarro-Avino J (2003) A plant genetically modi ed that accumulates Pb is especially promising for phytoremediation. Biochem. Biophys. Res. Commun. 303: 440–445
Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Skarzhinskaya M, Dushenkov S, Logendra S, Gleba YY & Raskin I (1999) Use of plant roots for phytoremediation and molecular farming. Proc. Natl. Acad. Sci. USA 96: 5973–5977
Gong JM, Lee DA & Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. 2003 Proc. Natl. Acad. Sci. USA 100: 10118–10123
Grichko VP, Filby B & Glick BR (2000) Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb, and Zn. J. Biotechnol. 81: 45–53
Guerinot ML (2000) The ZIP family of metal transporters. Biochim. Biophys. Acta (BBA)-Biomembranes 1465: 190–198
Hasegawa I, Terada E, Sunairi M, Wakita H, Shinmachi F & Noguchi A (1997) Genetic improvement of heavy metal tolerance in plants by transfer of the yeast metallothionein gene (CUP1). Plant Soil 196: 277–281
Hattori J, Labbe H & Miki BL (1994) Construction and expression of a metallothionein-beta-glucuronidase gene fusion. Genome 37: 508–512
Heaton ACP, Rugh CL, Wang N & Meagher RB (1998) Phytoremediation of mercury-and methylmercury-polluted soils using genetically engineered plants. J. Soil Contam. 7: 497–509
Hill KA, Lion LW & Ahner BA (2002) Reduced Cd accumu-lation in Zea mays: a protective role for phytosiderophores? Environ. Sci. Technol. 36: 5363–5368
Hirschi KD, Korenkov VD, Wilganowski NL & Wagner GJ (2000) Expression of Arabidopsis CAX2in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol. 124: 125–133
Homer FA, Morrison RS, Brooks RR, Clement J & Reeves RD (1991) Comparative studies of nickel, cobalt, and copper uptake by some nickel hyperaccumulators of the genus Alyssum. Plant Soil. 138: 195–205
Iannelli MA, Pietrini F, Fiore L, Petrilli L & Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol. Biochem. 40: 977–982
Jauert P, Schumacher TE, Boe A & Reese RN (2002) Rhizosphere acidification and cadmium uptake by strawberry clover. J. Environ. Qual. 31: 627–633
Kamnev AA & van der Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Biosci. Rep. 20: 239–258
Kärenlampi S, Schat H, Vangronsveld J, Verkleij JAC, van der Lelie D, Mergeay M & Tervahauta AI (2000) Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ. Pollut. 107: 225–231
Koppolu L & Clements LD (2003) Pyrolysis as a technique for separating heavy metals from hyperaccumulators. Part I: Preparation of synthetic hyperaccumulator biomass. Biomass & Bioenergy 24: 69–79
Krämer U & Chardonnens AN (2001) The use of transgenic plants in the bioremediation of soils contaminated with trace elements. Appl. Microbiol. Biotechnol. 55: 661–672
Krämer U (2000) Cadmium for all meals-plants with an unusual appetite. New Phytol. 145: 1–5
Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM & Smith JAC (1996) Free histidine as a metal chelator in plants that hyperaccumulate nickel. Nature 379: 635–638
Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, McIntyre L, Schroeder JI & Salt DE (2003) Genomic scale pro ling of nutrient and trace elements in Arabidopsis thaliana. Nat. Biotechnol. 21: 1215–1221
Lasat MM, Baker AJM & Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanism involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol. 118: 875–883
Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J. Environ. Qual. 31: 109–120
Lehoczky E, Marth P, Szabados I, Palkovics M & Lukács P (2000) Influence of soil factors on the accumulation of cadmium by lettuce. Commun. Soil Sci. Plant Anal. 31: 2425–2431
Lehoczky E, SzabóL & Horváth S (1998) Cadmium uptake by plants in different soils. Commun. Soil Sci. Plant Anal. 29: 1903–1912
Linger P, Müssig J, Fischer H & Kobert J (2002) Industrial hemp (Cannabis sativa L. ) growing on heavy metal contam-inated soil: bre quality and phytoremediation potential. Industr. Crops Protect. 16: 33–42
Liu D, Jiang W, Liu C, Xin C & Hou W (2000) Uptake and accumulation of lead by roots, hypocotyls and shoots of Indian mustard (Brassica juncea L. ). Bioresource Technol. 71: 273–277
Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ & McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol. 128: 1359–1367
Lombi E, Zhao FJ, Dunham SJ & McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi geosingense. New Phytol. 145: 11–20
Long XX, Yang XE, Ye ZQ, Ni WZ & Shi WY (2002) Differences of uptake and accumulation of zinc in four species of Sedum. Acta Botanica Sinica 44: 152–157
Luo YM, Christie P & Baker AJM (2000) Soil solution Zn and pH dynamics in non-rhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cd-contaminated soil. Chemosphere 41: 161–164
Ma LQ, Komar KM, Tu C, Zhang W, Cai Y & Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409: 579
Ma M, Lau PS, Jia YT, Tsang WK, Lam SKS, Tam NFY & Wong YS (2003) The isolation and characterization of Type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra cv. Merlin. Plant Sci. 164: 51–60
Macnair MR (2002) Within-and between-population genetic variation for Zn accumulation in Arabidopsis halleri. New Phytol. 155: 59–66
Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P & Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc. Royal Soc. London B 266: 2175–2179
Madejon P, Murillo JM, Maranon T, Cabrera F & Soriano MA (2003) Trace element and nutrient accumulation in sun. ower plants two years after the Aznalcollar mine spill. Sci. Total Environ. 20: 239–257
Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA & Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126: 1646–1667
McGrath SP, Shen ZG & Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188: 153–159
McGrath SP, Lombi E & Zhao FJ (2001) What's new about cadmium hyperaccumulation? New Phytol. 149: 2–3
McGrath SP, Zhao FJ & Lombi E (2002) Phytoremediation of metals, metalloids, and radionuclides. Adv. Agronomy 75: 1–56
McGrath SP & Zhao FJ (2003) Phytoextraction of metals and metalloids. Curr. Opin. Biotechnol. 14: 277–282
McIntyre T (2003) Phytoremediation of heavy metals from soils. Adv. Biochem. Eng. Biotechnol. 78: 97–123
Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr. Opin. Plant Biol. 3: 153–162
Mejare M & Bulow L (2001) Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol. 19: 67–73
Mengoni A, Gonnelli C, Galardi F, Gabbrielli R & Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random ampli ed polymorphic DNA analysis. Mol. Ecol. 9: 1319–1324
Misra S & Gedamu L (1989) Heavy metal tolerance transgenic Brassica napus L. and Nicotiana tabacum L. plants. Theor. Appl. Gen. 78: 161–168
Morgan AJ, Evans M, Winters C, Gane M & Davies MS (2002) Assaying the e. ects of chemical ameliorants with earthworms and plants exposed to a heavily polluted metalliferous soil. Eur. J. Soil Biol. 38: 323–327
Navari-Izzo F & Quartacci MF (2001) Phytoremediation of metals. Tolerance mechanisms against oxidative stress. Minerva Biotec. 13: 73–83
Nedelkoska TV & Doran PM (2000) Hyperaccumulation of cadmium by hairy roots of Thlaspi caerulescens. Biotechnol. Bioeng. 67: 607–615
O'Connor CS, Leppi NW, Edwards R & Sunderland G (2003) The combined use of electrokinetic remediation and phyto-remediation to decontaminate metal-polluted soils: a labora-tory-scale feasibility study. Environ. Monit. Assess. 84: 141–158
Oremland RS & Stolz JF (2003) The ecology of arsenic. Science 300: 939–944
Pawlowska TE, Chaney RL, Chin M& Charvat I (2000) Effects of metal phytoextraction practices on the indigenous com-munity of arbuscular mycorrhizal fungi at a metal-contam-inated land ll. Appl. Environ. Microbiol. 66: 2526–2530
Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D & Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperac-cumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 25: 4956–4960
Peralta-Videa JR, Gardea-Torresdey JL, Gómez E, Tiemann KJ, Parsons JG & Carrillo G (2002) Effect of mixed cadmium, copper, nickel and zinc at di. erent pHs upon alfalfa growth and heavy metal uptake. Environ. Pollut. 119: 291–301
Pichtel J, Kuroiwa K & Sawyerr HT (2000) Distribution of Pb, Cd and Ba in soils and plants of two contaminated soils. Environ. Pollut. 110: 171–178
Pickering IJ, Prince RC, George GN, Rauser WE, Wickrama-singhe WA, Watson AA, Dameron CT, Dance IG, Fairlie DP & Salt DE (1999) X-ray absorption spectroscopy of cadmium phytochelatin and model systems. Biochim. Biophys. Acta-Prot. Struct. Mol. Enzymol. 1429: 351–364
Pickering IJ, Prince RC, George GN, Smith RD, George GN & Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 122: 1171–1177
Pilon-Smits E & Pilon M (2000) Breeding mercury-breathing plants for environmental cleanup. Trends Plant Sci. 5: 235–236
Pineros MA, Shaff JE & Kochian LV (1998) Development, characterization, and application of a cadmium-selective microelectrode for the measurement of cadmium fluxes in roots of Thlaspi species and wheat. Plant Physiol. 116: 1393–1401
Pulford ID & Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees-a review. Environ. Int. 29: 529–540
Raskin I (1996) Plant genetic engineering may help with environmental cleanup (commentary). Proc. Natl. Acad. Sci. USA 93: 3164–3166
Raskin I, Smith RD & Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr. Opin. Biotechnol. 8: 221–226
Rea PA (2003) Ion genomics. Nat. Biotechnol. 21: 1149–1151
Rengel Z (2000) Ecotypes of Holcus lanatus tolerant to zinc toxicity also tolerate zinc deficiency. Ann. Bot. 86: 1119–1126
Robinson B, Russell C, Hedley M & Clothier B (2001) Cadmium uptake by rhizobacteria: implications for New Zealand pastureland. Agri., Eco. & Environ. 87: 315–321
Rout GR, Samantaray S & Das P (1999) In vitro selection and biochemical characterisation of zinc and manganese adapted callus lines in Brassica spp. Plant Sci. 146: 89–100
Rubinelli P, Siripornadulsil S, Gao-Rubinelli F & Sayre RT (2002) Cadmium-and iron-stress-inducible gene expression in the green alga Chlamydomonas reinhardtii: evidence for H43 protein function in iron assimilation. Planta 215: 1–13
Rugh CL, Gragson GM, Meagher RB & Merkle SA (1998a) Toxic mercury reduction and remediation using transgenic plants with a modi ed bacterial gene. Hort. Science 33: 618–621
Rugh CL, Senecoff JF, Meagher RB & Merkle SA (1998b) Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotechnol. 16: 925–928
Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO & Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modi ed bacterial merA gene. Proc. Natl. Acad. Sci. USA 93: 3182–3187
Sahi SV, Bryant NL, Sharma NC & Singh SR (2002) Characterization of a lead hyperaccumulator shrub, Sesbania drummondii. Environ. Sci. Technol. 36: 4676–4680
Salt DE, Blaylock M, Kumar PBAN, Dushenkov V, Ensley BD, Chet I & Raskin I (1995a) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnol. 13: 468–475
Salt DE, Prince RC, Pickering IJ & Raskin I (1995b) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 109: 1427–1433
Salt DE, Prince RC, Baker AJM, Raskin I & Pickering IJ (1999) Zinc ligand in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectros-copy. Environ. Sci. Technol. 33: 713–717
Salt DE, Prince RC & Pickering IJ (2002) Chemical speciation of accumulated metals in plants: evidence from X-ray absorption spectroscopy. Microchemical J. 71: 255–259
Salt DE, Smith RD & Raskin I (1998) Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 643–668
Sanitàdi Toppi L & Gabbrielli R (1999) Response to cadmium in higher plants. Environ. Experim. Bot. 41: 105–130
Sauge-Merle S, Cuine S, Carrier P, Lecomte-Pradines C, Luu DT & Peltier G (2003) Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Appl. Environ. Microbiol. 69: 490–494
Schat H, Llugany M, Vooijs R, Hartley-Whitaker J & Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J. Exp. Bot. 53: 1–12
Schneider T, Haag-Kerwer A, Maetz M, Niecke M, Povh B, Rausch T & Schübler A (1999) Micro-PIXE studies of elemental distribution in Cd-accumulating Brassica juncea L. Nuclear Instr. Methods Phys. Res. Section B: Interaction with Materials and Atoms 158: 329–334
Schutzendubel A & Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53: 1351–1365
Schwartz C, Morel JL, Saumier S, Whiting SN & Baker AJM (1999) Root development of the zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208: 103–115
Shanks JV & Morgan J (1999) Plant 'hairy root' culture. Curr. Opin. Biotechnol. 10: 151–155
Shann JR (1995) The role of plants and plant/microbial systems in the reduction of exposure. Environ. Health Perspect. 103: 13–15
Shen ZG, Zhao FJ & McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ. 20: 898–906
Singh OV, Labana S, Pandey G, Budhiraja R & Jain RK (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl. Microbiol. Biotechnol. 61: 405–412
Song W-Y, Sohn EJ, Martinoia E, Lee YJ, Yang Y-Y, Jasinski M, Forestier C, Hwang I & Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat. Biotechnol. 21: 914–919
Stomp AM, Han KH, Wilbert S, Gordon MP & Cunningham SD (1994) Genetic strategies for enhancing phytoremediation. Ann. NY Acad. Sci. 721: 481–491
Thomas JC, Davies EC, Malick FK, Endreszl C, Williams CR, Abbas M, Petrella S, Swisher K, Perron M, Edwards R, Ostenkowski P, Urbanczyk N, Wiesend WN & Murray KS (2003) Yeast metallothionein in transgenic tobacco promotes copper uptake from contaminated soils. Biotechnol. Prog. 19: 273–280
Tu C, Ma LQ & Bondada B (2002) Arsenic accumulation in the hyperaccumulator Chinese brake and its utilization potential for phytoremediation. J. Environ. Qual. 31: 1671–1675
United States Environmental Protection Agency (1992) Selection of control technologies for remediation of lead battery recycling sites. EPA/540/S-92/011. US Environmental Protection Agency, Office of Emergency and Remedial Response, Washington, DC, USA
United States Environmental Protection Agency (2000a) Electrokinetic and phytoremediation in situ treatment of metal-contaminated soil: state-of-the-practice. EPA/542. US Environmental Protection Agency, Office of Solid Waste and Emergency Response Technology Innovation Office, Washington, DC, USA
United States Environmental Protection Agency (2000b) Introduction to phytoremediation EPA/600/R-99/107. US Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, USA
Vatamaniuk OK, Bucher EA, Ward JT & Rea PA (2002) Worms take the 'phyto' out of 'phytochelatins'. Trends Biotechnol. 20: 61–64
Visoottiviseth P, Francesconi K & Sridokchan W (2002) The potential of Thai indigenous plant species for the phytoreme-diation of arsenic contaminated land. Environ. Pollut. 118: 453–461
Wang QR, Cui YS, Liu XM, Dong YT & Christie P (2003) Soil contamination and plant uptake of heavy metals at polluted sites in China. J. Environ. Sci. Health Part A Tox. Hazard Subst. Environ. Eng. 38: 823–838
Wang QR, Liu XM, Cui YS, Dong YT & Christie P (2002a) Responses of legumes and non-legume crop species to heavy metals in soils with multiple metal contamination. J. Environ. Sci. Health Part A Tox. Hazard Subst. Environ. Eng. 37: 611–621
Wang Z, Shan X & Zhang S (2002b) Comparison between fractionation and bioavailability of trace elements in rhizo-sphere and bulk soils. Chemosphere 46: 1163–1171
Weber O, Scholz RW, Bühlmann R & Grasmück D (2001) Risk perception of heavy metal soil contamination and attitudes toward decontamination strategies. Risk Analysis 21: 967–977
Wenzel WW, Adriano DC, Salt D & Smith R (1999) Phytoremediation: A plant-microbe-based remediation system. In: SSSA (Ed), Bioremediation of Contaminated Soils (pp 457–508) Agronomy Monograph no. 37, SSSA, Madison, WI, USA
Whiting SN, Leake JR, McGrath SP & Baker AJM (2000) Positive response to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol. 145: 199–210
Williams LE, Pittman JK & Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta (BBA)-Biomembranes 1465: 104–126
Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50: 775–780
Zhang W, Cai Y, Tu C & Ma LQ (2002) Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci. Total Environ. 300: 167–177
Zhao FJ, Lombi E, Breedon T & McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ. 23: 507–514
Zhao FJ, Hamon RE & McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol. 151: 613–620
Zhu YL, Pilon-Smits EA, Jouanin L & Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119: 73–80
Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L & Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma-glutamylcysteine synthetase. Plant Physiol. 121: 1169–1178
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Alkorta, I., Hernández-Allica, J., Becerril, J. et al. Recent Findings on the Phytoremediation of Soils Contaminated with Environmentally Toxic Heavy Metals and Metalloids Such as Zinc, Cadmium, Lead, and Arsenic. Re/Views in Environmental Science and Bio/Technology 3, 71–90 (2004). https://doi.org/10.1023/B:RESB.0000040059.70899.3d
Issue Date:
DOI: https://doi.org/10.1023/B:RESB.0000040059.70899.3d