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.
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
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
Reeves RD, Baker AJM (2000) In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals. Wiley, New York, pp 193–229
Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Science 193:579–580
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
Perrier N, Colin F, Jaffré T, Ambrosi J, Rose J, Bottero J (2004) CR Geoscience 336:567–577
Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Phytochemistry 47:339–347
Reeves RD, Baker AJM, Borhidi A, Berazain R (1996) New Phytol 133:217–224
Baker AJM (1981) J Plant Nutr 3:643–654
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
Salt DE, Krämer U (2000) In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals. Wiley, New York, pp 231–246
Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Nature 379:635–638
Brown SL, Chaney RL, Angle JS, Baker AJM (1994) J Environ Qual 23:1151–1157
McGrath SP, Shen ZG, Zhao FJ (1997) Plant Soil 188:153–159
Reeves RD, Baker AJM (1984) New Phytol 98:191–204
Hanson B, Lindblom SD, Loeffler ML, Pilon-Smits EAH (2004) New Phytol 162:655–662
Boyd RS (1998) In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB Int., Oxford, pp 181–201
Mesjasz-Przybylowicz J, Przybylowicz WJ (2001) S Afr J Sci 97:596–598
Davis MA, Boyd RS, Cane JH (2001) S Afr J Sci 97:554–557
Freeman JL, Garcia D, Kim D, Hopf A, Salt DE (2005) Plant Physiol 137:1082–1091
Clemens S, Palmgren MG, Krämer U (2002) Trends Plant Sci 7:309–315
Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Plant Cell 16:2176–2191
Whiting SN, de Souza MP, Terry N (2001) Environ Sci Technol 35:3144–3150
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London
Römheld V, Marschner H (1986) Plant Physiol 80:175–180
Rengel Z (1999) In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, Berlin Heidelberg New York, pp 231–251
Reichman SM, Parker DR (2005) In: Huang PMG, G (ed) Biogeochemistry of trace elements in the rhizosphere. Elsevier, Toronto
Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Environ Pollut 123:131–138
Zhao FJ, Hamon RE, McLaughlin MJ (2001) New Phytol 151:613–620
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
Lasat MM, Baker AJM, Kochian LV (1996) Plant Physiol 112:1715–1722
Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) Plant Physiol 115:1641–1650
Salt DE, Prince RC, Baker AJM, Raskin I, Pickering IJ (1999) Environ Sci Technol 33:713–717
Finney LA, O’Halloran TV (2003) Science 300:931–936
Fraser KA, Long HA, Candlin R, Harding MM (1965) Chem Comm 15:344–345
Deschamps P, Kulkarni PP, Gautam-Basak M, Sarkar B (2005) Coord Chem Rev 249:895–909
Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Plant Physiol 122:1343–1353
Kameda Y, Ito E, Takeshita A, Nakazawa R, Takenaga H (2002) Tokyo Nogyo Daigaku Nogaku Shuho 47:45–48
Kerkeb L, Krämer U (2003) Plant Physiol 131:716–724
Wycisk K, Kim EJ, Schroeder JI, Krämer U (2004) FEBS Lett 578:128–134
Persans MW, Yan X, Patnoe J-MML, Krämer U, Salt DE (1999) Plant Physiol 121:1117–1126
Ingle RA, Mugford ST, Rees JD, Campbell MM, Smith JAC (2005) Plant Cell 17:2089–2106
Terry N, Bañuelos GS (1999) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, FL
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
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
de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Chemosphere 55:1159–1168
Shan X, Wang H, Zhang S, Zhou H, Zheng Y, Yu H, Wen B (2003) Plant Sci 165:1343–1353
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
Boominathan R, Doran PM (2003) J Biotechnol 101:131–146
Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Funct Plant Biol 29:899–905
Memon AR, Yatazawa M (1984) J Plant Nutr 7:961–974
Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Plant Cell Environ 23:507–514
Küpper H, Mijovilovich A, Meyer-Klaucke W, Kroneck Peter MH (2004) Plant Physiol 134:748–757
Schaumlöffel D, Ouerdane L, Bouyssiere B, Lobinski R (2003) J Anal Atom Spectrom 18:120–127
Lee J, Reeves RD, Brooks RR, Jaffré T (1978) Phytochemistry 17:1033–1035
Shojima S, Nishizawa NK, Fushiya S, Nozoe S, Kumashiro T, Nagata T, Ohata T, Mori S (1989) Biol Met 2:142–145
Higuchi K, Kanazawa K, Nishizawa N-K, Chino M, Mori S (1994) Plant Soil 165:173–179
Noma M, Noguchi M, Tamaki E (1971) Tetrahedron Lett 22:2017–2020
Kristensen I, Larsen PO (1974) Phytochemistry 13:2791–2798
Nomoto K, Mino Y, Ishida T, Yoshioka H, Ota N, Inoue M, Takagi S, Takemoto T (1981) Chem Comm 7:338–339
Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) Biometals 9:84–90
Douchkov D, Herbik A, Koch G, Mock HP, Melzer M, Stephan UW, Baeumlein H (2002) Plant Soil 241:115–119
Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa Naoko K (2003) Plant Cell 15:1263–1280
Scholz G, Schlesier G, Seifert K (1985) Physiol Plant 63:99–104
Budesinsky M, Budzikiewicz H, Prochazka Z, Ripperger H, Roemer A, Scholz G, Schreiber K (1980) Phytochemistry 19:2295–2297
Stephan UW, Scholz G (1993) Physiol Plant 88:522–529
Ling HQ, Pich A, Scholz G, Ganal MW (1996) Mol Gen Genet 252:87–92
Pich A, Scholz G (1996) J Exp Bot 47:41–47
Von Wiren N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Plant Physiol 119:1107–1114
Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Planta 213:967–976
Weber M, Harada E, Vess C, Roepenack-Lahaye von E, Clemens S (2004) Plant J 37:269–281
Rauser WE (1999) Cell Biochem Biophys 31:19–48
Vacchina V, Mari S, Czernic P, Marques L, Pianelli K, Schaumlöffel D, Lebrun M, Lobinski R (2003) Anal Chem 75:2740–2745
Kenny PTM, Nomoto K (1995) J Mass Spectrom:S13–S18
Becher M, Talke IN, Krall L, Krämer U (2004) Plant J 37:251–268
Douchkov D, Gryczka C, Stephan UW, Hell R, Baeumlein H (2005) Plant Cell Environ 28:365–374
Shriver DF, Atkins PW (1999) Inorganic chemistry, 3rd edn. Oxford University Press, Oxford
Matsuura F, Hamada Y, Shioiri T (1994) Tetrahedron 50:9457–9470
Matsuura F, Hamada Y, Shiori T (1994) Tetrahedron 50:265–274
Shioiri T, Irako N, Sakakibara S, Matsuura F, Hamada Y (1997) Heterocycles 44:519–530
Klair SS, Mohan HR, Kitahara T (1998) Tetrahedron Lett 39:89–92
Miyakoshi K, Oshita J, Kitahara T (2001) Tetrahedron 57:3355–3360
Scholz G, Faust J, Ripperger H, Schreiber K (1988) Phytochemistry 27:2749–2754
Anderegg G, Ripperger H (1989) Chem Comm 10:647–650
Hamer DH (1986) Annu Rev Biochem 55:913–951
Martell AE, Hancock RD (1996) Metal complexes in aqueous solutions. Plenum, New York
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
Zhou J, Goldsbrough PB (1995) Mol Gen Genet 248:318–328
Murphy A, Taiz L (1995) Plant Physiol 109:945–954
Cobbett C, Goldsbrough P (2002) Annu Rev Plant Biol 53:159–182
Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker Petra M (2002) J Exp Bot 53:2381–2392
Gawel JE, Ahner BA, Friedland AJ, Morel FMM (1996) Nature 381:64–65
Maitani T, Kubota H, Sato K, Yamada T (1996) Plant Physiol 110:1145–1150
Ebbs S, Lau I, Ahner B, Kochian L (2002) Planta 214:635–640
Lee S, Moon JS, Ko T-S, Petros D, Goldsbrough PB, Korban SS (2003) Plant Physiol 131:656–663
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
Zhao FJ, Wang JR, Barker JHA, Schat H, Bleeker PM, McGrath SP (2003) New Phytol 159:403–410
Zhang W, Cai Y, Downum KR, Ma LQ (2004) J Chromatogr A 1043:249–254
Zhang W, Cai Y, Downum KR, Ma LQ (2004) Environ Pollut 131:337–345
Raab A, Feldmann J, Meharg AA (2004) Plant Physiol 134:1113–1122
Webb SM, Gaillard J-F, Ma LQ, Tu C (2003) Environ Sci Technol 37:754–760
Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Plant Physiol 122:1171–1177
Eitinger T, Mandrand-Berthelot M-A (2000) Arch Microbiol 173:1–9
Eitinger T, Suhr J, Moore L, Smith JAC (2005) Biometals 18:399–405
Baker AJM, Reeves RD, Hajar ASM (1994) New Phytol 127:61–68
Kelly RA, Andrews JC, DeWitt JG (2002) Microchem J 71:231–245
Szpunar J (2005) Analyst 130:442–465
Szpunar J (2000) Analyst 125:963–988
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
McGrath SP (1998) In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB Int., Wallingford, UK, pp 261–287
Benes I, Schreiber K, Ripperger H, Kircheiss A (1983) Experientia 39:261–262
Martell AE, Smith RM (1974) Critical stability constants. Plenum, New York
Perrin DD (1979) Stability constants of metal-ion complexes, 2nd edn. Pergamon, Oxford
Herbik A, Koch G, Mock HP, Dushkov D, Czihal A, Thielmann J, Stephan UW, Baumlein H (1999) Eur J Biochem 265:231–239
Author information
Authors and Affiliations
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-005-0056-7