Hyperaccumulators of metal and metalloid trace elements: Facts and fiction

Abstract

Background

Plants that accumulate metal and metalloid trace elements to extraordinarily high concentrations in their living biomass have inspired much research worldwide during the last decades. Hyperaccumulators have been recorded and experimentally confirmed for elements such as nickel, zinc, cadmium, manganese, arsenic and selenium. However, to date, hyperaccumulation of lead, copper, cobalt, chromium and thallium remain largely unconfirmed. Recent uses of the term in relation to rare-earth elements require critical evaluation.

Scope

Since the mid-1970s the term ‘hyperaccumulator’ has been used millions of times by thousands of people, with varying degrees of precision, aptness and understanding that have not always corresponded with the views of the originators of the terminology and of the present authors. There is therefore a need to clarify the circumstances in which the term ‘hyperaccumulator’ is appropriate and to set out the conditions that should be met when the terms are used. We outline here the main considerations for establishing metal or metalloid hyperaccumulation status of plants, (re)define some of the terminology and note potential pitfalls.

Conclusions

Unambiguous communication will require the international scientific community to adopt standard terminology and methods for confirming the reliability of analytical data in relation to metal and metalloid hyperaccumulators.

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References

  1. Anderson C, Brooks R, Chiarucci A, LaCoste C, Leblanc M, Robinson B, Simcock R, Stewart R (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415

    CAS  Google Scholar 

  2. Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Google Scholar 

  3. Azcue JM (1996) Comparison of different cleaning procedures of root material for analysis of trace elements. Int J Environ Anal Chem 62(2):137–146

    CAS  Google Scholar 

  4. Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    CAS  Google Scholar 

  5. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  6. Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994a) The possibility of in situ heavy metal decontamination of soils using crops of metal-accumulating plants. Resour Conserv Recyc 11:41–49

    Google Scholar 

  7. Baker AJM, Reeves RD, Hajar ASM (1994b) Heavy metal accumulation and tolerance in British populations of the metallophytes Thlaspi caerulescens J. and C. Presl (Brassicaceae). New Phytol 127:61–68

    CAS  Google Scholar 

  8. Baker AJM, Whiting SN (2002) In search of the Holy Grail—a further step in understanding metal hyperacumulation. New Phytol 155:1–7

    Google Scholar 

  9. Barillas JRV, Quinn CF, Pilon-Smits EAH (2011) Selenium accumulation in plants -phytotechnological applications and ecological implications. Int J Phytorem 13(1):166–178

    Google Scholar 

  10. Barry SAS, Clark SC (1978) Problems of interpreting the relationship between the amounts of lead and zinc in plants and soil on metalliferous wastes. New Phytol 81:773–783

    CAS  Google Scholar 

  11. Becquer T, Quantin C, Sicot M, Boudot J (2003) Chromium availability in ultramafic soils from New Caledonia. Sci Total Environ 301:251–261

    PubMed  CAS  Google Scholar 

  12. Bert V, Bonnin I, Saumitou-Laprade P, De Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    CAS  Google Scholar 

  13. Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18

    CAS  Google Scholar 

  14. Boyd RS, Jaffré T (2009) Elemental concentrations of eleven new caledonian plant species from serpentine soils: elemental correlations and leaf-age effects. In: Soil and biota of serpentine: a world view. Northeastern Naturalist 16 (Special Issue 5):93–110

  15. Broadley MR, Willey NJ, Wilkins JC, Baker AJM, Mead A, White PJ (2001) Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol 152:9–27

    CAS  Google Scholar 

  16. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    PubMed  CAS  Google Scholar 

  17. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland OR

  18. Brooks RR (1998) Biogeochemistry and hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford UK, pp 95–118

    Google Scholar 

  19. Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea bengalensis (Wall.) O.K. J Geochem Explor 7:295–300

    CAS  Google Scholar 

  20. Brooks RR, Lee J, Reeves RD, Jaffré T (1977a) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57

    CAS  Google Scholar 

  21. Brooks RR, McCleave JA, Schofield EK (1977b) Cobalt and nickel uptake by the Nyssaceae. Taxon 26:197–201

    Google Scholar 

  22. Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc Roy Soc Lond B 200:217–224

    CAS  Google Scholar 

  23. Brooks RR, Wither ED, Westra LYT (1978) Biogeochemical copper anomalies on Salajar Island Indonesia. J Geochem Explor 10:181–188

    CAS  Google Scholar 

  24. Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc Roy Soc Lond B 203:387–403

    CAS  Google Scholar 

  25. Brooks RR, Reeves RD, Morrison RS, Malaisse F (1980) Hyperaccumulation of copper and cobalt—a review. Bull Soc Roy Bot Belg 113:166–172

    CAS  Google Scholar 

  26. Brooks RR, Grégoire J, Madi L, Malaisse F (1982) Phytogéochimie des gisements cupro-cobaltifères de l’anticlinal de Kasonta (Shaba-Zaïre). Géo-Eco-Trop 6:219–228

    Google Scholar 

  27. Chaney RL, Brown SL, Li Y-M, Angle JS, Stuczynski TI, Daniels WL, Henry CL, Siebielec G, Malik M, Ryan JA, Compton H (2002) Progress in risk assessment for soil metals, and in-situ remediation and phytoextraction of metals from hazardous contaminated soils. In: Proc. USEPA Conf. ‘Phytoremediation: State of the Science.’ 1–2 May 2000, Boston, MA. USEPA, Washington, DC

  28. Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443

    PubMed  CAS  Google Scholar 

  29. Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    PubMed  CAS  Google Scholar 

  30. Cole MM, Provan DMJ, Tooms JS (1968) Geobotany, biogeochemistry and geochemistry in the Bulman-Waimuna Springs area, Northern Territory, Australia. Trans Inst Min Metall Sec B 77:81–104

    Google Scholar 

  31. 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 104:1052–1065

    Google Scholar 

  32. Deng D-M, Deng J-C, Li J-T, Zhang J, Hu M, Lin Z, Liao B (2008) Accumulation of zinc, cadmium, and lead in four populations of Sedum alfredii growing on lead/zinc mine spoils. J Integr Plant Biol 50:691–698

    PubMed  CAS  Google Scholar 

  33. Deram A, Petit D (1997) Ecology of bioaccumulation in Arrhenatherum elatius L. (Poaceae) populations—applications of phytoremediation of zinc, lead and cadmium contaminated soils. J Exp Bot 48:98, Special Supplement

    Google Scholar 

  34. Dunn CE (2007) New perspectives on biogeochemical exploration. Paper 12. Advances in prospect-scale geochemical methods. In: Milkereit B (ed) Proceedings of Exploration 07: Fifth decennial international conference on mineral exploration, pp 249–261

  35. Ernst WHO (2006) Evolution of metal tolerance in higher plants. For Snow Landsc Res 80(3):251–274

    Google Scholar 

  36. Escarré J, Lefèbvre C, Gruber W, Leblanc M, Lepart J, Rivière Y, Delay B (2000) Zinc and cadmium accumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437

    Google Scholar 

  37. Escarré J, Lefèbvre C, Raboyeau S, Dossantos A, Gruber W, Cleyet Marel JC, Frérot H, Noret N, Mahieu S, Collin C, Oort F (2011) Heavy metal concentration survey in soils and plants of the Les Malines mining district (southern France): implications for soil restoration. Water Air Soil Poll 216:485–504

    Google Scholar 

  38. Faucon M-P, Shutcha MN, Meerts P (2007) Revisiting copper and cobalt concentrations in supposed hyperaccumulators from SC Africa: influence of washing and metal concentrations in soil. Plant Soil 301:29–36

    CAS  Google Scholar 

  39. Feng MH, Shan XQ, Zhang S, Wen B (2005) A comparison of the rhizosphere-based method with DTPA, EDTA, CaCl2, and NaNO3 extraction methods for prediction of bioavailability of metals in soil to barley. Environ Pollut 137:231–240

    PubMed  CAS  Google Scholar 

  40. Fernando DR, Woodrow IE, Jaffré T, Dumontet V, Marshall AT, Baker AJM (2008) Foliar manganese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185

    PubMed  CAS  Google Scholar 

  41. Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJM, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Ann Bot 103:931–939

    PubMed  CAS  PubMed Central  Google Scholar 

  42. Freeman JL (2006) Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–34

    PubMed  CAS  PubMed Central  Google Scholar 

  43. Gao Y, Zhou P, Mao L, Shu W, Ye Z (2010) Phytoextraction of cadmium and physiological changes in Solanum nigrum as a novel cadmium hyperaccumulator. Russ J Plant Physiol 57:501–508

    CAS  Google Scholar 

  44. Garnier J, Quantin C, Martins E, Becquer T (2006) Solid speciation and availability of chromium in ultramafic soils from Niquelândia, Brazil. J Geochem Explor 88:206–209

    CAS  Google Scholar 

  45. Han FX, Sridhar BBM, Monts DL, Su Y (2004) Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytol 162:489–499

    CAS  Google Scholar 

  46. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroyman J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    PubMed  CAS  Google Scholar 

  47. Hobbs RH, Streit B (1986) Heavy metal concentrations in plants growing on a copper mine spoil in the Grand Canyon, Arizona. Am Midl Nat 115:277–281

    CAS  Google Scholar 

  48. Hoffmann P, Baker AJM, Proctor J, Madulid DA (2003) Phyllanthus balgooyi (Euphorbiaceae s.l.), a new nickel-hyperaccumulating species from Palawan and Sabah. Blumea 48:193–199

    Google Scholar 

  49. Jaffré T (1977) Accumulation du manganese par des especés associés aux terrains ultrabasiques de Nouvelle-Calédonie. C R Acad Sci Paris D 284:1573–1575

    Google Scholar 

  50. Jaffré T (1979) Accumulation du manganese par les Protéacées de Nouvelle-Calédonie. C R Acad Sci Paris D 289:425–428

    Google Scholar 

  51. Jaffré T (1980) Etude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle-Calédonie. Paris: Travaux et Documents de l'ORSTOM 124.

  52. Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle Calédonie, Psychotria douarrei (G. Beauvisage) Däniker. C R Acad Sci Paris D 278:1727–1730

    Google Scholar 

  53. Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580

    PubMed  Google Scholar 

  54. Jiang L, Yang X, He Z (2004) Growth response and phytoextraction of copper at different levels in soils by Elsholtzia splendens. Chemosphere 55:1179–1187

    PubMed  CAS  Google Scholar 

  55. Johnston WR, Proctor J (1977) A comparative study of metal levels in plants from two contrasting lead-mine sites. Plant Soil 46:251–257

    CAS  Google Scholar 

  56. Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halácsy. Pl Physiol 115:1641–1, 650

    Google Scholar 

  57. Krämer U (2010) Metal hyperaccumulation in plants. Ann Rev Plant Biol 61:517–534

    Google Scholar 

  58. Kubota J, Lazar VA, Beeson KC (1960) The study of cobalt status of soils in Arkansas and Louisiana using the black gum as the indicator plant. Soil Science Proceedings 24:527–528

    CAS  Google Scholar 

  59. Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    PubMed  CAS  Google Scholar 

  60. LaCoste C, Robinson BH, Brooks RR, Anderson CWN, Chiarucci A, Leblanc M (1999) The phytoremediation potential of thallium-contaminated soils using Iberis and Biscutella species. Int J Phytorem 1:327–338

    CAS  Google Scholar 

  61. Lai Y, Wang Q, Yang L, Huang B (2006) Subcellular distribution of rare earth elements and characterization of their binding species in a newly discovered hyperaccumulator Pronephrium simplex. Talanta 70:26–31

    PubMed  CAS  Google Scholar 

  62. Leblanc M, Petit D, Deram A, Robinson BH, Brooks RR (1999) The phytomining and environmental significance of hyperaccumulation of thallium by Iberis intermedia from southern France. Econ Geol 94:109–113

    CAS  Google Scholar 

  63. Leteinturier B (2002) Evaluation du potential phytocénotique des gisements cuprifères d’Afrique centro-australe en vue de la phytoremédiation de sites pollués par l’activitéminière. PhD Thesis, Faculté des Sciences Agronomiques de Gembloux, Belgium

  64. Li J-T, Deng DM, Peng GT, Deng JC, Zhang J, Liao B (2010) Successful micropropagation of the cadmium hyperaccumulator Viola baoshanensis (Violaceae). Int J Phytorem 12:761–771

    CAS  Google Scholar 

  65. Liu W, Shu W, Lan C (2004) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chinese Sci Bull 49:29–32

    CAS  Google Scholar 

  66. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20

    CAS  Google Scholar 

  67. Lombi E, Zhao F, McGrath S, Young S, Sacchi G (2001) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60

    CAS  Google Scholar 

  68. Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579

    PubMed  CAS  Google Scholar 

  69. Macnair M (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105

    CAS  Google Scholar 

  70. Malaisse F, Grégoire J, Brooks RR, Morrison RS, Reeves RD (1978) Aeolanthus biformifolius: a hyperaccumulator of copper from Zaïre. Science 199:887–888

    PubMed  CAS  Google Scholar 

  71. Malik M, Chaney RL, Brewer EP, Angle JS (2000) Phytoextraction of soil cobalt using hyperaccumulator plants. Int J Phytorem 2:319–329

    CAS  Google Scholar 

  72. Markert B (1994) Progress report on the element concentrations cadastre project (ECCP) of INTERCOL/IUBS, International Union of Biological Sciences, 25th General Assembly, Paris

  73. McGrath SP (1998) Phytoextraction for soil remediation. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford UK, pp 261–287

    Google Scholar 

  74. McGrath SP, Dunham SJ, Correll RL (1999) Potential for phytoextraction of zinc and cadmium from soils using hyperaccumulator plants. In: Terry N, Bañuelos GS (eds) Phytoremediation of contaminated soil and water. CRC Press, pp 109–128

  75. McLaughlin BE, Loon GW, Crowder AA (1985) Comparison of selected washing treatments on Agrostis gigantea samples from mine tailings near Copper Cliff, Ontario, before analysis for Cu, Ni, Fe and K content. Plant Soil 85(3):433–436

    CAS  Google Scholar 

  76. Metali F, Salim KA, Burslem DFRP (2012) Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plants. New Phytol 193:637–649

    PubMed  CAS  Google Scholar 

  77. Mohtadi A, Ghaderian SM, Schat H (2012) A comparison of lead accumulation and tolerance among heavy metal hyperaccumulating and non-hyperaccumulating metallophytes. Plant Soil 352(1–2):267–276

    CAS  Google Scholar 

  78. Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232

    PubMed  CAS  Google Scholar 

  79. Pence NS, Larsen PB, Ebbs SD, Letham DLD, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Nat Acad Sci USA 97:4956–4960

    PubMed  CAS  PubMed Central  Google Scholar 

  80. Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    CAS  Google Scholar 

  81. Pollard AJ, Stewart HS, Roberson CB (2009) Manganese hyperaccumulation in Phytolacca americana L. from the Southeastern United States. Northeast Nat 16:155–162

    Google Scholar 

  82. Rajakaruna N, Baker AJM (2006) Serpentine: a model habitat for botanical research in Sri Lanka. Ceylon J Sci 32:1–19

    Google Scholar 

  83. Redondo-Gomez S, Mateos-Naranjo E, Vecino-Bueno I, Feldman SR (2011) Accumulation and tolerance characteristics of chromium in a cordgrass Cr-hyperaccumulator, Spartina argentinensis. J Haz Mater 185:862–869

    CAS  Google Scholar 

  84. Reeves RD (1988) Nickel and zinc accumulation by species of Thlaspi L., Cochlearia L., and other genera of the Brassicaceae. Taxon 37:309–318

    Google Scholar 

  85. Reeves RD (1992) Hyperaccumulation of nickel by serpentine plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover UK, pp 253–277

    Google Scholar 

  86. Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65

    CAS  Google Scholar 

  87. Reeves RD (2005) Hyperaccumulation of trace elements by plants. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils, Proceedings of the NATO Advanced Study Institute, Třešť Castle, Czech Republic, 18–30 August 2002. NATO Science Series: IV: Earth and Environmental Sciences 68. Springer, Berlin, pp 25–52

  88. Reeves RD, Brooks RR (1983a) European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. J Geochem Explor 18:275–283

    CAS  Google Scholar 

  89. Reeves RD, Brooks RR (1983b) Hyperaccumulation of lead and zinc by two metallophytes from a mining area in Central Europe. Environ Pollut 31:277–287

    CAS  Google Scholar 

  90. Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217–224

    CAS  Google Scholar 

  91. 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 193–229

    Google Scholar 

  92. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytorem 3:145–172

    CAS  Google Scholar 

  93. Reeves RD, Ma RL, McLeod CW (2005) Lead isotope composition of some European mine and smelter soils and a possible application to hyperaccumulation studies. In: Abstracts of the 8th International Conference on the Biogeochemistry of Trace Elements, Adelaide, Australia, April 2005, pp 448–449

  94. Reeves RD, Baker AJM, Bequer T, Echevarria G, Miranda ZJC (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293:107–119

    CAS  Google Scholar 

  95. Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PLM, Smith JAC, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116

    PubMed  CAS  Google Scholar 

  96. Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56

    CAS  Google Scholar 

  97. Robinson BH, Brooks RR, Hedley MJ (1999) Cobalt and nickel accumulation in Nyssa (tupelo) species and its significance for New Zealand agriculture. NZ J Agric Res 42:235–240

    CAS  Google Scholar 

  98. Robinson BH, Kim N, Marchetti M, Moni C, Schroeter L, van den Dijssel C, Milne G, Clothier B (2006) Arsenic hyperaccumulation by aquatic macrophytes in the Taupo Volcanic Zone, New Zealand. Environ Exp Botany 58:206–215

    CAS  Google Scholar 

  99. Römkens P, Bouwman L, Japenga J, Draaisma C (2001) Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environ Pollut 116:109–121

    Google Scholar 

  100. Roosens N, Verbruggen N, Meerts P, Ximénez-Embún P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672

    CAS  Google Scholar 

  101. Rosenfeld I, Beath OA (1964) Selenium - Geobotany, Biochemistry, Toxicity and Nutrition. Academic, New York

    Google Scholar 

  102. Rotkittikhun P, Kruatrachue M, Chaiyarat R, Ngernsansaruay C, Pokethitiyook P, Paijitprapaporn A, Baker AJM (2006) Uptake and accumulation of lead by plants from the Bo Ngam lead mine area in Thailand. Environ Pollut 144:681–688

    PubMed  CAS  Google Scholar 

  103. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Phys Plant Molec Biol 49:643–668

    CAS  Google Scholar 

  104. Schat H (1999) Plant responses to inadequate and toxic micronutrient availability: General and nutrient-specific mechanisms. In: Gissel-Nielsen G, Jensen A (eds) Plant nutrition - molecular biology and genetics. Kluwer, Dordrecht, pp 311–326

    Google Scholar 

  105. Shan XQ, Wang HO, Zhang SZ, Zhou HF, Zheng Y, Yu H, Wen B (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicranopteris dichotoma. Plant Sci 165:1343–1353

    CAS  Google Scholar 

  106. Sun Y-B, Zhou Q-X, Ren L-P (2007) Growth responses of the newly-discovered Cd-hyperaccumulator Rorippa globosa and its accumulation characteristics of Cd and As under joint stress of Cd and As. Front Environ Sci Eng China 1:107–113

    Google Scholar 

  107. Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906

    CAS  Google Scholar 

  108. Swenson U, Munzinger J (2010) Revision of Pycnandra subgenus Sebertia (Sapotaceae) and a generic key to the family in New Caledonia. Adansonia 32:239–249

    Google Scholar 

  109. Talke IN, Hanikenne M, Krämer U (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 142:148–167

    PubMed  CAS  PubMed Central  Google Scholar 

  110. Tandy S, Mundus S, Yngvesson J, Bang TC, Lombi E, Schjoerring JK, Husted S (2011) The use of DGT for prediction of plant available copper, zinc and phosphorus in agricultural soils. Plant Soil 346:167–180

    CAS  Google Scholar 

  111. Tang Y-T, Qiua R-L, Zeng X-W, Ying R-R, Yu F-M, Zhou X-Y (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134

    CAS  Google Scholar 

  112. Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Ann Rev Plant Phys Plant Molec Biol 51:401–432

    CAS  Google Scholar 

  113. The Plant List (2010) Version 1. http://www.theplantlist.org/. Accessed 19 September 2011

  114. Van de Mortel JE, Almar VillAnueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Loren V, van Themaat E, Koornneef M, Aarts MGM (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 142:1127–1147

    PubMed  PubMed Central  Google Scholar 

  115. Vassil AD, Kapulnik Y, Raskin I, Salt DE (1998) The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiol 117:447–453

    PubMed  CAS  PubMed Central  Google Scholar 

  116. Visoottiviseth P, Francesconi K, Sridokchan W (2002) The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut 118:453–461

    PubMed  CAS  Google Scholar 

  117. Wang H, Shan X-Q, Wen B, Zhang S, Wang Z-J (2004) Responses of antioxidative enzymes to accumulation of copper in a copper hyperaccumulator of Commelina communis. Arch Environ Con Tox 47:1–9

    Google Scholar 

  118. Wang H, Wong MH, Lan C, Baker AJM, Qin Y, Chen G, Shu W, Ye ZH (2007) Uptake and accumulation of arsenic by 11 Pteris taxa from southern China. Environ Pollut 145:225–233

    PubMed  CAS  Google Scholar 

  119. Wang LF, Ji HB, Bai K, Li LB, Kuang TY (2006) Photosystem 2 activities of hyper-accumulator Dicranopteris dichotoma Bernh. from a light rare earth elements mine. Photosynthetica 44:202–207

    CAS  Google Scholar 

  120. Wang SL, Liao WB, Lu FQ, Liao B, Shu WS (2009) Hyperaccumulation of lead, zinc and cadmium in plants growing on a lead/zinc outcrop in Yunnan Province, China. Environ Geol 58:471–476

    CAS  Google Scholar 

  121. Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, Satake K, Takamatsu T, Tuah SJ, Osaki M (2007) Evolutionary control of leaf element composition in plants. New Phytol 174:516–523

    PubMed  CAS  Google Scholar 

  122. Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, Satake K, Tandy S, Mundus S, Yngvesson J, Bang TC, Lombi E, Schjoerring JK, Husted S (2011) The use of DGT for prediction of plant available copper, zinc and phosphorus in agricultural soils. Plant Soil 346:167–180

    Google Scholar 

  123. Wei S, Zhou Q, Koval PV (2006) Flowering stage characteristics of cadmium hyperaccumulator Solanum nigrum L. and their significance to phytoremediation. Sci Total Environ 369:441–446

    PubMed  CAS  Google Scholar 

  124. Wei Z, Hong F, Yin M, Li H, Hu F, Zhao G, Wong WJ (2005) Subcellular and molecular localization of rare earth elements and structural characterization of yttrium bound chlorophyll a in naturally grown fern Dicranopteris dichotoma. Microchem J 80:1–8

    CAS  Google Scholar 

  125. Willems G, Dräger DB, Courbot M, Godé C, Verbruggen N, Saumitou-Laprade P (2007) The genetic basis of zinc tolerance in the metalllophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674

    PubMed  CAS  PubMed Central  Google Scholar 

  126. Williams ST, McNeilly T, Wellington EHM (1977) The decomposition of vegetation growing on metal mine waste. Soil Biol Biochem 9:271–275

    CAS  Google Scholar 

  127. Wu LH, Luo Y-M, Xing XR, Christie P (2004) EDTA-enhanced phytoremediation of heavy metal-contaminated soil with Indian mustard and associated potential leaching risk. Agric Ecosyst Environ 102:307–318

    CAS  Google Scholar 

  128. Wu C, Liao B, Wang S-L, Zhang J, Li J-T (2010) Pb and Zn accumulation in a Cd-hyperaccumulator (Viola baoshanensis). Int J Phytoremediat 12:574–585

    CAS  Google Scholar 

  129. Xue SG, Chen YX, Reeves RD, Baker AJM, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399

    PubMed  CAS  Google Scholar 

  130. Zhang H, Lombi E, Smolders E, McGrath S (2004) Kinetics of Zn release in soils and prediction of Zn concentration in plants using diffusive gradients in thin films. Environ Sci Technol 38:3608–3613

    PubMed  CAS  Google Scholar 

  131. Zhang XH, Liu J, Huang HT, Chen J, Zhu Y, Wang DQ (2007) Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere 67:1138–1143

    PubMed  CAS  Google Scholar 

  132. 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 53:535–543

    PubMed  CAS  Google Scholar 

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Correspondence to Antony van der Ent.

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Responsible Editor: Fangjie Zhao.

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van der Ent, A., Baker, A.J.M., Reeves, R.D. et al. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 362, 319–334 (2013). https://doi.org/10.1007/s11104-012-1287-3

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Keywords

  • Hyperaccumulator
  • Metallophyte
  • Trace elements
  • Metal
  • Metalloid
  • Hydroponic experiments
  • Phytoextraction