Chelate-Enhanced Phytoremediation of Soils Polluted with Heavy Metals

  • I. Alkorta
  • J. Hernández-Allica
  • J.M. Becerril
  • I. Amezaga
  • I. Albizu
  • M. Onaindia
  • C. Garbisu


In general, hyperaccumulators are low biomass, slow-growing plants. High biomass non-hyperaccumulator plants by themselves are not a valid alternative for phytoextraction as they also have many limitations, such as small root uptake and little root-to-shoot translocation. In this context, chemically-induced phytoextraction (based on the fact that the application of certain chemicals, mostly chelating agents, to the soil significantly enhances metal accumulation by plants) has been proposed as an alternative for the cleaning up of metal polluted soils. But chelate-induced phytoextraction increases the risk of adverse environmental effects due to metal mobilization during extended periods of time. In order to minimize the phytotoxicity and environmental problems associated with the use of chelating agents, nowadays, research is being carried out on the gradual application of small doses of the chelating agent during the growth period. However, EDTA utilization in the future will most likely be limited to ex situconditions where control of the leachates can be achieved. There are other mobilizing agents which are much less harmful to the environment such as citric acid, NTA, and particularly EDDS. Research should also be aimed towards more innovative agronomic practices. Environmentally safe methods of chelate-induced phytoextraction must be developed before steps towards further development and commercialization of this remediation technology are taken. Most importantly, more applied projects in this field are needed to clarify the real potential and risks of this technology.

assisted phytoremediation bioavailability chelating agents enhanced phytoremediation ethylenediaminetetraacetic acid (EDTA) induced phytoremediation phytoextraction 


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  1. Albasel N & Cottenie A (1985) Heavy metals uptake from contaminated soils as affected by peat, lime and chelates. Soil Sci. Soc. Am. J. 49: 386–390Google Scholar
  2. Athalye VV, Ramachandran V & D'Souza TJ (1995) Infuence of chelating agents on plant uptake of 51Cr, 210 Pb and 210 Po. Environ. Pollut. 89: 47–53Google Scholar
  3. Baker AJM & Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1: 81–126Google Scholar
  4. Baker AJM, McGrath SP, Reeves RD & Smith JAC (2000) Metal hyperaccumulator plants:a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In:Terry N & Bañuelos G (Eds) Phytoremediation of Contaminated Soil and Water (pp. 85–107)Lewis Publ., Boca Raton, Florida, USAGoogle Scholar
  5. Baker AJM & Whiting SN (2002) In search of the Holy Grail-a further step in understanding metal hyperaccumulation? New Phytol. 155: 1–7Google Scholar
  6. Barocsi A, Csintalan Z, Kocsanyi L, Dushenkov S, Kuperberg JM, Kucharski R & Richter PI (2003) Optimizing phytoremediation of heavy metal-contaminated soil by exploiting plants' stress adaptation. Int. J. Phytoremediation 5: 13–23Google Scholar
  7. Barona A, Aranguiz I & Elias A (2001) Metal associations in soils before and after EDTA extractive decontamination: implications for the e. ectiveness of further clean-up proce-dures. Environ. Pollut. 113: 79–85Google Scholar
  8. Becerril JM, Barrutia O, Hernández-Allica J, García-Plazaola JI, Hernández A & Garbisu C (2002) Fitorremediacióny biorremediación:nuevas tecnologías biológicas para la eliminación de los contaminantes del suelo. In:F Valladares (Ed) Segundas Jornadas Cientícas sobre Medio Ambiente del CCMA-CSIC (pp145–152)Ciencia y Medio Ambiente-CCMA-CSIC, Madrid, SpainGoogle Scholar
  9. Berti WR & Cunningham SD (1997) In-place inactivation of Pb in Pb contaminated soils. Environ. Sci. Technol. 31: 1359–1364Google Scholar
  10. Blaylock MJ (2000) Field demonstrations of phytoremediation of lead contaminated soils. In:Terry N & Bañuelos G (Eds) Phytoremediation of Contaminated Soil and Water (pp. 1–12)Lewis Publ., Boca Raton, Florida, USAGoogle Scholar
  11. Blaylock MJ & Huang JW (1999) Phytoextraction of metals. In: Raskin I & Ensley BD (Eds) Phytoremediation of toxic metals:using plants to clean up the environment (pp 53–70)John Wiley, New York, NY, USAGoogle Scholar
  12. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O & Gussman C (1997) Enhanced accumulation of Pb in Indian mustard by soil applied chelating agents. Environ. Sci. Technol. 31: 860–865Google Scholar
  13. Bolton H, Girvin CC Jr, Plymale AE, Harvey SD & Workman DJ (1996) Degradation of metal-nitriloacetate complexes by Chelatobacter heintzii. Environ. Sci. Technol. 30: 931–938Google Scholar
  14. Briat JF & Lebrun M (1999) Plant responses to metal toxicity. Comptes Rendus de l'Académie des Sciences-Series III-Sciences de la Vie. 322: 43–54Google Scholar
  15. Brown SL, Chaney RL, Angle JS & Baker AM (1995) Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens and metal tolerant Silene vulgaris grown on sludge-amended soils. Environ. Sci. Technol. 29: 1581–1585Google Scholar
  16. Bundt M, Albrecht A, Froidevaux P, Blaser P & Flubler H (2000) Impact of preferential. ow on radionuclide distribution in soil. Environ. Sci. Technol. 34: 3895–3899Google Scholar
  17. Chaney RL, Brown JC & Tiffin LO (1972) Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol. 50: 208–213Google Scholar
  18. 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, USAGoogle Scholar
  19. Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS & Baker AJ (1997) Phytoremediation of metals. Curr. Opin. Biotechnol. 8: 279–284Google Scholar
  20. Chaney RL & Ryan JA (1994) Risk Based Standards for Arsenic, Lead and Cadmium in Urban Soils (pp 1–130)DECHEMA, Frankfurt, GermanyGoogle Scholar
  21. Chen H & Cutright T (2001) EDTA and HEDTA e. ects on Cd, Cr, and Ni uptake by Helianthus annuus. Chemosphere 45: 21–28Google Scholar
  22. Chen YX, Lin Q, Luo YM, He YF, Zhen SJ, Yu YL, Tian GM & Wong MH (2003) The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemosphere 50: 807–811Google Scholar
  23. 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, CanadaGoogle Scholar
  24. Cooper EM, Sims JT, Cunningham SD, Huang JW & Berti WR (1999) Chelate-assisted phytoextraction of lead from contaminated soils. J. Environ. Qual. 28: 1709–1719Google Scholar
  25. Crowley DE, Wang YC, Reid CPP & Szaniszlo PJ (1991) Mechanisms of iron acquisition from siderophores by microorganisms and plants. Plant Soil 130: 179–198Google Scholar
  26. Cunningham SD, Berti WR & Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol. 13: 393–397Google Scholar
  27. Cunningham SD & Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol. 110: 715–719Google Scholar
  28. Deram A, Petit D, Robinson B, Brooks RR, Greg P & Van Halluwyn C (2000) Natural and induced heavy metal accumulation by Arrhenatherum elatius:implications for phytoremediation. Commun. Soil Sci. Plant Anal. 31: 413–421Google Scholar
  29. Dijkshoorn W, Lampe JEM & van Broekhoven LW (1983) The effect of soil pH and chemical form of nitrogen fertilizer on heavy metal contents in ryegrass. Fert. Res. 4: 63–74Google Scholar
  30. Ebbs SD & Kochian L (1998) Phytoextraction of zinc by oat (Avena sativa), barley (Hordeum vulgare) and Indian mustard (Brassica juncea). Environ. Sci. Technol. 32: 802–806Google Scholar
  31. Elless MP & Blaylock MJ (2000) Amendment optimization to enhance lead extractability from contaminated soils for phytoremediation. Int. J. Phytol. 2: 75–89Google Scholar
  32. Elliot HA & Denneny CM (1982) Soil adsorption of Cd from solutions containing organic ligands. J. Environ. Qual. 11: 658–663Google Scholar
  33. Epstein AL, Gussman CD, Blaylock MJ, Yermiyahu U, Huang JW, Kapulnik Y & Orser CS (1999) EDTA and Pb-EDTA accumulation in Brassica juncea grown in Pb-amended soil. Plant Physiol. 208: 87–94Google Scholar
  34. ETCS (European Topic Centre Soil) (1998) Topic report-Contaminated sites. European Environment Agency, Copenhagen, DenmarkGoogle Scholar
  35. European Community (1986) On the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Council Directive 86/278/EEC. In: EC Official Journal L181. European Community, Brussels, Belgium, 4. 7. 1986Google Scholar
  36. Flathman PE & Lanza GR (1998) Phytoremediation:current views on an emerging green technology. J. Soil Contamin. 7: 415–432Google Scholar
  37. Garbisu C & Alkorta I (1997) Bioremediation:principles and future. J. Clean Technol. Environ. Toxicol. & Occup. Med. 6: 1–16Google Scholar
  38. Garbisu C & Alkorta I (2001) Phytoextraction:a cost-effective plant-based technology for the removal of metals from the environment. Bioresource Technol. 77: 229–236Google Scholar
  39. Garbisu C, Hernández-Allica J, Barrutia O, Alkorta I & Becerril JM (2002) Phytoremediation:A technology using green plants to remove contaminants from polluted areas. Reviews Environ. Health 17: 75–90Google Scholar
  40. Glass DJ (2000) Economic potential of phytoremediation. In: Raskin I & Ensley BD (Eds) Phytoremediation of Toxic Metals (pp. 15–31). John Wiley & Sons, New York, USAGoogle Scholar
  41. 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: 5973–5977Google Scholar
  42. Grčman H, Velikonja-Bolta Š, Vodnik D, Kos B & Leštan D (2001) EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant Soil 235: 105–114Google Scholar
  43. Grčman H, Vodnik D, Velikinja-Bolta Š & Leštan D (2003) Ethylenediaminedissucinate as a new chelate for environmentally safe enhanced lead phytoextraction. J. Environ. Qual. 32: 500–506Google Scholar
  44. Hammer D & Keller C (2002) Changes in the rhizosphere of metal-accumulating plants evidenced by chemical extractants. J. Environ. Qual. 31: 1561–1569Google Scholar
  45. Harter RD (1983) Effect of soil pH on adsorption of lead, copper, zinc and nickel. Soil Sci. Soc. Am. J. 47: 47–51Google Scholar
  46. Hong PKA, Li C, Banerji SK & Regmi T (1999) Extraction, recovery, and biostability of EDTA for remediation of heavy metal-contaminated soil. J. Soil Contam. 8: 81–103Google Scholar
  47. Huang JW, Chen J & Berti WR (1997) Phytoremediation of Pb-contaminated soils:role of synthetic chelates in lead phytoextraction. Environ. Sci. Technol. 31: 800–805Google Scholar
  48. Huang JW & Cunningham SD (1996) Lead phytoextraction: species variation in lead uptake and translocation. New Phytol. 134: 75–84Google Scholar
  49. Huang JW, Cunningham SD & Germani SJ (1996) Lead phytoextraction:species variation in lead uptake and translocation. New Phytol. 134: 75–84Google Scholar
  50. Jarvis MD & Leung DWM (2001) Chelated lead transport in Chamaecytisus proliferus (L. f. ) link ssp. proliferus var. palmensis (H. Christ):an ultrastructural study. Plant Science. 161: 433–441Google Scholar
  51. Jarvis MD & Leung DWM (2002) Chelated lead transport in Pinus radiata:an ultrastructural study. Environ. Experimental Bot. 48: 21–32Google Scholar
  52. Jaworska JS, Schowanek D & Feijtel TCJ (1999) Environmental risk assessment for trisodium [S, S']-ethylene diamine disuccinate, a biodegradable chelator used in detergent application. Chemosphere 38: 3597–3625Google Scholar
  53. Jiang XJ, Luo YM, Zhao QG, Baker AJM, Christie P & Wong MH (2003) Soil Cd availability to Indian mustard and environmental risk following EDTA addition to Cd-contaminated soil. Chemosphere 50: 813–818Google Scholar
  54. Jones PW & Williams DR (2001) Chemical speciation used to assess [S, S']-ethylenediaminedissuccinic acid (EDDS) as a readily-biodegradable replacement for EDTA in radiochemical decontamination formulations. Appl. Radiat. Isot. 54: 587–593Google Scholar
  55. Kambhampati MS, Begonia GB, Begonia MF & Bufford Y (2003) Phytoremediation of a lead-contaminated soil using morning glory (Ipomoea lacunosa L. ):effects of a synthetic chelate. Bull. Environ. Contam. Toxicol. 71: 379–386Google Scholar
  56. Kamnev AA & van der Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Bioscience Reports 20: 239–258Google Scholar
  57. Kari FG & Giger W (1996) Speciation and fate of ethylene-diaminetetraacetate (EDTA) in municipal wastewater treatment. Water Res. 30: 122–134Google Scholar
  58. Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK & Schulin R (2000) Enhancement of phytoextraction of Zn, Cd and Cu from calcareous soil:the use of NTA and sulfur amendments. Environ. Sci. Technol. 34: 1778–1783Google Scholar
  59. Khan AG, Kuek C, Chaudhry TM, Khoo CS & Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41: 197–207Google Scholar
  60. Kirkham MB (2000) EDTA-facilitated phytoremediation of soil with heavy metals from sewage sludge. Int. J. Phytol. 2: 159–172Google Scholar
  61. Kos B & Leštan D (2003a) Induced phytoextraction/soil washing of lead using biodegradable chelate and permeable barriers. Environ. Sci. Technol. 37: 624–629Google Scholar
  62. Kos B & Leštan D (2003b) Influence of a biodegradable ([S, S ]-EDDS) and nondegradable (EDTA) chelate and hydrogen modified soil water sorption capacity on Pb phytoextraction and leaching. Plant Soil. 253: 403–411Google Scholar
  63. Krämer U & Chardonnens AN (2001) The use of transgenic plants in the bioremediation of soils contaminated with trace elements. Appl. Microbiol. Biotechnol. 55: 661–672Google Scholar
  64. Kulli B, Balmer M, Krebs R, Lothenbach B, Geiger G & Schulin R (1999) The in. uence of nitrilotriacetate on heavy metal uptake of lettuce and ryegrass. J. Environ. Qual. 28: 1699–1705Google Scholar
  65. Lasat MM (2002) Phytoextraction of toxic metals:a review of biological mechanisms. J. Environ. Qual. 31: 109–120Google Scholar
  66. Lombi E, Zhao FJ, Dunham SJ & McGrath SP (2001) Phytoremediation of heavy-metal contaminated soils: natural hyperaccumulation versus chemically enhanced phytoextraction. J. Environ. Qual. 30: 1919–1926Google Scholar
  67. Luo YM, Wu LH, Jiang XJ, Wu SC & Christie P (2000) Chelate enhanced phytoextraction of metal contaminated soils and environmental risk. In: Proceedings of Soil Rem 2000, International Conference of Soil Remediation (pp 166–168). Hangzhou, China, October 15-19Google Scholar
  68. Madrid F, Liphadzi MS & Kirkham MB (2003) Heavy metal displacement in chelate-irrigated soil during phytoremediation. J. Hydrology 272: 107–119Google Scholar
  69. Maier RM, Neilson JW, Artiola JF, Jordan FL, Glenn EP & Descher SM (2001) Remediation of metal-contaminated soil and sludge using biosurfactant technology. Int. J. Occup. Med. Environ. Health 14: 241–248Google Scholar
  70. Marschner H (1995) Mineral Nutrition of Higher Plants. 2nd edn. Academic Press, London, UKGoogle Scholar
  71. McBride MB (1994) Environmental Chemistry of Soils. Oxford University Press, New York, USAGoogle Scholar
  72. McGrath SP (1987) Long-term studies of metal transfers following applications of sewage sludge. In: Coughtrey PJ, Martin MH & Unsworth MH (Eds) Pollutant Transport and Fate in Ecosystems. Special Publication No. 6 of the British Ecological Society (pp 301–317). Blackwell Scientific, Oxford, UKGoogle Scholar
  73. McGrath SP (1998) Phytoextraction for soil remediation. In: RR Brooks (Ed) Plants that Hyperaccumulate Heavy Metals (pp. 261–288). CAB International, Oxon, UKGoogle Scholar
  74. McGrath SP, Zhao FJ & Lombi E (2002) Phytoremediation of metals, metalloids, and radionuclides. Adv. Agronomy. 75: 1–56Google Scholar
  75. McGrath SP & Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr. Opin. Biotechnol. 14: 277–282Google Scholar
  76. Means JL & Crerar DA (1978) Migration of radioactive wastes: radionuclide mobilization by complexing agents. Science 200: 1477–1481Google Scholar
  77. Miller RR (1996) Phytoremediations. Ground-Water Remediation Technologies Analysis Center (GWRTAC)-Technology Overview Report TO-96-03, GWRTAC-O-SeriesGoogle Scholar
  78. Mulligan CN, Yong RN & Gibbs BF (2001) Remediation technologies for metal-contaminated soil and groundwater: an evaluation. Eng. Geol. 60: 193–207Google Scholar
  79. Navari-Izzo F & Quartacci MF (2001) Phytoremediation of metals. Tolerance mechanisms against oxidative stress. Minerva Biotec 13: 73–83Google Scholar
  80. Nishikiori T, Okuyama A, Naganawa T, Takita T, Hamida M, Takeuchi T, Aoyagi T & Umezawa H (1984) Production of actinomycetes of (S, S')-N, N'-ethylenediamine-dissuccinic acid, an inhibitor of phospholipase. J. Antibiot. 37: 426–427Google Scholar
  81. Nörtemann B (1999) Biodegradation of EDTA. Appl. Microbiol. Biotechnol. 51: 751–759Google Scholar
  82. Norwell WA (1984) Comparison of chelating agents as extractants for metals in diverse soil materials. Soil Sci. Soc. Am. J. 48: 1285–1292Google Scholar
  83. Pahlsson AMB (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Pollut. 47: 287–319Google Scholar
  84. Puschenreiter M, Stöger G, Lombi E, Horak O & Wenzel WW (2001) Phytoextraction of heavy metal contaminated soils with Thlaspi goesingense and Amaranthus hybridus:rhizo-sphere manipulation using EDTA and ammonium sulfate. J. Plant Nutr. Soil Sci. 164: 615–621Google Scholar
  85. Raskin I, Kumar PBAN, Dushenkov S & Salt DE (1994) Bioconcentration of heavy metals by plants. Curr. Opin. Biotechnol. 5: 285–290Google Scholar
  86. Raskin I, Smith RD & Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr. Opin. Biotechnol. 8: 221–226Google Scholar
  87. Robinson B, Fernández JE, Madejón P, Marañón T, Murillo JM, Green S & Clothier B (2003) Phytoextraction:An assessment of biogeochemical and economic viability. Plant Soil. 249: 117–125Google Scholar
  88. Robinson BH (1997) The phytoextraction of heavy metals from metalliferous soils. Ph. D. Thesis. Massey University, New ZealandGoogle Scholar
  89. Robinson BH, Brooks RR, Howes AW, Kirkman JH & Gregg PEH (1997) The potential of the high-biomass nickel hyper-accumulator Berkheya coddii for phytoremediation and phytomining. J. Geochem. Explor. 60: 115–126Google Scholar
  90. Romheld V & Marschner H (1986) Mobilization of iron in the rhizosphere of different plant species. Adv. Plant Nutr. 2: 155–204Google Scholar
  91. Römkens P, Bouwman L, Japenga J & Draaisma C (2002) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ. Pollut. 116: 109–121Google Scholar
  92. Ruby MV, Schoof R, Brattin W, Goldade M, Post G, Harnois M, Mosby DE, Casteel SW, Berti W, Carpenter M, Edwards D, Cragin D & Chappell W(1999) Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ. Sci. Technol. 32: 3697–3705Google Scholar
  93. Sahut C, Geniaut G & Lillo MP (2003) Phytoremediation of metals contaminated dredged sediments:use of synthetic chelates in metals phytoextraction. J. Phys. IV France 107: 1169–1171Google Scholar
  94. Salido AL, Hasty KL, Lim JM & Butcher DJ (2003) Phytoremediation of arsenic and lead in contaminated soil using Chinese brake ferns (Pteris vittata) and Indian mustard (Brassica juncea). Int. J. Phytoremediation 5: 89–103Google Scholar
  95. Salt DE, Blaylock M, Kumar PBAN, Dushenkov V, Ensley BD, Chet I & Raskin I (1995) Phytoremediation:A novel strategy for the removal of toxic metals from the environment using plants. Biotechnol. 13: 468–475Google Scholar
  96. Salt DE, Smith RD & Raskin I (1998) Phytoremediation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 643–668Google Scholar
  97. Sanitàdi Toppi L & Gabbrielli R (1999) Response to cadmium in higher plants. Environ. Experimental Bot. 41: 105–130Google Scholar
  98. Sarret G, Vangronsveld J, Manceau A, Musso M, D'Haen J, Menthonnex JJ & Hazemann JL (2001) Accumulation forms of Zn and Pb in Phaseolus vulgaris in the presence and absence of EDTA. Environ. Sci. Technol. 35: 2854–2859Google Scholar
  99. Satroutdinov AD, Dedyukhina EG, Chistyakova TI, Witschel M, Minkevich IG, Eroshin VK & Egli T (2000) Degradation of metal-EDTA complexes by resting cells of the bacterial strain DSM 9103. Environ. Sci. Technol. 34: 1715–1720Google Scholar
  100. Schäfer HJ, Haag-Kerwer A & Rausch T (1998) cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cd-induction of a putative mitochondrial c glutamylcysteine synthetaseisoform. Plant Mol. Biol. 37: 87–97Google Scholar
  101. Schulman RN, Salt DE & Raskin I (1999) Isolation and partial characterization of a lead-accumulating Brassica juncea. Theor. Appl. Genet. 99: 398–404Google Scholar
  102. Schutzendubel A & Polle A (2002) Plant responses to abiotic stress:heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53: 1351–1365Google Scholar
  103. Shen Z-G, Li X-D, Wang C-C, Chen H-M & Chua H (2002) Lead phytoextraction from contaminated soil with high-biomass plant species. J. Environ. Qual. 31: 1893–1900Google Scholar
  104. Stanhope KG, Young SD, Hutchinson JJ & Kamath R (2000) Use of isotopic dilution techniques to assess the mobilization of nonlabile Cd by chelating agents in phytoremediation. Environ. Sci. Technol. 34: 4123–4127Google Scholar
  105. Sun B, Zhao FJ, Lombi E & McGrath SP (2001) Leaching of heavy metals from contaminated soils using EDTA. Environ. Pollut. 113: 111–120Google Scholar
  106. Thayalakumaran T, Vogeler I, Scotter DR, Percival HJ, Robinson BH & Clothier BE (2003) Leaching of copper from contaminated soil following the application of EDTA. I. Repacked soil experiments and a model. Aust. J. Soil Res. 41: 323–333Google Scholar
  107. Tiedje JM & Mason BB (1974) Biodegradation of nitrilotr-iacetate (NTA) in soils. Soil Sci. Soc. Am. Proc. 38: 278–283Google Scholar
  108. United States Environmental Protection Agency (2000) Introduction to phytoremediation EPA/600/R-99/107. US Environmental Protection Agency, Office of Research and Development, Cincinnati, OH, USAGoogle Scholar
  109. Vassil AD, Kapulnik Y, Raskin I & Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol. 117: 447–453Google Scholar
  110. Walker DJ, Clemente R, Roig A & Bernal MP (2003) The effects of soil amendments on heavy metal bioavailability in two contaminated Mediterranean soils. Environ. Pollut. 122: 303–312Google Scholar
  111. Wenger K, Gupta SK, Furrer G & Schulin R (2003) The role of nitrilotriacetate in copper uptake by tobacco. J. Environ. Qual. 32: 1669–1676Google Scholar
  112. Wenzel WW, Unterbrunner R, Sommer P & Sacco P (2003) Chelate-assisted phytoextraction using canola (Brassica napus L. ) in outdoors pot and lysimeter experiments. Plant Soil. 249: 83–96Google Scholar
  113. Wu J, Hsu FC & Cunningham SD (1999) Chelate-assisted Pb phytoextraction:Pb availability, uptake, and translocation constraints. Environ. Sci. Technol. 33: 1898–1904Google Scholar
  114. Wu LH, Luo YM, Christie P & Wong MH (2003) Effects of EDTA and low molecular weight organic acids on soil solution properties of a heavy metal polluted soil. Chemosphere 50: 819–822Google Scholar
  115. Zenk MH (1996) Heavy metal detoxi cation in higher plants-a review. Gene 179: 21–30Google Scholar
  116. Zhu YL, Pilon-Smits EAH, Jouanin L & Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119: 73–79Google Scholar
  117. Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L & Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing c glutamylcysteine synthetase. Plant Physiol. 121: 1169–1177Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • I. Alkorta
    • 1
  • J. Hernández-Allica
    • 2
  • J.M. Becerril
    • 3
  • I. Amezaga
    • 3
  • I. Albizu
    • 2
  • M. Onaindia
    • 3
  • C. Garbisu
    • 2
  1. 1.Unidad de BiofísicaCentro Mixto UPV/EHUSpain
  2. 2.NEIKERBasque Institute of Agricultural Research and Development, c/Spain
  3. 3.Department of Plant Biology and EcologyUniversity of the Basque CountrySpain

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