Environmental Science and Pollution Research

, Volume 16, Issue 2, pp 162–175

Implications of metal accumulation mechanisms to phytoremediation



Background, aim, and scope

Trace elements (heavy metals and metalloids) are important environmental pollutants, and many of them are toxic even at very low concentrations. Pollution of the biosphere with trace elements has accelerated dramatically since the Industrial Revolution. Primary sources are the burning of fossil fuels, mining and smelting of metalliferous ores, municipal wastes, agrochemicals, and sewage. In addition, natural mineral deposits containing particularly large quantities of heavy metals are found in many regions. These areas often support characteristic plant species thriving in metal-enriched environments. Whereas many species avoid the uptake of heavy metals from these soils, some of them can accumulate significantly high concentrations of toxic metals, to levels which by far exceed the soil levels. The natural phenomenon of heavy metal tolerance has enhanced the interest of plant ecologists, plant physiologists, and plant biologists to investigate the physiology and genetics of metal tolerance in specialized hyperaccumulator plants such as Arabidopsis halleri and Thlaspi caerulescens. In this review, we describe recent advances in understanding the genetic and molecular basis of metal tolerance in plants with special reference to transcriptomics of heavy metal accumulator plants and the identification of functional genes implied in tolerance and detoxification.


Plants are susceptible to heavy metal toxicity and respond to avoid detrimental effects in a variety of different ways. The toxic dose depends on the type of ion, ion concentration, plant species, and stage of plant growth. Tolerance to metals is based on multiple mechanisms such as cell wall binding, active transport of ions into the vacuole, and formation of complexes with organic acids or peptides. One of the most important mechanisms for metal detoxification in plants appears to be chelation of metals by low-molecular-weight proteins such as metallothioneins and peptide ligands, the phytochelatins. For example, glutathione (GSH), a precursor of phytochelatin synthesis, plays a key role not only in metal detoxification but also in protecting plant cells from other environmental stresses including intrinsic oxidative stress reactions. In the last decade, tremendous developments in molecular biology and success of genomics have highly encouraged studies in molecular genetics, mainly transcriptomics, to identify functional genes implied in metal tolerance in plants, largely belonging to the metal homeostasis network.


Analyzing the genetics of metal accumulation in these accumulator plants has been greatly enhanced through the wealth of tools and the resources developed for the study of the model plant Arabidopsis thaliana such as transcript profiling platforms, protein and metabolite profiling, tools depending on RNA interference (RNAi), and collections of insertion line mutants. To understand the genetics of metal accumulation and adaptation, the vast arsenal of resources developed in A. thaliana could be extended to one of its closest relatives that display the highest level of adaptation to high metal environments such as A. halleri and T. caerulescens.


This review paper deals with the mechanisms of heavy metal accumulation and tolerance in plants. Detailed information has been provided for metal transporters, metal chelation, and oxidative stress in metal-tolerant plants. Advances in phytoremediation technologies and the importance of metal accumulator plants and strategies for exploring these immense and valuable genetic and biological resources for phytoremediation are discussed.

Recommendations and perspectives

A number of species within the Brassicaceae family have been identified as metal accumulators. To understand fully the genetics of metal accumulation, the vast genetic resources developed in A. thaliana must be extended to other metal accumulator species that display traits absent in this model species. A. thaliana microarray chips could be used to identify differentially expressed genes in metal accumulator plants in Brassicaceae. The integration of resources obtained from model and wild species of the Brassicaceae family will be of utmost importance, bringing most of the diverse fields of plant biology together such as functional genomics, population genetics, phylogenetics, and ecology. Further development of phytoremediation requires an integrated multidisciplinary research effort that combines plant biology, genetic engineering, soil chemistry, soil microbiology, as well as agricultural and environmental engineering.


Accumulator plants Heavy metals Metal transporters Metallothioneins Phytochelatins Phytoremediation 


  1. Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464Google Scholar
  2. Arrick BA, Nathan CF, Griffith OW, Cohn ZA (1982) Glutathione depletion sensitizes tumor cells to oxidative cytolysis. J Biol Chem 257:1231–1237Google Scholar
  3. Assunçao AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360Google Scholar
  4. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyper-accumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:181–126Google Scholar
  5. Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants, heavy metal tolerance in plants. In: Shaw AJ (ed) Evolutionary aspects. CRC, Boca Raton, pp 155–177Google Scholar
  6. 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, Vangronsveld J (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, USA, pp 85–107Google Scholar
  7. Banuelos GS, Meek DW (1990) Accumulation of selenium in plants grown on selenium-treated soil. J Environ Qual 19:727–777Google Scholar
  8. Becher M, Talke IN, Krall L, Kramer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268Google Scholar
  9. Bennett LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EAH (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal contaminated, mine tailings. J Environ Qual 32:432–440Google Scholar
  10. Bereczky Z, Wang HY, Schubert V, Ganal M, Bauer P (2003) Differential regulation of Nramp and IRT metal transporter genes in wild type and iron uptake mutants of tomato. J Biol Chem 278:24697–24704Google Scholar
  11. Bernal M, Testillano PS, Alfonso M, Del Carmen Risueno M, Picorel R, Yruela I (2007) Identification and subcellular localization of the soybean copper P1B-ATPase GmHMA8 transporter. J Struct Biol 158:146–158Google Scholar
  12. Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPxATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148Google Scholar
  13. Blaudez D, Kohler A, Martin F, Sanders D, Chalot M (2003) Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15:2911–2928Google Scholar
  14. Bratteler M, Lexer C, Widmer A (2006) Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris. J Evol Biol 19:1149–1156Google Scholar
  15. Brooks RR (1983) Biological methods of prospecting for minerals. Wiley, New YorkGoogle Scholar
  16. Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid Sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133:1272–1284Google Scholar
  17. Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyper-accumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ Sci Technol 40:6792–6798Google Scholar
  18. Clemens S (2001) Molecular mechanisms of plant metal hoemostatsis. Planta 212:475–486Google Scholar
  19. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719Google Scholar
  20. Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthase from plants and yeast. EMBO J 18:3325–3333Google Scholar
  21. Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216Google Scholar
  22. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins, roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182Google Scholar
  23. Cobbett S, Meagher RB (2002) Arabidopsis and the genetic potential for the phytoremediation of toxic elemental and organic pollutants. The Arabidopsis book. American Society of Plant Biologists, ISNN 1543–8120, http://www.org/publications/arabidopsis open access pp 1–22
  24. Cosio C, Martinoia E, Keller C (2004) Hyperaccumulation of cadmium and zinc in Thlaspi caerulescens and Arabidopsis hallari at the leaf cellular level. Plant Physiol 134:716–725Google Scholar
  25. Coupe SA, Taylor JE, Roberts JA (1995) Characterization of an m-RNA encoding a metallothionein-like protein that accumulates during ethylene-promoted abscission of Sambucus nigra L. Planta 197:442–447Google Scholar
  26. Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065Google Scholar
  27. David-Assael O, Berezin I, Shoshani-Knaani N, Saul H, Mizrachy-Dagri T, Chen J, Brook E, Shaul O (2006) AtMHX is an auxin and ABA-regulated transporter whose expression pattern suggests a role in metal homeostasis in tissues with photosynthetic potential. Funct Plant Biol 33:661–672Google Scholar
  28. Deniau AX, Pieper B (2006) WMT-B, QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920Google Scholar
  29. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244Google Scholar
  30. Domenech J, Mir G, Huguet G, Capdevila M, Molinas M, Atrian S (2006) Plant metallothionein domains: functional insight into physiological metal binding and protein folding. Biochimie 88:583–593Google Scholar
  31. Drager DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Kramer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439Google Scholar
  32. Ducruix C, Junot C, Fievet JB, Villiers F, Ezan E, Bourguignon J (2006) New insights into the regulation of phytochelatin biosynthesis in A. thaliana cells from metabolite profiling analyses. Biochimie 88:1733–1742Google Scholar
  33. EC (2002) Towards a thematic strategy for soil protection. COM 179 final. European Commission, Brussels, BelgiumGoogle Scholar
  34. EEA (2003) Europe’s environment: the third assessment. Environmental assessment report no. 10. European Environment Agency, Copenhagen, DenmarkGoogle Scholar
  35. Ensley BD (2000) Rationale for use of phytoremediation pp. 3–11. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. J. Wiley & Sons, New York, USA, 304 ppGoogle Scholar
  36. Fernando DR, Woodrow IE, Jaffre T, Dumontet V, Marshall AT, Baker AJM (2007) Foliar manganese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185Google Scholar
  37. Filatov V, Dowdle J, Smirnoff N (2006) Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol Ecol 15:3045–3059Google Scholar
  38. Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair MR (2007) A quantitative trait loci analysis of zinc hyperaccumulation in Arabidopsis halleri. New Phytol 174:580–590Google Scholar
  39. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signaling. Physiol Plant 100:241–254Google Scholar
  40. Franzius V (1994) Aktuelle Entwicklungen zur Altlastenproblematik in der Bundesrepublik Deutschland. Umwelt Technologie Aktuell 6:443–449Google Scholar
  41. Freeman JL, Salt DE (2007) The metal tolerance profile of Thlaspi goesingense is mimicked in Arabdopsis thaliana heterologously expressing serine acetyl-transferase. BMC Plant Biol 7(63):1–10Google Scholar
  42. Gaither LA, Eide DJ (2001) Eukaryotic zinc transporters and their regulation. Biometals 14:251–270Google Scholar
  43. Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194Google Scholar
  44. Ghandilyan A, Vreugdenhil D, Aarts MGM (2006) Progress in the genetic understanding of plant iron and zinc nutrition, nutriomics and biofortification. Physiol Plant 126:407–417Google Scholar
  45. Glass DJ (2000) Economic potential of phytoremediation. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 15–31Google Scholar
  46. Grant CM, Maclver FH, Dawes IW (1996) Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr Genet 29:511–515Google Scholar
  47. Grill E, Löffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy metals-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamilcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842Google Scholar
  48. Guo WJ, Meetam M, Goldsbrough P (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 164(4):1697–1706Google Scholar
  49. Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connel MJ, Goldsborough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast, Schizosaccaromyces pombe. Plant Cell 11:1153–1164Google Scholar
  50. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11Google Scholar
  51. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613Google Scholar
  52. Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, Baker AJM (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260Google Scholar
  53. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395Google Scholar
  54. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113Google Scholar
  55. Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133Google Scholar
  56. Hodoshima H, Enomoto Y, Shoji K, Shimada H, Goto F, Yoshihara T (2007) Differential regulation of cadmium-inducible expression of iron-deficiency-responsive genes in tobacco and barley. Physiol Plant 129:622–634Google Scholar
  57. Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107:1059–1066Google Scholar
  58. Hsieh HM, Liu WK, Huang PC (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol 28:381–389Google Scholar
  59. Hussain D, Michael JH, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbet CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339Google Scholar
  60. Ishimaru Y, Suzuki M, Kobayashi T, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) OsZIP4, a novel zinc-regulated zinc transporter in rice. J Exp Bot 56:3207–214Google Scholar
  61. Kawachi M, Kobae Y, Mimura T, Maeshima M (2008) Deletion of a histidine-rich loop of AtMTP1, a vacuolar Zn2+/H+ antiporter of Arabidopsis thaliana, stimulates the transport activity. J Biol Chem 283:8374–8383Google Scholar
  62. Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis iron-regulated transporter1 metal transporter requires lysine residues. Plant Physiol 146:1964–1973Google Scholar
  63. Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39:237–251Google Scholar
  64. Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:1–11Google Scholar
  65. Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Kramer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNramp3 and AtNramp4 is essential for seed germination on low iron. EMBO J 24:4041–4051Google Scholar
  66. Ledger SE, Gardner RC (1994) Cloning and characterization of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinia deliciosa var deliciosa). Plant Mol Biol 25:877–886Google Scholar
  67. Lee S, Kim Y-Y, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol 145:831–842Google Scholar
  68. Lewandowski U, Schmidt M, Londo A, Faaij (2006) The economic value of the phytoremediation function—assessed by the example of cadmium remediation by willow (Salix ssp). Agric Syst 89(1):68–89 (July)Google Scholar
  69. Lopez-Millan AF, Ellis DR, Grusak MA (2004) Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol Biol 54:583–596Google Scholar
  70. Maathuis FJM, Filatov V, Krijger GC, Herzyk P, Axelsen KB (2003) Transcriptome analysis of Arabidopsis thaliana cation transport. Plant J 35:675–692Google Scholar
  71. Macnair MR (1993) The genetic of metal tolerance in vascular plants. New Phytol 124:541–559Google Scholar
  72. Marmiroli N, Maestri E (2008) Health implications of trace elements in the environment and the food chain. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 23–53Google Scholar
  73. 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 126:1646–1667Google Scholar
  74. Maughan S, Foyer CH (2006) Genetic approaches to modulating the glutathione network in plants, nutriomics and biofortification. Physiol Planta 126:382–397Google Scholar
  75. May MJ, Leaver CJ (1995) Arabidopsis thaliana g-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast and Escherichia coli homologues. Proc Natl Acad Sci U S A 91:10059–10063Google Scholar
  76. 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 141:115–125Google Scholar
  77. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760Google Scholar
  78. Memon AR, Yatazawa M (1982) Chemical nature of manganese in the leaves of manganese accumulator plants. Soil Sci Plant Nutr 28:401–412Google Scholar
  79. Memon AR, Yatazawa M (1984) Nature of manganese complexes in Mn accumulator plant—Acanthopanax sciadophylloides. J Plant Nutr 7:961–974Google Scholar
  80. Memon AR, Chino M, Yatazawa M (1981) Microdistribution of aluminum and manganese in the tea leaf tissue as revealed by X-ray microanalyzer. Commun Soil Sci Plant Nutr 27:317–328Google Scholar
  81. Memon AR, Aktoprakligıl D, Özdemir A, ve Vertii A (2000) Heavy metal accumulation and detoxification mechanisms in plants. Turk J Bot 25:111–121Google Scholar
  82. Memon AR, Yildizhan Y, Demirel U (2006) Cu tolerance and accumulation in Brassica nigra and development of in vitro regeneration system for phytoremediation. COST action 859: phytotechnologies to promote sustainable land use and improve food safety. WG2 and WG3 workshop -omics approaches and agricultural management: driving forces to improve food quality and safety? Universite Jean Monnet et Ecole Nationale Superieure des Mines, Saint-Etienne, France, pp 37–38Google Scholar
  83. Memon AR, Yildizhan Y, Keskin BC (2008a) Enhanced Cu tolerance in Brassica nigra (L.) is associated with increased transcription level of γ-glutamylcysteine synthatase (γ-ECS) and phytochelatin synthase (PCS). COST action 859: genes and proteins involved in steps of phytoextraction and degradation of pollutants, workshop WG2: exploiting “-omics” approaches in phytotechnologies. University of Verona, Verona, Italy, p 68Google Scholar
  84. Memon AR, Yildizhan Y, Kaplan E (2008b) Metal accumulation in crops—human health issue. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 81–98Google Scholar
  85. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13Google Scholar
  86. Mirouze M, Sels J, Richard O, Czernic P, Loubet S, Jacquier A, Francois IEJA, Cammue BPA, Lebrun M, Berthomieu P, Marques L (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47:329–342Google Scholar
  87. Moreau S, Thomson RM, Kaiser BN, Trevaskis B, Guerinot ML, Udvardi MK, Puppo A, Day DA (2002) GmZIP1 encodes a symbiosis-specific zinc transporter in soybean. J Biol Chem 277:4738–4746Google Scholar
  88. Morris CA, Nicolaus B, Sampson V, Harwood JL, Kille P (1999) Identification and characterization of a recombinant metallothionein protein from a marine alga, Fucus vesiculosus. Biochem J 338:553–560Google Scholar
  89. Murphy A, Taiz L (1995) Comparison of metallothionein gene expression and non-protein thiols in 10 Arabidopsis ecotypes correlation with copper tolerance. Plant Physiol 109:1–10Google Scholar
  90. Murphy A, Zhou J, Goldsbrough PB, Taiz L (1997) Purification and immunological identification of metallothioneins 1and 2 from Arabidopsis thaliana. Plant Physiol 113:1293–1301Google Scholar
  91. Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647Google Scholar
  92. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454Google Scholar
  93. Ortiz DF, Russcitti T, McCuc KF, Ow DW (1995) Transport of metal binding peptides by HMT1, a fission yeast ABC type vacuolar membrane protein. J Biol Chem 27:4721–4728Google Scholar
  94. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper accumulation of metals in plants. Water Air Soil Pollut 184:105–126Google Scholar
  95. Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823Google Scholar
  96. 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 hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960Google Scholar
  97. Pilson-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39Google Scholar
  98. Plaza S, Tearall KL, Zhao FJ, Buchner P, McGrath SP, Hawkesford MJ (2007) Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 58:1717–1728Google Scholar
  99. Prasad MNV (2008) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USAGoogle Scholar
  100. Rauser WE (1990) Phytochelatins. Annu Rev Biochem 59:61–86Google Scholar
  101. Rauser WE (1999) Structure and function of metal chelators produced by plants; the case for organic acids, amino acids, phytin and metallothioneins. Cell Biochem Biophys 31:19–48Google Scholar
  102. Rauser WE (2000) Roots of maize seedlings retain most of their cadmium through two complexes. J Plant Physiol 156:545–551Google Scholar
  103. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375Google Scholar
  104. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediat 3:145–172Google Scholar
  105. Rigola D, Fiers M, Vurro E, Aarts MGM (2006) The heavy metal hyperaccumulator Thlaspi caerulescens expresses many species-specific genes, as identified by comparative expressed sequence tag analysis. New Phytol 170:753–766Google Scholar
  106. Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295:1–10Google Scholar
  107. Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799Google Scholar
  108. Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci 97:12356–12360Google Scholar
  109. Roosens N, Bernard C, Leplae R, Verbruggen N (2004) Evidence for copper homeostasis function of metallothionein (MT3) in the hyperaccumulator Thlaspi caerulescens. FEBS Lett 577:9–16Google Scholar
  110. Roosens NH, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222:716–729Google Scholar
  111. Roosens NHCJ, Willems G, Saumitou-Laprade P (2008) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci 13:208–215Google Scholar
  112. Rüegsegger A, Brunold C (1992) Effect of cadmium on g-glutamylcysteine synthesis in maize seedlings. Plant Physiol 99:428–433CrossRefGoogle Scholar
  113. Sahi SV, Bryant NL, Sharma NC, Singh SR (2002) Characterization of lead hyperaccumulator shrub, Sesbania drummondii. Environ Sci Technol 36:4676–4680Google Scholar
  114. Salt DE, Blaylock M, Kumar PBAN, Dushenkov S, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474Google Scholar
  115. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668Google Scholar
  116. Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inze D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci U S A 94:2745–2750Google Scholar
  117. Sanchez-Fernandez R, Emyr Davies TG, Coleman JOD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily a complete inventory. J Biol Chem 276:30231–30244Google Scholar
  118. Sarry J-E, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amerkraz B, Moulin C, Ezan E, Garin J, Bourguignon (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198Google Scholar
  119. Schat H, Ten Bookum WM (1992) Genetic control of copper tolerance in Silene vulgaris. Heredity 68:219–229Google Scholar
  120. Schneider A, Bergmann L (1995) Regulation of glutathione synthesis in suspension cultures of parsley and tobacco. Bot Acta 108:34–40Google Scholar
  121. Schröder P (2007) Exploiting plant metabolism for phytoremediation of organic xenobiotics. In: Willey N (ed) Phytoremediation: methods and reviews. Humana, New Jersey, USAGoogle Scholar
  122. Schröder P, Navarro Avino J, Azaizeh H, Golan Goldhirsh A, DiGregorio S, Komives T, Langergraber G, Lenz A, Maestri E, Memon A, Ranalli A, Sebastiani L, Smrcek S, Vanek T, Vuillemier S, Wissing F (2007) Position paper: using phytoremediation technologies to upgrade waste water treatment in Europe. Environ Sci Pollut Res Int 14:490–497Google Scholar
  123. Schröder P, Herzig R, Bojnov B, Ruttens A, Nehnevajova E, Stamatiadis S, Memon AR, Vassilev A, Caviezel M, Vangronsveld J (2008) Bioenergy to save the world—novel plants for bioenergy production. Environ Sci Pollut Res Int 15:196–204Google Scholar
  124. Shaul O, Mironov V, Burssens S, Van Montagu MV, Inze D (1996) Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronised tobacco 3Y-2 cells. Proc Natl Acad Sci U S A 93:4868–4872Google Scholar
  125. Shingu Y, Kudo T, Ohsato S, Kimura M, Ono Y, Yamaguchi I, Hamamoto H (2005) Characterization of genes encoding metal tolerance proteins isolated from Nicotiana glauca and Nicotiana tabacum. Biochem Biophys Res Commun 331:675–680Google Scholar
  126. Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623Google Scholar
  127. Stearns JC, Shah S, Glick BR (2007) Increasing plant tolerance to metals in the environment. In: Willey N (ed) Methods in biotechnology. Phytoremediation. Methods and review. vol. 23. Humana, New Jersey, pp 15–26Google Scholar
  128. Talke IN, Kramer U, Hanikenne M (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167Google Scholar
  129. Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci 97:4991–4996Google Scholar
  130. Tong YP, Kneer R, Zhu YG (2004) Vacuolar compartmentalization: a second generation approach to engineering plants for phytoremediation. Trends Plant Sci 9:7–9Google Scholar
  131. Van de Mortel JE (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147Google Scholar
  132. Vatamanuik OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci 96:7110–7115Google Scholar
  133. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richand P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of Zn and Cd and plant metal tolerance. FEBS Lett 576:306–312Google Scholar
  134. Verrier P, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159Google Scholar
  135. Vestergaard M, Matsumoto S, Nishikori S, Shiraki K, Hirata K, Takagi M (2008) Chelation of cadmium ions by phytochelatin synthase: role of the cystein-rich C-terminal. Anal Sci 24:277–281Google Scholar
  136. Wang C, Oliver DJ (1996) Cloning of the cDNA and genomic clones for glutathione synthetase from Arabidopsis thaliana and complementation of gsh2 mutant in fission yeast. Plant Mol Biol 31:1093–1104Google Scholar
  137. Wangeline AL, Burkhead JL, Hale KL, Lindblom SD, Terry N, Pilon M, Pilon-Smits EAH (2004) Overexpression of ATP sulfurylase in Indian mustard: effects on tolerance and accumulation of 12 metals. J Environ Qual 33:54–60CrossRefGoogle Scholar
  138. Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotinamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281Google Scholar
  139. Wei S, Zhou Q (2008) Trace elements in agro-ecosystems. In: Prasad MNV (ed) Trace elements as contaminants and nutrients—consequences in ecosystems and human health. Wiley, New Jersey, USA, pp 55–80Google Scholar
  140. Welch RM, Graham RD (2003) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364Google Scholar
  141. Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, McIntyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12:106–116Google Scholar
  142. Willems G, Dräger DB, Courbot M (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. Halleri (Brassicaceae) an analysis of quantitative trait loci. Genetics 176:659–674Google Scholar
  143. Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104–126Google Scholar
  144. Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653Google Scholar
  145. Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 178:315–325Google Scholar
  146. Zhou J, Goldsbrough PB (1994) Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884Google Scholar
  147. Zhou GK, Xu YF, Liu JY (2005) Characterization of a rice class II metallothionein gene: tissue expression patterns and induction in response to abiotic factors. J Plant Physiol 162:686–696Google Scholar
  148. Zhu LY, 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
  149. Zhu LH, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.TÜBİTAK, Marmara Research CenterInstitute for Genetic Engineering and BiotechnologyGebzeTurkey
  2. 2.Helmholtz-Zentrum München, German Research Center for Environmental HealthNeuherbergGermany

Personalised recommendations