Environmental Chemistry Letters

, Volume 8, Issue 1, pp 1–17 | Cite as

Field crops for phytoremediation of metal-contaminated land. A review

  • Teofilo Vamerali
  • Marianna Bandiera
  • Giuliano Mosca
Review

Abstract

The use of higher plants to remediate contaminated land is known as phytoremediation, a term coined 15 years ago. Among green technologies addressed to metal pollution, phytoextraction has received increasing attention starting from the discovery of hyperaccumulator plants, which are able to concentrate high levels of specific metals in the above-ground harvestable biomass. The small shoot and root growth of these plants and the absence of their commercially available seeds have stimulated study on biomass species, including herbaceous field crops. We review here the results of a bibliographical survey from 1995 to 2009 in CAB abstracts on phytoremediation and heavy metals for crop species, citations of which have greatly increased, especially after 2001. Apart from the most frequently cited Brassica juncea (L.) Czern., which is often referred to as an hyperaccumulator of various metals, studies mainly focus on Helianthus annuus L., Zea mays L. and Brassica napus L., the last also having the greatest annual increase in number of citations. Field crops may compensate their low metal concentration by a greater biomass yield, but available data from in situ experiments are currently very few. The use of amendments or chelators is often tested in the field to improve metal recovery, allowing above-normal concentrations to be reached. Values for Zn exceeding 1,000 mg kg−1 are found in Brassica spp., Phaseolus vulgaris L. and Zea mays, and Cu higher than 500 mg kg−1 in Zea mays, Phaseolus vulgaris and Sorghum bicolor (L.) Moench. Lead greater than 1,000 mg kg−1 is measured in Festuca spp. and various Fabaceae. Arsenic has values higher than 200 mg kg−1 in sorghum and soybean, whereas Cd concentrations are generally lower than 50 mg kg−1. Assisted phytoextraction is currently facilitated by the availability of low-toxic and highly degradable chelators, such as EDDS and nitrilotriacetate. Currently, several experimental attempts are being made to improve plant growth and metal uptake, and results are being achieved from the application of organic acids, auxins, humic acids and mycorrhization. The phytoremediation efficiency of field crops is rarely high, but their greater growth potential compared with hyperaccumulators should be considered positively, in that they can establish a dense green canopy in polluted soil, improving the landscape and reducing the mobility of pollutants through water, wind erosion and water percolation.

References

  1. Abbott DE, Essington ME, Mullen MD, Ammons JT (2001) Fly ash and lime-stabilized biosolid mixtures in mine spoil reclamation. Simulated weathering. J Environ Qual 30:608–616Google Scholar
  2. Adriano DC (1986) Trace elements in the terrestrial environment. Springer, New YorkGoogle Scholar
  3. Adriano DC (1992) Biogeochemistry of trace metals. Lewis Publishers, Boca RatonGoogle Scholar
  4. Adriano DC (2001) Trace elements in the terrestrial environments. Biogeochemistry, bioavailability, and risks of heavy metals, 2nd edn. Springer, New YorkGoogle Scholar
  5. Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142CrossRefGoogle Scholar
  6. Alloway BJ (1990) Soil processes and behaviour of metals. In: Alloway BJ (ed) Heavy metals in soils. Blackie, Glasgow, pp 7–28Google Scholar
  7. Alvarenga P, Gonçalves AP, Fernandes RM, de Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2009) Organic residues as immobilizing agents in aided phytostabilization: (I) effects on soil chemical characteristics. Chemosphere 74:1292–1300CrossRefGoogle Scholar
  8. Álvarez E, Fernández Marcos ML, Vaamonde C, Fernández-Sanjurjo MJ (2003) Heavy metals in the dump of an abandoned mine in Galicia (NW Spain) and in the spontaneously occurring vegetation. Sci Total Environ 313:185–197CrossRefGoogle Scholar
  9. Anderson TA, Coats JR (1995) An overview of microbial degradation in the rhizosphere and its implications for bioremediation. In: Skipper HD, Turco RF (eds) Bioremediation, science and applications. SSSA, ASA, and CSS, Madison, pp 135–143Google Scholar
  10. Angelova V, Ivanov K (2009) Bio-accumulation and distribution of heavy metals in black mustard (Brassica nigra Koch). Environ Monit Assess 153:449–459CrossRefGoogle Scholar
  11. Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soils from a metallurgical site. Sci Total Environ 319:13–25CrossRefGoogle Scholar
  12. Arshad J (2007) Allelopathic interactions in mycorrhizal associations. Allelopathy J 20:9–42Google Scholar
  13. 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
  14. Baker AJM, Walker PL (1989) Ecophysiology of metal uptake by tolerant plants. In: Shaw A (ed) Heavy metal tolerance in plants—Evolutionary aspects. CRC Press, Boca Raton, Florida, pp 155–178Google Scholar
  15. Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resour Conserv Recycling 1:41–49CrossRefGoogle Scholar
  16. 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. Lewis Publ, Boca Raton, pp 85–107Google Scholar
  17. Bandiera M, Mosca G, Vamerali T (2009a) Effectiveness of roots in preventing metal leaching in EDDS-assisted phytoextraction with Brassica carinata A. Braun. and Raphanus sativus L. var. oleiformis. In: Proceedings of 7th ISRR symposium “root research and applications” (RootRAP), Boku, Vienna, 2–4 Sept 2009, pp 1–4Google Scholar
  18. Bandiera M, Mosca G, Vamerali T (2009b) Humic acids affect root characteristics of fodder radish (Raphanus sativus L. var oleiformis Pers.) in metal-polluted wastes. Desalination 247:79–92Google Scholar
  19. Barceló J, Vázquez MD, Mádico J, Poschenrieder C (1994) Hyperaccumulation of zinc and cadmium in Thlaspi caerulescens. In: Varnavas SP (ed) Environmental contamination. CEP Consultants Ltd., Edinburgh, pp 132–134Google Scholar
  20. Basta NT, Gradwohl R, Snethen KL, Schroder JL (2001) Chemical immobilization of lead, zinc, and cadmium in smelter-contaminated soils using biosolids and rock phosphate. J Environ Qual 30:1222–1230CrossRefGoogle Scholar
  21. Basta NT, Ryan JA, Chaney RL (2005) Trace element chemistry in residual-treated soil. Key concepts and metal bioavailability. J Environ Qual 34:49–63Google Scholar
  22. Baum C, Hrynkiewicz K, Lienweber P, Meiβner R (2006) Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix x dasyclados). Plant Nutr Soil Sci 169:516–522CrossRefGoogle Scholar
  23. Berti WR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 71–88Google Scholar
  24. Bianchi V, Masciandaro G, Giraldi D, Ceccanti B, Iannelli R (2008) Enhanced heavy metal phytoextraction from marine dredged sediments comparing conventional chelating agents (citric acid and EDTA) with humic substances. Water Air Soil Pollut 193:323–333CrossRefGoogle Scholar
  25. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agents. Environ Sci Technol 31:860–865CrossRefGoogle Scholar
  26. Boyd RS, Jaffré T, Odom JW (1999) Variation of nickel content in the nickel-hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica 31:403–410CrossRefGoogle Scholar
  27. Brooks RR (1998) Plants that hyperaccumulate heavy metals. CAB International, WallingfordGoogle Scholar
  28. Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57CrossRefGoogle Scholar
  29. Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362CrossRefGoogle Scholar
  30. Brown SL, Henry CH, Chaney R, Compton H, Volder PSD (2003) Using municipal biosolids in combination with other residuals to restore metal-contaminated areas. Plant Soil 249:203–215CrossRefGoogle Scholar
  31. Brown SL, Sprenger M, Maxemchuk A, Compton H (2005) Ecosystem function in alluvial tailings after biosolids and lime application. J Environ Qual 34:1–6Google Scholar
  32. Brunnert H, Zadrazil F (1985) The influence of zinc on the translocation of cadmium and mercury in the fungus Agrocybe aegerita (a model system). Angew Bot 59:469–477Google Scholar
  33. Bucheli-Witschel M, Egli T (2001) Environmental fate and microbial degradation of aminopolycarboxylic acids. FEMS Microbiol Rev 25:69–106CrossRefGoogle Scholar
  34. Cakmak I, Sari N, Marschner H, Ekiz H, Kalayci M (1996) Phytosiderophore release in bread and durum wheat genotypes differing in zinc efficiency. Plant Soil 180:183–189CrossRefGoogle Scholar
  35. Campbell BD, Grime JP (1989) A new method of exposing developing root systems to controlled patchiness in mineral nutrient supply. Ann Bot 63:395–400Google Scholar
  36. Cataldo DA, Wildung RE (1978) Soil and plant factors influencing the accumulation of heavy metals by plants. Environ Health Perspect 27:149–159CrossRefGoogle Scholar
  37. Cataldo DA, Garland TR, Wildung RE (1978) Nickel in plants: II. Distribution and chemical form in soybean plants. Plant Physiol 62:566–570CrossRefGoogle Scholar
  38. Chaney RL, Malik M, Li YM, Brown SL, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284CrossRefGoogle Scholar
  39. 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 50:807–811CrossRefGoogle Scholar
  40. Chen YH, Li XD, Shen ZG (2004) Leaching and uptake of heavy metals by ten different species of plants during an EDTA-assisted phytoextraction process. Chemosphere 57:187–196CrossRefGoogle Scholar
  41. Cieśliński G, Van Rees KCJ, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117CrossRefGoogle Scholar
  42. Clarkson DT (1996) Root structure and sites of ion uptake. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker Inc., New York, pp 483–510Google Scholar
  43. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719CrossRefGoogle Scholar
  44. Clemens S, Palmgren MG, Kraemer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315CrossRefGoogle Scholar
  45. Clemente R, Walker DJ, Berna MP (2005) Uptake of heavy metals and As by Brassica juncea grown in a contaminated soil in Aznalcollar (Spain): the effect of soil amendments. Environ Pollut 138:46–58CrossRefGoogle Scholar
  46. Cobbet CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832CrossRefGoogle Scholar
  47. Colpaert JV, Van Assche JA (1992) The effects of cadmium and the cadmium-zinc interaction on the axenic growth of ectomycorrhizal fungi. Plant Soil 145:237–243CrossRefGoogle Scholar
  48. Davies FT Jr, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). Plant Physiol 158:777–786CrossRefGoogle Scholar
  49. Delfine S, Tognetti R, Desiderio E, Alvino A (2005) Effect of foliar application of N and humic acids on growth and yield of durum wheat. Agron Sustain Dev 25:183–191CrossRefGoogle Scholar
  50. Dietz AC, Schnoor JL (2001) Advances in phytoremediation. Environ Health Perspect 109:163–168CrossRefGoogle Scholar
  51. Dimkpa CO, Svatoš A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25CrossRefGoogle Scholar
  52. Dorlhac de Borne F, Elmayan T, De Roton C, De Hys L, Tepfer M (1998) Cadmium partitioning in transgenic tobacco plants expressing a mammalian metallothionein gene. Molecul Breeding 4:83–90CrossRefGoogle Scholar
  53. Duffus JH (2002) “Heavy metals”—A meaningless term? Pure Appl Chem 74:793–807CrossRefGoogle Scholar
  54. Dushenkov S, Skarzhinskaya M, Glimelius K, Gleba D, Raskin I (2002) Bioengineering of a phytoremediation plant by means of somatic hybridization. Int J Phytorem 4:117–126CrossRefGoogle Scholar
  55. Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781CrossRefGoogle Scholar
  56. Ebbs SD, Lasat MM, Brady DJ, Cornish J, Gordon R, Kochian LV (1997) Phytoextraction of cadmium and zinc from a contaminated site. J Environ Qual 26:1424–1430CrossRefGoogle Scholar
  57. EEA (2003) Soil degradation. In: Europe’s environment: the third assessment. Environmental assessment report N. 10. EEA, Copenhagen, pp 198–212Google Scholar
  58. EEA (2007) Progress in management of contaminated sites (CSI 015)—May 2007 assessment. European environment agency. http://themes.eea.europa.eu/IMS/IMS/ISpecs/ISpecification20041007131746/IAssessment1152619898983/view_content. Accessed 01 July 2009
  59. EEA-UNEP (2000) Down to earth: soil degradation and sustainable development in Europe. A challenge for the 21st century. Environmental Issues Series N. 6. EEA, UNEP, LuxembourgGoogle Scholar
  60. Ehrlich HL (1997) Microbes and metals. Appl Microbiol Biotechnol 48:687–692CrossRefGoogle Scholar
  61. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J. Plant Nutr 15:763–782CrossRefGoogle Scholar
  62. Ensley BD, Blaylock MJ, Dushenkov S, Nanda-Kumar PBA, Kapulnik Y (1999) Inducing hyperaccumulation of metals in plant shoots. US Patent 5,917,117, 29 JuneGoogle Scholar
  63. Evangelou MWH, Dagan H, Schaeffer A (2004) The influence of humic acids on the phytoextraction of cadmium from soil. Chemosphere 57:207–213CrossRefGoogle Scholar
  64. Fellet G, Marchiol L, Perosa D, Zerbi G (2007) The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol Eng 31:207–214CrossRefGoogle Scholar
  65. Fitter AH, Stickland TR (1991) Architectural analysis of plant root systems. 2. Influence of nutrient supply on architecture in contrasting plant species. New Phytol 118:383–389CrossRefGoogle Scholar
  66. Förstner U (1995) Land contamination by metals: global scope and magnitude of problem. In: Allen HE, Huang CP, Bailey GW, Bowers AR (eds) Metal speciation and contamination of soil. CRC Press, Boca Raton, pp 1–33Google Scholar
  67. French CJ, Dickinson NM, Putwain PD (2006) Woody biomass phytoremediation of contaminated brownfield land. Environ Pollut 141:387–395CrossRefGoogle Scholar
  68. Gao Y, He J, Ling W, Hu H, Liu F (2003) Effects of organic acids on copper and cadmium desorpion from contaminated soils. Environ Int 29:613–618CrossRefGoogle Scholar
  69. Garbisu C, Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Min Proc Einviron Protect 3:229–236Google Scholar
  70. Gaweda M, Capecka E (1995) Effect of substrate pH on the accumulation of lead in radish (Raphanus sativus L. subvar. radicula) and spinach (Spinacia oleracea L.). Acta Physiol Plant 17:333–340Google Scholar
  71. Giasson P, Jaouich A, Gagné S, Moutoglis P (2005) Arbuscular mycorrhizal fungi involvement in zinc and cadmium speciation change and phytoaccumulation. Remediat J 15:75–81CrossRefGoogle Scholar
  72. Grčman H, Velikonja-Bolta Š, Vodnic D, Leštan D (2001) EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant Soil 235:105–114CrossRefGoogle Scholar
  73. Grčman H, Vodnic D, Velikonja-Bolta Š, Leštan D (2003) Ethylenediamine disuccinate as a new chelate for environmentally safe enhanced lead phytoremediation. J Environ Qual 32:500–506CrossRefGoogle Scholar
  74. Guan ZQ, Chai TY, Zhang YX, Xu J, Wei W, Han L, Cong L (2008) Gene manipulation of a heavy metal hyperaccumulator species Thlaspi caerulescens L. via Agrobacterium-mediated transformation. Mol Biotechnol 40:77–86CrossRefGoogle Scholar
  75. Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505CrossRefGoogle Scholar
  76. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52:265–275CrossRefGoogle Scholar
  77. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613CrossRefGoogle Scholar
  78. Han YY, Zhang WZ, Zhang BL, Zhang SS, Wang W, Ming F (2009) One novel mitochondrial citrate synthase from Oryza sativa L. can enhance aluminum tolerance in transgenic tobacco. Mol Biotechnol 42:299–305CrossRefGoogle Scholar
  79. Hartley J, Caimey JWG, Meharg AA (1997) Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant Soil 189:303–319CrossRefGoogle Scholar
  80. Hartley W, Dickinson NM, Clemente R, French C, Piearce TG, Sparke S, Lepp NW (2009) Arsenic stability and mobilization in soil at an amenity grassland overlying chemical waste (St. Helens, UK). Environ Pollut 157:847–856CrossRefGoogle Scholar
  81. Haussling M, Jorns CA, Lehmbecker G, Hecht-Buchholz C, Marschner H (1988) Ion and water uptake in relation to root development in Norway Spruce (Picea abies (L) Karst). J. Plant Physiol 133:486–491Google Scholar
  82. Haynes RJ (1980) Ion exchange properties of roots and ionic interactions within the root apoplasm: their role in ion accumulation by plants. Bot Rev 46:75–99CrossRefGoogle Scholar
  83. Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471–479CrossRefGoogle Scholar
  84. Hofrichter M, Steinbüchel A (2001) Biopolymers, Vol. 1. Lignin, humic substances and coal. Wiley Europe-VCH, WeinheimGoogle Scholar
  85. Huang JW, Chen J, Berti WR, Cunningham SD (1997) Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805CrossRefGoogle Scholar
  86. Jaffre T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580CrossRefGoogle Scholar
  87. Jaworska JS, Schowanek D, Feijtel TCJ (1999) Environmental risk assessment for trisodium [S,S]-ethylene diamine disuccinate, a biodegradable chelator used in detergent applications. Chemosphere 38:3597–3625CrossRefGoogle Scholar
  88. Kanazawa K, Higuchi K, Nishizawa NK, Fushiya S, Chino M, Mori S (1994) Nicotianamine aminotransferase activities are correlated to the phytosiderophore secretion under Fe-deficient conditions in Gramineae. J Exp Bot 45:1903–1906CrossRefGoogle Scholar
  89. Kayser A, Wenger K, Keller A, Attinger W, Felix H, 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 34:1778–1783CrossRefGoogle Scholar
  90. King RF, Royle A, Putwain PD, Dickinson NM (2006) Changing contaminant mobility in a dredged canal sediment during a three-year phytoremediation trial. Environ Pollut 143:318–326CrossRefGoogle Scholar
  91. Kos B, Leštan D (2004) Chelator induced phytoextraction and in situ washing of Cu. Environ Pollut 132:333–339CrossRefGoogle Scholar
  92. Krishnamurti GSR, Cielinski G, Huang PM, van Rees KCJ (1997) Kinetics of cadmium release from soils as influenced by organic acid: implementation in cadmium availability. J Environ Qual 26:271–277CrossRefGoogle Scholar
  93. Kulli B, Balmer M, Krebs R, Lothenbach B, Geiger G, Schulin R (1999) The influence of nitrilotriacetate on heavy metal uptake of lettuce and ryegrass. J Environ Qual 28:1699–1705CrossRefGoogle Scholar
  94. Lagier T, Feuillade G, Matejka G (2000) Interactions between copper and organic macromolecules: determination of conditional complexation constants. Agronomie 20:537–546CrossRefGoogle Scholar
  95. Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117:19–27CrossRefGoogle Scholar
  96. Lasat MM (2002) Phytoremediation of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120CrossRefGoogle Scholar
  97. Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883CrossRefGoogle Scholar
  98. Li HF, Gray C, Mico C, Zhao FJ, McGrath SP (2009) Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere 75:979–986CrossRefGoogle Scholar
  99. Liphadzi MS, Kirkham MB, Paulsen GM (2006) Auxin-enhanced root growth for phytoremediation of sewage-sludge amended soil. Environ Technol 27:695–704CrossRefGoogle Scholar
  100. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001) Phytoremediation of heavy metal-contaminated soils: natural hyperaccumulation versus chemically enhanced phytoextraction. J Environ Qual 30:1919–1926CrossRefGoogle Scholar
  101. López ML, Peralta-Videa JR, Benitez T, Gardea-Torresdey JL (2005) Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere 61:595–598CrossRefGoogle Scholar
  102. Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59:1–11CrossRefGoogle Scholar
  103. Luo C, Shen Z, Luo L, Li X (2006) EDDS and EDTA-enhanced phytoextraction of metals from artificially contaminated soil and residual effects of chelant compounds. Environ Pollut 144:862–871CrossRefGoogle Scholar
  104. Luo CL, Shen ZG, Li XD (2008) Hot NTA application enhanced metal phytoextraction from contaminated soil. Water Air Soil Pollut 188:127–137CrossRefGoogle Scholar
  105. Ma LQ, Komar KM, Tu C, Zhang WH, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579CrossRefGoogle Scholar
  106. MacCarthy P (2001) The principles of humic substances. Soil Sci 166:738–751CrossRefGoogle Scholar
  107. Macek T, Macková M, Pavlíková D, Száková J, Truksa M, Singh-Cundy A, Kotrba P, Yancey N, Scouten WH (2002) Accumulation of cadmium by transgenic tobacco. Acta Biotechnol 22:101–106CrossRefGoogle Scholar
  108. Marchiol L, Sacco P, Assolari S, Zerbi G (2004) Reclamation of polluted soil: phytoremediation potential of crop-related Brassica species. Water Air Soil Pollut 158:345–356CrossRefGoogle Scholar
  109. Marchiol L, Fellet G, Perosa D, Zerbi G (2007) Removal of trace metals by Sorghum bicolor and Helianthus annuus in a site polluted by industrial wastes: a field experience. Plant Physiol Biochem 45:379–387CrossRefGoogle Scholar
  110. Marin AR, Masscheleyn PH, Patrick WH Jr (1992) The influence of chemical form and concentration of arsenic on rice growth and tissue arsenic concentration. Plant Soil 139:175–183CrossRefGoogle Scholar
  111. McCutcheon SC, Schnoor JL (2003) Phytoremediation. Wiley, HobokenCrossRefGoogle Scholar
  112. McGrath SP (1998) Phytoextraction for soil remediation. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, pp 261–287Google Scholar
  113. McGrath SP, Lombi E, Gray CW, Caille N, Dunham SJ, Zhao FJ (2006) Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125CrossRefGoogle Scholar
  114. Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162CrossRefGoogle Scholar
  115. Meda AR, Scheuermann EB, Prechsl UE, Erenoglu B, Schaaf G, Hayen H, Weber G, von Wirén N (2007) Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiol 143:1761–1773CrossRefGoogle Scholar
  116. Meers E, Hopgood M, Lesge E, Vervake P, Tack FMG, Verloo MG (2004) Enhanced phytoextraction: in search of EDTA alternatives. Int J Phytoremediat 6:95–109CrossRefGoogle Scholar
  117. Meeuseen JCL, Keizer MG, Reimsdijk WH, Haan FAM (1994) Solubility of cyanide in contaminated soil. J Environ Qual 23:785–792CrossRefGoogle Scholar
  118. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytol 154:29–43CrossRefGoogle Scholar
  119. Mellem JJ, Baijnath H, Odhav B (2009) Translocation and accumulation of Cr, Hg, As, Pb, Cu and Ni by Amaranthus dubius (Amaranthaceae) from contaminated sites. J Environ Sci Heal A 44:568–575CrossRefGoogle Scholar
  120. Mench M, Bussière S, Boisson J, Castaing E, Vangronsveld J, Ruttens A (2003) Progress in remediation and revegetation of the barren Jales gold mine spoil after in situ treatments. Plant Soil 249:187–202CrossRefGoogle Scholar
  121. Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments—an emerging remediation technology. Environ Health Perspect 116:278–283CrossRefGoogle Scholar
  122. Moreno FN, Anderson CWN, Stewart RB, Robinson BH, Ghomshei M, Meech JA (2005) Induced plant uptake and transport of mercury in the presence of sulphur-containing ligands and humic acid. New Phytol 166:445–454CrossRefGoogle Scholar
  123. Mosca G, Vamerali T, Ganis A, Coletto L, Bona S (2004) Miglioramento dell’efficienza agronomica della fitodecontaminazione di metalli pesanti. In: Zerbi G, Marchiol L (eds) Fitoestrazione Di Metalli Pesanti—Contenimento Del Rischio Ambientale E Relazioni Suolo-Mirorganismi-Pianta. Forum Editrice Universitaria Udinese, Udine, pp 105–135Google Scholar
  124. Murakami M, Ae N (2009) Potential for phytoextraction of copper, lead, and zinc by rice (Oryza sativa L.), soybean (Glycine max [L.] Merr.), and maize (Zea mays L.). J Hazard Mater 162:1185–1192CrossRefGoogle Scholar
  125. Nanda-Kumar PBA, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238CrossRefGoogle Scholar
  126. Navari-Izzo F, Quartacci MF (2001) Phytoremediation of metals. Tolerance mechanisms against oxidative stress. Minerva Biotec 13:73–83Google Scholar
  127. Neunhäuserer C, Berreck M, Insam H (2001) Remediation of soils contaminated with molybdenum using soil amendments and phytoremediation. Water Air Soil Pollut 128:85–96CrossRefGoogle Scholar
  128. Pajuelo E, Carrasco JA, Romero LC, Chamber MA, Gotor C (2007) Evaluation of the metal phytoextraction potential of crop legumes. Regulation of the expression of O-acetylserine (thiol)lyase under metal stress. Plant Biol 9:672–681CrossRefGoogle Scholar
  129. Pavlikova D, Macek T, Mackova M, Sura M, Szakova J, Tlustos P (2004) The evaluation of cadmium, zinc and nickel accumulation ability of transgenic tobacco bearing different transgenes. Plant Soil Environ 50:513–517Google Scholar
  130. Pellet MD, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminium tolerance mechanism in maize (Zea mays L.). Planta 196:788–795CrossRefGoogle Scholar
  131. Pirbazari M, Badriyha BN, Ravindran V, Kim S (1989) Treatment of landfill leachate by biologically active carbon adsorbers. In: Bell JM (ed) Proceedings of 44th annual Purdue conference on industrial wastes. Lewis Publishers, Chelsea, pp 555–563Google Scholar
  132. Pizzeghello D, Nicolini G, Nardi S (2000) Hormone-like activities of humic substances in different forest ecosystems. New Phytol 155:393–402CrossRefGoogle Scholar
  133. Prasad MNV, De Oliveira-Freitas HM (2003) Metal hyperaccumulation in plants—Biodiversity prospecting for phytoremediation technology. Electr J Biotech 6:285–321Google Scholar
  134. Probst A, Liu H, Fanjul M, Liao B, Hollande E (2009) Response of Vicia faba L. to metal toxicity on mine tailing substrate: geochemical and morphological changes in leaf and root. Environ Exp Bot 66:297–308CrossRefGoogle Scholar
  135. Quartacci MF, Cosi E, Meneguzzo S, Sgherri C, Navari-Izzo F (2003) Uptake and translocation of copper in Brassicaceae. J Plant Nutr 26:1065–1083CrossRefGoogle Scholar
  136. Quartacci MF, Baker AJM, Navari-Izzo F (2005) Nitrilotriacetate- and citric acid-assisted phytoextraction of cadmium by Indian mustard (Brassica juncea (L.) Czernj, Brassicaceae). Chemosphere 59:1249–1255CrossRefGoogle Scholar
  137. Quartacci MF, Argilla A, Baker AJM, Navari-Izzo F (2006) Phytoextraction of metals from a multiply contaminated soil by Indian mustard. Chemosphere 63:918–925CrossRefGoogle Scholar
  138. Quartacci MF, Irtelli B, Baker AJM, Navari-Izzo F (2007) The use of NTA and EDDS for enhanced phytoextraction of metals from a multiply contaminated soil by Brassica carinata. Chemosphere 68:1920–1928CrossRefGoogle Scholar
  139. Raskin I (1996) Plant genetic engineering may help with environmental cleanup. Proc Natl Acad Sci USA 93:3164–3166CrossRefGoogle Scholar
  140. Raskin I, Kumar PBAN, Dushenkov S, Salt D (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285–290CrossRefGoogle Scholar
  141. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–230Google Scholar
  142. Reisinger S, Schiavon M, Terry N, Pilon-Smits EAH (2008) Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial gamma-glutamylcysteine synthetase or glutathione synthetase. Int J Phytoremediat 10:440–454CrossRefGoogle Scholar
  143. Rizzi L, Petruzelli G, Poggio G, Vigna Guidi G (2004) Soil physical changes and plant availability of Zn and Pb in a treatability test of phytostabilization. Chemosphere 57:1039–1046CrossRefGoogle Scholar
  144. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997a) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126CrossRefGoogle Scholar
  145. Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, DeDominicis V (1997b) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86CrossRefGoogle Scholar
  146. Robinson BH, Meblanc L, Petit D, Broks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56CrossRefGoogle Scholar
  147. Ruley AT, Sharma NC, Sahi SV, Singh SR, Sajwan KS (2006) Effects of lead and chelators on growth, photosynthetic activity and Pb uptake in Sesbania drummondii grown in soil. Environ Pollut 144:11–18CrossRefGoogle Scholar
  148. Salt DE, Kramer U (2000) Mechanisms of metal hyperaccumulation in plants. In: Raskin I, Ensley B (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 231–246Google Scholar
  149. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668CrossRefGoogle Scholar
  150. Sappin-Didier V, Vansuyts G, Mench M, Briat JF (2005) Cadmium availability at different soil pH to transgenic tobacco overexpressing ferritin. Plant Soil 270:189–197CrossRefGoogle Scholar
  151. Schmidt U (2003) Enhancing phytoextraction: the effect of chemical soil manipulation on mobility, plant accumulation, and leaching of heavy metals. J Environ Qual 32:1939–1954CrossRefGoogle Scholar
  152. Schnoor JL, Licht LA, McCutcheon SC, Wolfe NL, Carreira LH (1995) Phytoremediation of organic and nutrient contaminants. Environ Sci Technol 29:318–323CrossRefGoogle Scholar
  153. Schowanek D, Feijtel TCJ, Perkins CM, Hartman FA, Federle TW, Larson RJ (1997) Biodegradation of [S,S], [R,R] and mixed stereoisomers of ethylene diamine disuccinic acid (EDDS), a transition metal chelator. Chemosphere 34:2375–2391CrossRefGoogle Scholar
  154. 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 localisation in soil. Plant Soil 208:103–115CrossRefGoogle Scholar
  155. Sheng XF, Xia JJ (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64:1036–1042CrossRefGoogle Scholar
  156. Soriano AM, Fereres E (2003) Use of crops for in situ phytoremediation of polluted soils following a toxic flood from a mine spill. Plant Soil 256:253–264CrossRefGoogle Scholar
  157. Sun B, Zhao FJ, Lombi E, McGrath SP (2001) Leaching of heavy metals from contaminated soils using EDTA. Environ Pollut 113:111–120CrossRefGoogle Scholar
  158. Suthersan SS (1997) Remediation engineering: design concepts. CRC Press/Lewis Publishers, Boca RatonGoogle Scholar
  159. Sutton P, Dick WA (1987) Reclamation of acidic mined lands in humid areas. Adv Agron 41:377–406CrossRefGoogle Scholar
  160. Tandy S, Bossart K, Mueller R, Ritschel J, Hauser L, Schulin R, Nowack B (2004) Extraction of heavy metals from soils using biodegradable chelating agents. Environ Sci Technol 38:937–944CrossRefGoogle Scholar
  161. Tandy S, Schulin R, Nowack B (2006) Uptake of metals during chelant-assisted phytoextraction with EDDS related to the solubilized metal concentration. Environ Sci Technol 40:2753–2758CrossRefGoogle Scholar
  162. Tanton TW, Crowdy SH (1971) The distribution of lead chelate in the transpirational stream of higher plants. Pestic Sci 2:211–213CrossRefGoogle Scholar
  163. Tassi E, Pouget J, Petruzzelli G, Barbafieri M (2008) The effects of exogenous plant growth regulators in the phytoextraction of heavy metals. Chemosphere 71:66–73CrossRefGoogle Scholar
  164. Taub DR, Goldberg D (1996) Root system topology of plants from habitats differing in soil resource availability. Funct Ecol 10:258–264CrossRefGoogle Scholar
  165. Terry N, Bañuelos GS (2000) Phytoremediation of contaminated soil and water. CRC Press, Lewis Publ, Boca RatonGoogle Scholar
  166. The Conservation Foundation (1987) State of the environment: a view toward the nineties. The Conservation Foundation, Washington, DCGoogle Scholar
  167. Tiwari KK, Dwivedi S, Singh NK, Rai UN, Tripathi RD (2009) Chromium (VI) induced phytotoxicity and oxidative stress in pea (Pisum sativum L.): biochemical changes and translocation of essential nutrients. J Environ Biol 30:389–394Google Scholar
  168. Tode K, Hartwig L (2001) Fusicoccin- and IAA-induced elongation growth share the same pattern of K+ dependence. J Exp Bot 52:251–255CrossRefGoogle Scholar
  169. Tomsett AB, Sewell AK, Jones SJ, Miranda JR, de Thurman DA (1992) Metal-binding proteins and metal-regulated gene expression in higher plants. In: Wray JL (ed) Inducible plant proteins: their biochemistry and molecular biology. Cambridge University Press, Cambridge, pp 1–24Google Scholar
  170. Trewavas AJ (2000) Signal perception and transduction. In: Buchannan B, Gruisem W, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiology, USA, pp 930–988Google Scholar
  171. Vamerali T, Bandiera M, Coletto L, Zanetti F, Dickinson NM, Mosca G (2009) Phytoremediation trials on metal- and arsenic-contaminated pyrite wastes (Torviscosa, Italy). Environ Pollut 157:887–894CrossRefGoogle Scholar
  172. Van der Lelie D, Schwitzgübel JP, Glass DJ, Vangronsveld J, Baker AJM (2001) Assessing phytoremediation progress in the United States and Europe. Environ Sci Technol 35:446–452CrossRefGoogle Scholar
  173. Vandevivere P, Saveyn H, Verstraete W, Feijtel TCJ, Schowanek D (2001) Biodegradation of metal-[S,S]-EDDS complexes. Environ Sci Technol 35:1765–1770CrossRefGoogle Scholar
  174. Vangronsveld J, Assche FV, Clijsters H (1995) Reclamation of a bare industrial area contaminated by non-ferrous metals: in situ metal immobilization and revegetation. Environ Pollut 87:51–59CrossRefGoogle Scholar
  175. Visoottiviseth P, Francesconi K, Sridokchan V (2002) The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut 118:453–461CrossRefGoogle Scholar
  176. Wallace A, Mueller RT, Wood RA (1980) Arsenic phytotoxicity and interactions in bush bean plants grown in solution culture. J Plant Nutr 2:111–113CrossRefGoogle Scholar
  177. Wang QR, Liu XM, Cui YS, Dong YT, Christie P (2002) Response of legume and non-legume crop species to heavy metals in soils with multiple metal contamination. J Environ Sci Health 37:611–621CrossRefGoogle Scholar
  178. Wang F, Lin X, Yin R (2005) Heavy metal uptake by arbuscular mycorrhizas of Elsholtzia splendens and the potential for phytoremediation of contaminated soil. Plant Soil 269:225–232CrossRefGoogle Scholar
  179. Ward TE (1986) Aerobic and anaerobic biodegradation of nitrilotriacetate in subsurface soils. Ecotox Environ Safe 11:112–125CrossRefGoogle Scholar
  180. Wenger K, Gupta SK, Furrer G, Schulin R (2003) The role of nitrilotriacetate in copper uptake by tobacco. J Environ Qual 32:1669–1676CrossRefGoogle Scholar
  181. 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 145:199–210CrossRefGoogle Scholar
  182. Wong MH (2003) Ecological restoration of degraded soils with emphasis on metal contaminated soils. Chemosphere 50:775–780CrossRefGoogle Scholar
  183. 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 50:819–822CrossRefGoogle Scholar
  184. Wu LH, Sun XF, Luo YM, Xing XR, Christie P (2007) Influence of [S, S]-EDDS on phytoextraction of copper and zinc by Elsholtzia splendens from metal-contaminated soil. Int J Phytorem 9:227–241CrossRefGoogle Scholar
  185. Ye ZH, Wong JWC, Wong MH, Lan CY, Baker AJM (1999) Lime and pig manure as ameliorants for revegetating lead/zinc mine tailings: a greenhouse study. Bioresour Technol 69:35–43CrossRefGoogle Scholar
  186. Yoon J, Cao X, Zhou O (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464CrossRefGoogle Scholar
  187. Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Teofilo Vamerali
    • 1
  • Marianna Bandiera
    • 2
  • Giuliano Mosca
    • 2
  1. 1.Department of Environmental SciencesUniversity of ParmaParmaItaly
  2. 2.Department of Environmental Agronomy and Crop SciencesUniversity of PadovaLegnaro, PadovaItaly

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