Skip to main content
Log in

Metal ion ligands in hyperaccumulating plants

  • Minireview
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

Metal-hyperaccumulating plants have the ability to take up extraordinary quantities of certain metal ions without succumbing to toxic effects. Most hyperaccumulators select for particular metals but the mechanisms of selection are not understood at the molecular level. While there are many metal-binding biomolecules, this review focuses only on ligands that have been reported to play a role in sequestering, transporting or storing the accumulated metal. These include citrate, histidine and the phytosiderophores. The metal detoxification role of metallothioneins and phytochelatins in plants is also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Scheme 1
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

Ala:

Alanine

Arg:

Arginine

Asn:

Asparagine

Asp:

Aspartic acid

Cys:

Cysteine

EXAFS:

Extended X-ray absorption fine structure spectroscopy

Gln:

Glutamine

Glu:

Glutamic acid

Gly:

Glycine

His:

Histidine

Ile:

Isolucine

Leu:

Leucine

Lys:

Lysine

MT:

Metallothionein

NA:

Nicotianamine

NAAT:

Nicotianamine aminotransferase

NAS:

Nicotianamine synthase

NiCoTs:

Ni/Cobalt transporters

PC:

Phytochelatin

Phe:

Phenylalanine

Pro:

Proline

PS:

Phytosiderophores

SAM:

S-adenosyl-methionine

Ser:

Serine

Thr:

Threonine

Tyr:

Tyrosine

Val:

Valine

XAS:

X-ray absorption spectroscopy

References

  1. Anderson C, Deram A, Petit D, Brooks R, Stewart R, Simcock R (2001) In: Iskandar IK, Kirkham MB (eds) Trace elements in soil: bioavailability, flux, and transfer. Lewis, Washington DC, pp 63–76

  2. Reeves RD, Baker AJM (2000) In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals. Wiley, New York, pp 193–229

  3. Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Science 193:579–580

    Article  PubMed  Google Scholar 

  4. Bollard EG (1983) In: Lauchli A, Bielsky RL (eds) Inorganic plant nutrition (Encyclopedia of plant physiology, vol 15B). Springer, Berlin Heidelberg New York, pp 695–744

  5. Perrier N, Colin F, Jaffré T, Ambrosi J, Rose J, Bottero J (2004) CR Geoscience 336:567–577

    Article  CAS  Google Scholar 

  6. Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Phytochemistry 47:339–347

    Article  PubMed  CAS  Google Scholar 

  7. Reeves RD, Baker AJM, Borhidi A, Berazain R (1996) New Phytol 133:217–224

    Article  CAS  Google Scholar 

  8. Baker AJM (1981) J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  9. McGrath SP, Dunham SJ, Correll RL (1999) In: Terry N, Bañuelos GS (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL, pp 109–128

  10. Salt DE, Krämer U (2000) In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals. Wiley, New York, pp 231–246

  11. Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Nature 379:635–638

    Article  Google Scholar 

  12. Brown SL, Chaney RL, Angle JS, Baker AJM (1994) J Environ Qual 23:1151–1157

    Article  CAS  Google Scholar 

  13. McGrath SP, Shen ZG, Zhao FJ (1997) Plant Soil 188:153–159

    Article  CAS  Google Scholar 

  14. Reeves RD, Baker AJM (1984) New Phytol 98:191–204

    Article  CAS  Google Scholar 

  15. Hanson B, Lindblom SD, Loeffler ML, Pilon-Smits EAH (2004) New Phytol 162:655–662

    Article  CAS  Google Scholar 

  16. Boyd RS (1998) In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB Int., Oxford, pp 181–201

  17. Mesjasz-Przybylowicz J, Przybylowicz WJ (2001) S Afr J Sci 97:596–598

    CAS  Google Scholar 

  18. Davis MA, Boyd RS, Cane JH (2001) S Afr J Sci 97:554–557

    CAS  Google Scholar 

  19. Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Plant Physiol 137:1082–1091

    Article  PubMed  CAS  Google Scholar 

  20. Clemens S, Palmgren MG, Krämer U (2002) Trends Plant Sci 7:309–315

    Article  PubMed  CAS  Google Scholar 

  21. Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Plant Cell 16:2176–2191

    Article  PubMed  CAS  Google Scholar 

  22. Whiting SN, de Souza MP, Terry N (2001) Environ Sci Technol 35:3144–3150

    Article  PubMed  CAS  Google Scholar 

  23. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London

  24. Römheld V, Marschner H (1986) Plant Physiol 80:175–180

    PubMed  Google Scholar 

  25. Rengel Z (1999) In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, Berlin Heidelberg New York, pp 231–251

  26. Reichman SM, Parker DR (2005) In: Huang PMG, G (ed) Biogeochemistry of trace elements in the rhizosphere. Elsevier, Toronto

  27. Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Environ Pollut 123:131–138

    Article  PubMed  CAS  Google Scholar 

  28. Zhao FJ, Hamon RE, McLaughlin MJ (2001) New Phytol 151:613–620

    Article  CAS  Google Scholar 

  29. Salt DE, Kato N, Krämer U, Smith RD, Raskin I (2000) In: Terry N, Bañuelos GS (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL, pp 189–200

  30. Lasat MM, Baker AJM, Kochian LV (1996) Plant Physiol 112:1715–1722

    PubMed  CAS  Google Scholar 

  31. Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) Plant Physiol 115:1641–1650

    PubMed  Google Scholar 

  32. Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Environ Sci Technol 33:713–717

    Article  CAS  Google Scholar 

  33. Finney LA, O’Halloran TV (2003) Science 300:931–936

    Article  PubMed  CAS  Google Scholar 

  34. Fraser KA, Long HA, Candlin R, Harding MM (1965) Chem Comm 15:344–345

    Google Scholar 

  35. Deschamps P, Kulkarni PP, Gautam-Basak M, Sarkar B (2005) Coord Chem Rev 249:895–909

    Article  CAS  Google Scholar 

  36. Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Plant Physiol 122:1343–1353

    Article  PubMed  Google Scholar 

  37. Kameda Y, Ito E, Takeshita A, Nakazawa R, Takenaga H (2002) Tokyo Nogyo Daigaku Nogaku Shuho 47:45–48

    CAS  Google Scholar 

  38. Kerkeb L, Krämer U (2003) Plant Physiol 131:716–724

    Article  PubMed  CAS  Google Scholar 

  39. Wycisk K, Kim EJ, Schroeder JI, Krämer U (2004) FEBS Lett 578:128–134

    Article  PubMed  CAS  Google Scholar 

  40. Persans MW, Yan X, Patnoe J-MML, Krämer U, Salt DE (1999) Plant Physiol 121:1117–1126

    Article  PubMed  CAS  Google Scholar 

  41. Ingle RA, Mugford ST, Rees JD, Campbell MM, Smith JAC (2005) Plant Cell 17:2089–2106

    Article  PubMed  CAS  Google Scholar 

  42. Terry N, Bañuelos GS (1999) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL

    Google Scholar 

  43. Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann J-L, Traverse A, Marcus Matthew A, Manceau A (2002) Plant Physiol 130:1815–1826

    Article  PubMed  CAS  Google Scholar 

  44. Qiu R-L, Tang Y-T, Fang X-H, Chaney RL, Li Y-M, Angle JS, Liu W, Zeng X-W (2004) Zhongshan Daxue Xuebao, Ziran Kexueban 43:144–149

    Google Scholar 

  45. de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Chemosphere 55:1159–1168

    Article  PubMed  CAS  Google Scholar 

  46. Shan X, Wang H, Zhang S, Zhou H, Zheng Y, Yu H, Wen B (2003) Plant Sci 165:1343–1353

  47. de la Rosa G, Gardea-Torresdey JL, Peralta-Videa JR, Parsons JG, Montes M (2003) ACS National Meeting, Division of Environmental Chemistry 43:601–606

    Google Scholar 

  48. Boominathan R, Doran PM (2003) J Biotechnol 101:131–146

    Article  PubMed  CAS  Google Scholar 

  49. Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Funct Plant Biol 29:899–905

    Article  CAS  Google Scholar 

  50. Memon AR, Yatazawa M (1984) J Plant Nutr 7:961–974

    CAS  Google Scholar 

  51. Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Plant Cell Environ 23:507–514

    Article  CAS  Google Scholar 

  52. Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck Peter MH (2004) Plant Physiol 134:748–757

    Article  PubMed  CAS  Google Scholar 

  53. Schaumlöffel D, Ouerdane L, Bouyssiere B, Lobinski R (2003) J Anal Atom Spectrom 18:120–127

    Article  CAS  Google Scholar 

  54. Lee J, Reeves RD, Brooks RR, Jaffré T (1978) Phytochemistry 17:1033–1035

    Article  CAS  Google Scholar 

  55. Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Kumashiro T, Nagata T, Ohata T, Mori S (1989) Biol Met 2:142–145

    Article  CAS  Google Scholar 

  56. Higuchi K, Kanazawa K, Nishizawa N-K, Chino M, Mori S (1994) Plant Soil 165:173–179

    Article  CAS  Google Scholar 

  57. Noma M, Noguchi M, Tamaki E (1971) Tetrahedron Lett 22:2017–2020

    Article  Google Scholar 

  58. Kristensen I, Larsen PO (1974) Phytochemistry 13:2791–2798

    Article  CAS  Google Scholar 

  59. Nomoto K, Mino Y, Ishida T, Yoshioka H, Ota N, Inoue M, Takagi S, Takemoto T (1981) Chem Comm 7:338–339

    Article  Google Scholar 

  60. Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) Biometals 9:84–90

    Article  CAS  Google Scholar 

  61. Douchkov D, Herbik A, Koch G, Mock HP, Melzer M, Stephan UW, Baeumlein H (2002) Plant Soil 241:115–119

    Article  CAS  Google Scholar 

  62. Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa Naoko K (2003) Plant Cell 15:1263–1280

    Article  PubMed  Google Scholar 

  63. Scholz G, Schlesier G, Seifert K (1985) Physiol Plant 63:99–104

    Article  CAS  Google Scholar 

  64. Budesinsky M, Budzikiewicz H, Prochazka Z, Ripperger H, Roemer A, Scholz G, Schreiber K (1980) Phytochemistry 19:2295–2297

    Article  CAS  Google Scholar 

  65. Stephan UW, Scholz G (1993) Physiol Plant 88:522–529

    Article  CAS  Google Scholar 

  66. Ling HQ, Pich A, Scholz G, Ganal MW (1996) Mol Gen Genet 252:87–92

    Article  PubMed  CAS  Google Scholar 

  67. Pich A, Scholz G (1996) J Exp Bot 47:41–47

    Article  CAS  Google Scholar 

  68. Von Wiren N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Plant Physiol 119:1107–1114

    Article  PubMed  Google Scholar 

  69. Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Planta 213:967–976

    PubMed  CAS  Google Scholar 

  70. Weber M, Harada E, Vess C, Roepenack-Lahaye von E, Clemens S (2004) Plant J 37:269–281

    Article  PubMed  CAS  Google Scholar 

  71. Rauser WE (1999) Cell Biochem Biophys 31:19–48

    Article  PubMed  CAS  Google Scholar 

  72. Vacchina V, Mari S, Czernic P, Marques L, Pianelli K, Schaumlöffel D, Lebrun M, Lobinski R (2003) Anal Chem 75:2740–2745

    Article  PubMed  CAS  Google Scholar 

  73. Kenny PTM, Nomoto K (1995) J Mass Spectrom:S13–S18

    Google Scholar 

  74. Becher M, Talke IN, Krall L, Krämer U (2004) Plant J 37:251–268

    PubMed  CAS  Google Scholar 

  75. Douchkov D, Gryczka C, Stephan UW, Hell R, Baeumlein H (2005) Plant Cell Environ 28:365–374

    Article  CAS  Google Scholar 

  76. Shriver DF, Atkins PW (1999) Inorganic chemistry, 3rd edn. Oxford University Press, Oxford

  77. Matsuura F, Hamada Y, Shioiri T (1994) Tetrahedron 50:9457–9470

    Article  CAS  Google Scholar 

  78. Matsuura F, Hamada Y, Shiori T (1994) Tetrahedron 50:265–274

    Article  CAS  Google Scholar 

  79. Shioiri T, Irako N, Sakakibara S, Matsuura F, Hamada Y (1997) Heterocycles 44:519–530

    CAS  Google Scholar 

  80. Klair SS, Mohan HR, Kitahara T (1998) Tetrahedron Lett 39:89–92

    Article  CAS  Google Scholar 

  81. Miyakoshi K, Oshita J, Kitahara T (2001) Tetrahedron 57:3355–3360

    Article  CAS  Google Scholar 

  82. Scholz G, Faust J, Ripperger H, Schreiber K (1988) Phytochemistry 27:2749–2754

    Article  CAS  Google Scholar 

  83. Anderegg G, Ripperger H (1989) Chem Comm 10:647–650

    Article  Google Scholar 

  84. Hamer DH (1986) Annu Rev Biochem 55:913–951

    PubMed  CAS  Google Scholar 

  85. Martell AE, Hancock RD (1996) Metal complexes in aqueous solutions. Plenum, New York

  86. Calderone V, Dolderer B, Hartmann H-J, Echner H, Luchinat C, Del Bianco C, Mangani S, Weser U (2005) Proc Natl Acad Sci USA 102:51–56

    Article  PubMed  CAS  Google Scholar 

  87. Zhou J, Goldsbrough PB (1995) Mol Gen Genet 248:318–328

    Article  PubMed  CAS  Google Scholar 

  88. Murphy A, Taiz L (1995) Plant Physiol 109:945–954

    Article  PubMed  CAS  Google Scholar 

  89. Cobbett C, Goldsbrough P (2002) Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

  90. Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker Petra M (2002) J Exp Bot 53:2381–2392

    Article  PubMed  CAS  Google Scholar 

  91. Gawel JE, Ahner BA, Friedland AJ, Morel FMM (1996) Nature 381:64–65

    Article  CAS  Google Scholar 

  92. Maitani T, Kubota H, Sato K, Yamada T (1996) Plant Physiol 110:1145–1150

    PubMed  CAS  Google Scholar 

  93. Ebbs S, Lau I, Ahner B, Kochian L (2002) Planta 214:635–640

    Article  PubMed  CAS  Google Scholar 

  94. Lee S, Moon JS, Ko T-S, Petros D, Goldsbrough PB, Korban SS (2003) Plant Physiol 131:656–663

    Article  PubMed  CAS  Google Scholar 

  95. Cobbett CS, Goldsbrough PB (2000) In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment, Wiley, New York, pp 247–269

  96. Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) New Phytol 159:403–410

    Article  CAS  Google Scholar 

  97. Zhang W, Cai Y, Downum KR, Ma LQ (2004) J Chromatogr A 1043:249–254

    Google Scholar 

  98. Zhang W, Cai Y, Downum KR, Ma LQ (2004) Environ Pollut 131:337–345

    Google Scholar 

  99. Raab A, Feldmann J, Meharg AA (2004) Plant Physiol 134:1113–1122

    Article  PubMed  CAS  Google Scholar 

  100. Webb SM, Gaillard J-F, Ma LQ, Tu C (2003) Environ Sci Technol 37:754–760

    Article  PubMed  CAS  Google Scholar 

  101. Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Plant Physiol 122:1171–1177

    Article  PubMed  CAS  Google Scholar 

  102. Eitinger T, Mandrand-Berthelot M-A (2000) Arch Microbiol 173:1–9

    Article  PubMed  CAS  Google Scholar 

  103. Eitinger T, Suhr J, Moore L, Smith JAC (2005) Biometals 18:399–405

    Article  PubMed  CAS  Google Scholar 

  104. Baker AJM, Reeves RD, Hajar ASM (1994) New Phytol 127:61–68

    Article  CAS  Google Scholar 

  105. Kelly RA, Andrews JC, DeWitt JG (2002) Microchem J 71:231–245

    Article  CAS  Google Scholar 

  106. Szpunar J (2005) Analyst 130:442–465

    Article  PubMed  CAS  Google Scholar 

  107. Szpunar J (2000) Analyst 125:963–988

    Article  PubMed  CAS  Google Scholar 

  108. Pence NS, Larsen PB, Ebbs SD, Letham DL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) Proc Natl Acad Sci USA 97:4956–4960

    Article  PubMed  CAS  Google Scholar 

  109. McGrath SP (1998) In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB Int., Wallingford, UK, pp 261–287

  110. Benes I, Schreiber K, Ripperger H, Kircheiss A (1983) Experientia 39:261–262

    Article  CAS  Google Scholar 

  111. Martell AE, Smith RM (1974) Critical stability constants. Plenum, New York

  112. Perrin DD (1979) Stability constants of metal-ion complexes, 2nd edn. Pergamon, Oxford

    Google Scholar 

  113. Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, Stephan UW, Baumlein H (1999) Eur J Biochem 265:231–239

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alan J. M. Baker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Callahan, D.L., Baker, A.J.M., Kolev, S.D. et al. Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11, 2–12 (2006). https://doi.org/10.1007/s00775-005-0056-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-005-0056-7

Keywords

Navigation