Metal Hyperaccumulation and Tolerance in Alyssum, Arabidopsis and Thlaspi: An Overview

Part of the Environmental Pollution book series (EPOL, volume 21)


Toxic metals (TMs) and metalloids are natural components of environments, but elevated toxic levels and high persistence of TMs and metalloids in major compartments of the biosphere has posed various uncompromising and fatal effects on flora and fauna, and thus, has threatened the stability of the ecosystems as well. In addition, with the rapid increase in anthropological practices, a large number of TMs and metalloids ions are being added to the natural environment disrupting the ecosystem. A plethora of plant species have been identified so far to have potential for the remediation of TMs and metalloids-contaminated sites. Although, a large number of natural metal hyperaccumulator plant species from 34 different plant families including Asteraceace, Brassicaceae, Caryophyllaceae, Poaceae, Violaceae and Fabaceae has evolved the ability to take up, tolerate and accumulate exceptionally high concentrations of metals and metalloids present in the soil (and water) and, more importantly, in their aboveground biomass without visible toxicity symptoms but with 87 species classified as metal hyperaccumulators, the family Brassicaceae best represents amongst these metal-hyperaccumulator families. Of these 87 different metal-hyperaccumulator plant species in the family Brassicaceae, plant species in particular model metal hyperaccumutaor plant species Alyssum, Thlaspi and Arabidopsis have been studied extensively for their ability to hyperaccumulate, remove, destroy, degrade, sequester, transform, assimilate, metabolize or detoxify majority of TMs and metalloids in varied environmental compartments. Additionally, significant technological advancements in varied scientific fields have now deciphered important physiological and molecular mechanisms of TMs- and metalloids-remediation processes/intricacies in metal hyper accumulating plant species. Based on the plethora of recent published reports the current chapter critically discusses important strategies adopted by Alyssum, Arabidopsis and Thlaspi for TMs- and metalloids-hyperaccumulation/remediation and tolerance.


Alyssum Arabidopsis Thlaspi Remediation Tolerance Toxic metals Metalloids 



NAA (SFRH/BPD/64690/2009), IA, MP, ACD and EP are grateful to the Portuguese Foundation for Science and Technology (FCT) and the Aveiro University Research Institute/Centre for Environmental and Marine Studies (CESAM) for partial financial supports. SSG, SU, PT, GS and NAK would like to acknowledge the receipt of funds from DBT, DST and UGC, Govt. of India, New Delhi. Authors apologize if some references related to the main theme of the current chapter could not be cited due to space constraint.


  1. Aboudrar W, Schwartz C, Benizri E, Morel JL, Boularbah A (2007) Soil microbial diversity as affected by the rhizosphere of the hyperaccumulator Thlaspi caerulescens under natural conditions. Int J Phytorem 9:41–52Google Scholar
  2. Abou-Shanab RAI, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224Google Scholar
  3. Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate, and high Ni soils. Soil Biol Biochem 38:2882–2889Google Scholar
  4. Alford ER, Pilon-Smits EAH, Paschke MW (2010) Metallophytes – a view from the rhizosphere. Plant Soil 337:33–50Google Scholar
  5. Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci BioTechnol 3:71–90Google Scholar
  6. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trend Biotechnol 25:356–362Google Scholar
  7. Asemaneh T, Ghaderian SM, Crawford SA, Marshall AT, Baker AJM (2006) Cellular and subcellular compartmentation of Ni in the Eurasian serpentine plants Alyssum bracteatum, Alyssum murale (Brassicaceae) and Cleome heratensis (Capparaceae). Planta 225:193–290Google Scholar
  8. Assunção AGL, Martins PD, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226Google Scholar
  9. Assunção 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
  10. Baker AJM (1981) Accumulators and excluders ‐strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654Google Scholar
  11. 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
  12. 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
  13. Baker AJM, Whiting SN (2002) In search of the Holy Grail–a further step in understanding metal hyperaccumulation? New Phytol 155:1–4Google Scholar
  14. Baker AJM, McGrath SP, Reeves DR, Smith JAC (2000) Metal hyperaccumulators plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC Press LLC, Boca Raton, pp 85–107Google Scholar
  15. Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, Mengoni A (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microb Ecol 53:306–316Google Scholar
  16. Becerra-Castro C, Monterroso C, García-Lestón M, Prieto-Fernández A, Acea MJ, Kidd PS (2009) Rhizosphere microbial densities and trace metal tolerance of the nickel hyperaccumulator Alyssym serpyllifloium subsp. lusitanicum. Int J Phytoremediation 11:525–541Google Scholar
  17. 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
  18. Bernal MP, McGrath SP (1994) Effects of pH and heavy-metal concentrations in solution culture on the proton release, growth and elemental composition of Alyssum murale and Raphanus sativus L. Plant Soil 166:83–92Google Scholar
  19. Bernal MP, McGrath SP, Miller AJ, Baker AJM (1994) Comparison of the chemical changes in the rhizosphere of the nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus. Plant Soil 164:251–259Google Scholar
  20. 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
  21. Blaylock MJ, Huang JW (2000) Phytoextraction of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, pp 53–70Google Scholar
  22. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702Google Scholar
  23. Brooks RR (ed) (1998) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, p 384Google Scholar
  24. Brooks RR, Lee J, Reeves RD, Jaffrré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57Google Scholar
  25. Brown SL, Chaney RL, Angle JS, Baker AJM (1994) Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc and cadmium-contaminated soil. J Environ Qual 23:1151–1157Google Scholar
  26. Burd GI, Dixon DG, Glick BR (2000) Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245Google Scholar
  27. 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
  28. Canovas N, Vooijs R, Schat H, de Lorenzo V (2004) The role of thiol species in the hypertolerance of Aspergillus sp. P37 to arsenic. J Biol Chem 279:51234–51240Google Scholar
  29. Chaney R, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279–284Google Scholar
  30. Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390Google Scholar
  31. 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
  32. Clemens S (2001) Molecular mechanisms of plant metal hoemostatsis. Planta 212:475–486Google Scholar
  33. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719Google Scholar
  34. 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
  35. Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315Google Scholar
  36. Cobbett CS (2000) Phytochelatin biosynthesis and function in heavymetal detoxification. Curr Opin Plant Biol 3:211–216Google Scholar
  37. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins, roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182Google Scholar
  38. 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, pp 1–22. ISNN 1543-8120. open access
  39. Cobbett CS, Hussain D, Haydon MJ (2003) Structural and functional relationships between type 1 B heavy metal transporting P-type ATPases in Arabidopsis. New Phytol 159:315–321Google Scholar
  40. Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330Google Scholar
  41. Coupe SA, Taylor JE, Roberts JA (1995) Characterization of an mRNA encoding a metallothionein-like protein that accumulates during ethylene-promoted abscission of Sambucus nigra L. Planta 197:442–447Google Scholar
  42. 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
  43. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat JF, Walker EL (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349Google Scholar
  44. Dechamps C, Noret N, Mozek R, Draye X, Meerts P (2008) Root allocation in metal-rich patch by Thlaspi caerulescens from normal and metalliferous soil – new insights into the rhizobox approach. Plant Soil 310:211–224Google Scholar
  45. Delhaize E, Kataoka T, Hebb DM, White RG, Ryan PR (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15:1131–1142Google Scholar
  46. Delorme TA, Gagliardi JV, Angle JS, Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J. & C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can J Microbiol 47:773–776Google Scholar
  47. DiDonato RJ Jr, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis YELLOW STRIPE-LIKE2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414Google Scholar
  48. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869Google Scholar
  49. 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
  50. Dräger DB, Desbrosses-Fonrouge AG, Krach C, Chardonnens AN, Meyer RC, Saumitou-Laprade P, Krämer U (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins cosegregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439Google Scholar
  51. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205Google Scholar
  52. Ebbs S, Lau I, Ahner B, Kochian L (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescences (J. and C. Presl). Planta 214:635–640Google Scholar
  53. Eide D, Broderius M, Fett J, Guerinoy ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci U S A 93:5624–5628Google Scholar
  54. Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143Google Scholar
  55. Filatov V, Dowdle J, Smirnoff N, Ford-Lloyd B, Newbury HJ, Macnair M (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
  56. Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278Google Scholar
  57. Garbisu C, Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Eur J Miner Proc Environ Protect 3:58–66Google Scholar
  58. Garcìa-Hernàndez M, Murphy A, Taiz L (1988) Metallothioneins 1 and 2 have distinct but overlapping expression patterns in Arabidopsis. Plant Physiol 118:387–397Google Scholar
  59. Gasic K, Korban S (2007) Expression of Arabidopsis phytochelatin synthase in Indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta 225:1277–1285Google Scholar
  60. Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL et al (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194Google Scholar
  61. Gekeler W, Grill E, Winnacker EL, Zenk MH (1989) Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. J Naturforsch Teil 44C:361–369Google Scholar
  62. Gendre D, Czernic P, Conéjéro G, Pianelli K, Briat J-F, Lebrun M, Mari S (2007) TcYSL3, a member of the YSL gene family from the hyperaccumulator specie Thlaspi caerulescens, encodes a nicotinamine-Ni/Fe transporter. Plant J 49:1–15Google Scholar
  63. Ghaderian YSM, Lyon AJE, Baker AJM (2000) Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp. New Phytol 146:219–224Google Scholar
  64. Gong JM, Lee DA, Schroeder JI (2003) Long-distance root-toshoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci U S A 100:10118–10123Google Scholar
  65. Gonzaga MI, Ma LQ, Santos JA, Matias MI (2009) Rhizosphere characteristics of two arsenic hyperaccumulating Pteris ferns. Sci Total Environ 407:4711–4716Google Scholar
  66. Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561:22–28Google Scholar
  67. Grill E, Winnacker E-L, Zenk MH (1985) Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230:674–676Google Scholar
  68. Grill E, Loffler S, Winnacker E-L, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific g-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842Google Scholar
  69. Grotz N, Fox TC, Connolly E, Park W, Gurinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci U S A 95:7220–7224Google Scholar
  70. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465:190–198Google Scholar
  71. Guo WJ, Bundithya W, Goldsbrough PB (2003) Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytol 159:369–381Google Scholar
  72. Guo W, Meetam M, Goldsbrough PB (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706Google Scholar
  73. Ha S-B, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1164Google Scholar
  74. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11Google Scholar
  75. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613Google Scholar
  76. Hammond JP, Bowen HC, White PJ, Mills V, Pyke K, Baker AJM, Whiting SN, May ST, Broadley MR (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260Google Scholar
  77. Hannikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymanns J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–396Google Scholar
  78. Hanson B, Garifullina GF, Hanson B, Garifullina GF, Lindblom SD, Wangeline A et al (2003) Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol 159:461–469Google Scholar
  79. Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63Google Scholar
  80. Hassinen VH, Tervahauta AI, Halimaa P, Plessl M, Peraniemi S, Schat H, Aarts MGM, Servomaa K, Karenlampi SO (2007) Isolation of Zn-responsive genes from two accessions of the hyperaccumulator plant Thlaspi caerulescens. Planta 225:977–989Google Scholar
  81. Hassinen VH, Tuomainen M, Peräniemi S, Schat H, Kärenlampi SO, Tervahauta AI (2009) Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. J Exp Bot 60:187–196Google Scholar
  82. Hernandez-Allica J, Garbisu C, Becerril JM, Barrutia O, Garcia-Plazaola JI, Zhao FJ, McGrath SP (2006) Synthesis of low molecular weight thiols in response to Cd exposure in Thaspi caerulescens. Plant Cell Environ 29:1422–1429Google Scholar
  83. 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
  84. Howden R, Cobbett CS (1992) Cadmium sensitive mutants of Arabidopsis thaliana. Plant Physiol 100:100–107Google Scholar
  85. Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995) A cadmium-sensitive, glutathionedeficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073Google Scholar
  86. Hsieh HM, Liu WK, Huang PC (1995) A novel stress-inducible metallothionein-like gene from rice. Plant Mol Biol 28:381–389Google Scholar
  87. Huitson SB, Macnair MR (2003) Does zinc protect the zinc hyperaccumulator Arabidopsis halleri from herbivory by snails? New Phytol 159:453–459Google Scholar
  88. Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPases heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339Google Scholar
  89. Idris R, Trifinova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677Google Scholar
  90. Kamińska J, Moniuszko G, Gaganidze D, Aarts MGM, Sirko A (2008) Effects of ectopic expression of cDNAs from Thlaspi caerulescens on accumulation of heavy metals in tobacco plants. In: Furini A et al (eds) Genes and proteins involved in limiting steps of phytoextraction and degradation of pollutants, COST Action 859. University of Verona, Verona, pp 13–14Google Scholar
  91. Kawashima I, Kennedy TD, Chino M, Lane BG (1992) Wheat E, metallothionein enes: like mammalian Zn2+ metallothionein genes, wheat ZnA metallothionein genes are conspicuously expressed during embryogenesis. Eur J Biochem 209:971–976Google Scholar
  92. Kerkeb L, Krämer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724Google Scholar
  93. Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932Google Scholar
  94. Kohler A, Blaudez D, Chalot M, Martin F (2004) Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytol 164:83–93Google Scholar
  95. Kondo N, Imai K, Isobe M, Goto T, Murasugi A, Wada-Nakagawa C, Hayashi Y (1984) Cadystin A and B, major unit peptides comprising cadmium-binding peptides induced in a fission yeast – separation, revision of structures and synthesis. Tetrahedron Lett 25:3869–3872Google Scholar
  96. Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16:133–141Google Scholar
  97. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534Google Scholar
  98. Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638Google Scholar
  99. Kramer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Physiol Plant 115:1641–1650Google Scholar
  100. Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speculation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353Google Scholar
  101. Krämer U, Talke IN, Hannikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272Google Scholar
  102. Küpper H, Kochian LV (2009) Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytol 185:114–129Google Scholar
  103. Küpper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311Google Scholar
  104. Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84Google Scholar
  105. Küpper H, Aravind P, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to Cd-stress in the Cd hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674Google Scholar
  106. Larsson E, Asp H, Bornman J (2002) Influence of prior Cd(2+)-exposure on the uptake of Cd(2+) and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana. J Exp Bot 53:447–453Google Scholar
  107. Lasat MM, Kochian LV (2000) Physiology of Zn hyperaccumulation in Thlaspi caerulescens. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 159–169Google Scholar
  108. Lasat MM, Baker AJM, Kochain LV (1996) Physiological characterisation of root Zn2+ absorption and translocation to shoots in Zn hyperaccumulator and non-accumulator species of Thlaspi. Plant Physiol 112:1715–1722Google Scholar
  109. Lasat MM, Baker AJM, Kochain LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883Google Scholar
  110. Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochaian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–79Google Scholar
  111. Ledger SE, Gardner RC (1994) Cloning and characterization of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinidia deliciosa var. deliciosa). Plant Mol Biol 25:877–886Google Scholar
  112. Lee J, Reeves RD, Brooks RR, Jaffré T (1978) The relation between nickel and citric acid in some nickel-accumulating plants. Phytochemistry 17:1033–1035Google Scholar
  113. Lee S, Petros D, Moon JS, Ko T-S, Goldsbrough PB, Korban SS (2003a) Higher levels of ectopic expression of Arabidopsis phytochelatin synthase do not lead to increased cadmium tolerance and accumulation. Plant Physiol Biochem 41:903–910Google Scholar
  114. Lee S, Moon JS, Ko T-S, Petros D, Goldsbrough PB, Korban SS (2003b) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–663Google Scholar
  115. Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277:5360–5368Google Scholar
  116. Li Y, Dankher OP, Carreira L, Smith AP, Meagher RB (2006) The shoot-specific expression of γ-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol 141:288–298Google Scholar
  117. Li YM, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115Google Scholar
  118. Liu G-Y, Zhang Y-X, Chai T-Y (2011) Phytochelatin synthase of Thlaspi caerulescens enhanced tolerance and accumulation of heavy metals when expressed in yeast and tobacco. Plant Cell Rep 30:1067–1076Google Scholar
  119. Lodewyckx C, Mergeay M, Vangronsveld J, Clijsters H, Van Der Lelie D (2002) Isolation, characterization, and identification of bacteria associated with the zinc hyperaccumulator Thlaspi caerulescens subsp calaminaria. Int J Phytoremediation 4:101–115Google Scholar
  120. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20Google Scholar
  121. Long XX, Yang XE, Ni WZ (2002) Current status and perspective on phytoremediation of heavy metal polluted soils. J Appl Ecol 13:757–762Google Scholar
  122. Luo YM, Christie P, Baker AJM (2000) Soil solution Zn and pH dynamics in non-rhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cd contaminated soil. Chemosphere 41:161–164Google Scholar
  123. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736Google Scholar
  124. Ma Y, Rajkumar M, Freitas H (2009) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J Hazard Mater 166:1154–1161Google Scholar
  125. Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc R Soc Biol Sci 266:2175–2179Google Scholar
  126. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13Google Scholar
  127. Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Gene 39:1156–1161Google Scholar
  128. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038Google Scholar
  129. McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282Google Scholar
  130. McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159Google Scholar
  131. McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214Google Scholar
  132. McIntyre T (2003) Phytoremediation of heavy metals from soils. Adv Biochem Eng Biotechnol 78:97–123Google Scholar
  133. Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162Google Scholar
  134. Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231Google Scholar
  135. Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Environ Sci Pollut Res 16:162–175Google Scholar
  136. Mench M, Schwitzguébel JP, Schroeder P, Bert V, Gawronski S, Gupta S (2009) Assessment of successful experiments and limitations of phytotechnologies: contaminant uptake, detoxification and sequestration, and consequences for food safety. Environ Sci Pollut Res 16:876–900Google Scholar
  137. Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase in the Zn/Co/Cd/Pb subclass. Plant J 35:164–176Google Scholar
  138. Mills RF, Francini A, da Rocha PSCF, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P-1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791Google Scholar
  139. Milner MJ, Kochian LV (2008) Investigating heavy metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13Google Scholar
  140. Morita Y, Kodama K, Shiota S, Mine T, Kataoka A, Mizushima T, Tsuchiya T (1998) NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 42:1778–1782Google Scholar
  141. 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
  142. 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
  143. 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
  144. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper accumulation of metals in plants. Water Air Soil Pollut 184:105–126Google Scholar
  145. Pal R, Rai JPN (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160:945–963Google Scholar
  146. Palmgren MG, Clemens S, Williams LE, Krmer U, Borg S, Schjørrings JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trend Plant Sci 13:464–473Google Scholar
  147. Papoyan A, Kochain LV (2004) Indentification 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
  148. Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochain LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 95:4956–4960Google Scholar
  149. Persans MW, Yan X, Patnoe J-MML, Krämer U, Salt DE (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Hálácsy). Plant Physiol 121:1117–1126Google Scholar
  150. Pilson-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39Google Scholar
  151. 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
  152. Pollard AJ, Powell KD, Harper FA, Smith JA (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566Google Scholar
  153. Puschenreiter M, Schnepf A, Millan IM, Fitz WJ, Horak O, Klepp J, Schrefl T et al (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 271:205–218Google Scholar
  154. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181Google Scholar
  155. 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
  156. 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
  157. Rauser WE (2000) Roots of maize seedlings retain most of their cadmium through two complexes. J Plant Physiol 156:545–551Google Scholar
  158. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375Google Scholar
  159. 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 193–229Google Scholar
  160. Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PL, Smith JA, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116Google Scholar
  161. Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295:1–10Google Scholar
  162. Robinson B, Mills T, Petit D, Fung L, Green S, Clothier B (2000) Natural and induced cadmium-accumulation in poplar and willow: implications for phytoremediation. Plant Soil 227:301–306Google Scholar
  163. 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
  164. Roosens NH, 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
  165. 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
  166. Roosens NH, Willems G, Saumitou-Laprade P (2008) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trend Plant Sci 13:208–215Google Scholar
  167. Saier MH Jr, Trevors JT (2010) Phytoremediation. Water Air Soil Pollut 205(Suppl 1):S61–S63Google Scholar
  168. Salt DE, Kramer U (2000) Mechanisms of metal hyperaccumulation in plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 231–245Google Scholar
  169. 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
  170. Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717Google Scholar
  171. 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
  172. Schat H, Llugany M, Berhard R (2000) Metal specific patterns of tolerance, uptake and transport of heavy metals in hyperaccumulating and non-hyperaccumulating metallophytes. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soils and water. CRC Press, Boca Raton, pp 171–188Google Scholar
  173. Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM (2002) The role of phytochelatins in constitutive and adaptive heavy metal tolerance in hyperaccumulator and non-hyperaccumulator metallophytes. J Exp Bot 53:2381–2392Google Scholar
  174. Schwartz C, Morel JL, Saumier S, Whiting SN, Baker AJM (1999) Root development of the zinc-hyperaccumulator Thlaspi caerulescens is affected by metal origin, content and localization in the soil. Plant Soil 208:103–115Google Scholar
  175. Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35Google Scholar
  176. Shah K, Nongkynrih JM (2007) Metal hyperaccumulation and bioremediation. Biol Plant 51:618–634Google Scholar
  177. Shanmugam V, Lo J-C, Wu C-L, Wang S-L, Lai C-C, Connolly EL et al (2011) Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana – the role in zinc tolerance. New Phytol 190:125–137Google Scholar
  178. Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906Google Scholar
  179. Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl Microbiol Biotechnol 61:405–412Google Scholar
  180. 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
  181. Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948Google Scholar
  182. 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
  183. van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD et al (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
  184. van de Mortel JE, Schat H, Moerland PD, Loren V, van Themaat E, van der Ent S et al (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324Google Scholar
  185. van der Zaal BJ, Neuteboom LW, Pinas JE, Chardonnens AN, Schat H, Verkleij JAC, Hooykaas PJJ (1999) Overexpression of a novel Arabidopsis gene related to putative zinc-transporter genes from animals can lead to enhanced zinc resistance and accumulation. Plant Physiol 119:1047–1056Google Scholar
  186. Vatamaniuk OK, Mari S, Lu YP, Rea PA (1999) AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci U S A 96:7110–7115Google Scholar
  187. Vazquez MD, Poschenrieder C, Barcelo J, Baker AJM, Hatton P, Cope GH (1994) Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens J & C Presl. Bot Acta 107:243–250Google Scholar
  188. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776Google Scholar
  189. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312Google Scholar
  190. Verret F, Gravot A, Auroy P, Preveral S, Forestier C, Vavasseur A, Richaud P (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His(11) stretch. FEBS Lett 579:1515–1522Google Scholar
  191. Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337Google Scholar
  192. Weber M, Harada E, Vess C, Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281Google Scholar
  193. Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963Google Scholar
  194. 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 York, pp 55–80Google Scholar
  195. Weis J, Weis P (2004) Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environ Int 30:685–700Google Scholar
  196. Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408Google Scholar
  197. Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123:131–138Google Scholar
  198. Wenzel WW, Lombi E, Adriano DC (2004) Root and rhizosphere processes in metal hyperaccumulation and phytoremediation technology. In: Prasad MNV (ed) Heavy metal stress in plants from biomolecules to ecosystems, 2nd edn. Springer, Berlin, pp 313–344Google Scholar
  199. White PJ, Whitingm SN, Baker AJM, Broadley MR (2002) Does zinc move apoplastically to the xylem in roots of Thlaspi caerulescens? New Phytol 153:201–207Google Scholar
  200. Whiting SN, Leake JR, McGrath SP, Baker AJM (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol 145:199–210Google Scholar
  201. Whiting SN, de Souza MP, Terry N (2001) Rhizosphere bacteria mobilize Zn for hyperaccumulation by Thlaspi caerulescens. Environ Sci Technol 35:3144–3150Google Scholar
  202. Wieshammer G, Unterbrunner R, Garcia TB, Zivkovic MF, Puschenreiter M, Wenzel WW (2007) Phytoextraction of Cd and Zn from agricultural soils by Salix ssp. and intercropping of Salix caprea and Arabidopsis halleri. Plant Soil 298:255–264Google Scholar
  203. Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta Biomembr 1465:104–126Google Scholar
  204. 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
  205. Wójcik M, Vangronsveld J, Tukiendorf A (2005a) Cadmium tolerance in Thlaspi caerulescens I. Growth parameters, metal accumulation and phytochelatin synthesis in response to cadmium. Environ Exp Bot 53:151–161Google Scholar
  206. Wójcik M, Vangronsveld J, D’Haen J, Tukiendorf A (2005b) Cadmium tolerance in Thlaspi caerulescens II. Localization of cadmium in Thlaspi caerulescens. Environ Exp Bot 53:163–171Google Scholar
  207. Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78Google Scholar
  208. Wu J, Zhao F-J, Ghandilyan A, Logoteta B, Guzman M, Schat H et al (2009) Identification and functional analysis of two ZIP metal transporters of the hyperaccumulator Thlaspi caerulescens. Plant Soil 325:79–95Google Scholar
  209. Wycisk K, Kimb EJ, Schroeder JI, Krämer U (2004) Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett 578:128–134Google Scholar
  210. Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574Google Scholar
  211. Xie HL, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318:205–215Google Scholar
  212. 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
  213. Xiong J, He Z, Liu D, Mahmood Q, Yang X (2008) The role of bacteria in the heavy metals removal and growth of Sedum alfredii Hance in an aqueous medium. Chemosphere 70:489–904Google Scholar
  214. Yang X, Feng Y, He Z, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353Google Scholar
  215. Yazaki K, Sugiyama A, Morita M, Shitan N (2008) Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochem Rev 7:513–524Google Scholar
  216. Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514Google Scholar
  217. Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620Google Scholar
  218. Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543Google Scholar
  219. Zhou J, Goldsbrough PB (1994) Functional homologues of fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884Google Scholar
  220. 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
  221. Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmium and are required for cadmium tolerance and accumulation. Plant Mol Biol 58:839–855Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Plant Molecular Biology GroupInternational Centre for Genetic Engineering and BiotechnologyNew DelhiIndia
  2. 2.Stress Physiology and Molecular Biology Lab, Centre for BiotechnologyMD UniversityRohtakIndia
  3. 3.Centre for Environmental and Marine Studies (CESAM) & Department of ChemistryUniversity of AveiroAveiroPortugal
  4. 4.Centre for Environmental and Marine Studies (CESAM) & Department of Chemistry and BiologyUniversity of AveiroAveiroPortugal
  5. 5.Department of Environmental SciencePeriyar UniversitySalemIndia
  6. 6.Department of Plant Biotechnology, School of BiotechnologyMadurai Kamaraj UniversityMaduraiIndia
  7. 7.Centre for Environmental and Marine Studies (CESAM) & Department of BiologyUniversity of AveiroAveiroPortugal
  8. 8.Department of Botany, Faculty of ScienceHamdard UniversityNew DelhiIndia
  9. 9.Department of Botany, Faculty of Life SciencesAligarh Muslim UniversityAligarhIndia

Personalised recommendations