Abstract
Metal accumulating plants exposed to toxic levels of zinc (Zn) and cadmium (Cd) uptake metals through extracellular and intracellular complexation with inorganic and organic ligand formation. However, little is known about the nature and formation mechanism of these metal–ligand complexes. Though, Zn and Cd have many similar chemical properties, yet their complexation and compartmentalization in plants vary with plant species. In principal, the question arises what factors govern Zn and Cd partitioning in plants? What form of the metal is taken up by the root, and is further distributed and accumulated in both vegetative and reproductive tissues? Therefore, the aim of present study is to address several questions concerning the mechanisms of Zn and Cd coordination and compartmentalization in plants using X-ray absorption spectroscopy (XAS) technique. XAS allows direct determination of elemental oxidation states and coordination environments in different plant tissues. This review article briefly explains some other important techniques of XAS; EXAFS (extended X-ray absorption fine structure) and XANES (X-ray absorption near edge structure), which are employed for determining Zn and Cd complexation within the plant. Therefore, In present review, the predominant as well as the minor chemical forms of Zn and Cd present in particular plant tissue have been discussed which could give better insight towards metal accumulation and detoxification mechanisms operated in plants. This information could assist in employing suitable hyperaccumulator plants for metal phytoextraction and reclamation of metal contaminated sites.
Similar content being viewed by others
References
Adriano D (2001) Cadmium. In: Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New York, pp 264–314
Aldrich MV, Gardea-Torresdey JL, Peralta-Videa JR, Parsons JG (2003) Uptake and Reduction of Cr(VI) to Cr(III) by Mesquite (Prosopis spp.): chromate-plant interaction in hydroponics and solid media studied using XAS. Environ Sci Technol 37:1859–1864
Auda MA, Ali EES (2010) Cadmium and zinc toxicity effects on growth and mineral nutrients of carrot (daucus carota). Pak J Bot 42:341–351
Bhatia NP, Orlic I, Siegele R, Ashwath N, Baker AJM, Walsh KB (2003) Elemental mapping using PIXE shows the main pathway of nickel movement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii. New Phytol 160:479–488
Bittsanszky A, Komives T, Gullner G, Gyulai G, Kiss J, Heszky L, Radimszky L, Rennenberg H (2005) Ability of transgenic poplars with elevated glutathione content to tolerate zinc(2+) stress. Environ Int 31:251–254
Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen TL (1999) S-methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11:1485–1498
Bracey MH, Christiansen J, Tovar P, Cramer SP, Bartlett SG (1994) Spinach carbonic anhydrase: investigation of the zinc-binding ligands by site-directed mutagenesis, elemental analysis, and EXAFS. Biochemistry 33:13126–13131
Brandle JE, Labbe H, Hattori J, Miki BL (1993) Field performance and heavy metal concentrations of transgenic flue-cured tobacco expressing a mammalian metallothionein-b-glucuronidase gene fusion. Genome 36:255–260
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702
Castiglione S, Franchin C, Fossati T, Lingua G, Torrigiani P, Biondi S (2007) High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar (Populus alba cv. Villafranca). Chemos 67:1117–1126
Chaney RL (1993) Zinc phytotoxicity. In: Robson AD (ed) Zinc in soil and plants. Kluwer, Dordrecht, pp 135–150
Choi Y, Harada E, Wada M, Tsuboi H, Morita Y, Kusano SHT (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213:45–50
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy metal detoxification. Curr Opin Plant Biol 3:211–216
Cobbett CS, Goldsbrough PB (2002) Mechanisms of metal resistance: phytochelatins and metallothioneins. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, London, pp 247–269
Cosio C, DeSantis L, Frey B, Diallo S, Keller C (2004) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775
Czuba M, Kraszewski A (1994) Long-term cadmium accelerates oxidant injury: significant of bound/free water status during long-term metal stress. Ecotoxicol Environ Saf 29:330–348
De la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsola kali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemos 55:1159–1168
Deef HES (2008) Effect of cadmium and zinc on growth parameters of tomato seedlings. Acad J Plant Sci 1:5–11
Di Baccio D, Tognetti R, Sebastiani L, Vitagliano C (2003) Responses of Populus deltoids X Populus nigra (Populus X euramericana) clone I-214 to high zinc concentrations. New Phytol 159:443–451
Di Baccio D, Kopriva S, Sebastiani L, Rennenberg H (2005) Does glutathione metabolism have a role in the defence of poplar against zinc excess? New Phytol 167:73–80
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Ernst WHO, Nelissen HJM, Ten Bookum WM (2000) Combination toxicology of metal-enriched soils: physiological responses of Zn- and Cd-resistant ecotype of Silene vulgaris on polymetallic soils. Environ Exp Bot 43:55–71
Fan TW, Lane AN, Higashi RM (2004) An electrophoretic profiling method for thiol-rich phytochelatins and metallothioneins. Phytochem Anal 15:175–183
Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559
Garbisu C, Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Eur J Min Proc Environ Prot 3:58–66
Gardea-Torresdey JL, Gomez E, Peralta-Videa JR, Parsons JG, Troiani H, Jose-Yacaman M (2003) Alfalfa sprouts: a natural source for the synthesis of silver nanoparticles. Langmuir 19:1357–1361
Gardea-Torresdey JL, Peralta-Vide JR, de la Rosa G, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797–1810
Gupta DK, Rai UN, Singh A, Inouhe M (2003) Cadmium accumulation and toxicity in Cicer aerietinium L. Poll Res 22:457–463
Gzyl J, Gwozdz EA (2005) Selection in vitro and accumulation of phytochelatins in cadmium tolerant cell lines of cucumber (Cucumis sativus). Plant Cell Tissue Organ Cult 80:59–67
Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemos 52:265–275
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395
Harada E, Yamaguchi Y, Koizumi N, Hiroshi S (2002) Cadmium stress induces production of thiols compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159:445–448
Hernandez LE, Carpena-Ruiz R, G′arate A (1996) Alterations in the mineral nutrition of pea seedlings exposed to cadmium. J. Plant Nutr 19:1581–1598
Isaure MP, Fayard B, Sarret G, Pairis S, Bourguignon J (2006) Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochimica Acta B 61:1242–1252
Kabata-Pendias A, Pendias H (1989) Trace elements in the soil and plants. CRC Press, Florida
Kachenko AG, Bhatia NP, Siegele R, Walsh KB, Singh B (2009) Nickel, Zn and Cd localisation in seeds of metal hyperaccumulators using μ-PIXE spectroscopy. Nucl Instrum Methods Phys Res B Beam Interact Mater Atoms 267:2176–2180
Koningsberger DC, Prins R (1988) X-ray absorption: principles, applications, techniques of EXAFS SEXAFS, and XANES. In: Koningsberger DC, Prins R (eds) Chemical analysis 92. Wiley, New York, p 673
Koprivova A, Kopriva S, Jager D, Will B, Jouanin L, Rennenberg H (2002) Evaluation of transgenic poplars over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium. Plant Biol 4:664–670
Kramer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thalaspi species. Plant Physiol 122:1343–1353
Kupper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311
Kupper 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 212:75–84
Kupper H, Mijovilovich A, Meyer-Klaucke W, Kroneck PHM (2004) Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol 134:748–757
Fukuda N, Hokura A, Kitajima N, Terada Y, Saito H, Abed T, Nakai A (2008) Micro X-ray fluorescence imaging and micro X-ray absorption spectroscopy of cadmium hyper-accumulating plant, Arabidopsis halleri ssp. gemmifera, using high-energy synchrotron radiation. J Anal Atom Spec 23:1068–1075
Lagriffoul A, Mocquot B, Mench M, Vangronsveld J (1998) Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200:241–250
Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883
Lehoczky E, Marth P, Szabados I, Palkovics M, Luka′cs P (2000) Influence of soil factors on the accumulation of cadmium by lettuce. Commun Soil Sci Plant Anal 31:2425–2431
Lei B, Li-Chan ECY, Oomah BD, Mazza G (2003) Distribution of cadmium-binding components in flax (Linum usitatissimum L.) seed. J Agric Food Chem 51:814–821
Leyval C, Turnau K, Wandter H (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153
Lyons TJ, Gasch A, Gaither LA, Botstein D, Brown PO, Eide D (2000) Genome-wide characterization of the Zap1p zinc- responsive regulon in yeast. Proc Natl Acad Sci USA 97:7957–7962
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 220:731–736
Ma Y, Dickinson NM, Wong MH (2006) Beneficial effects of earthworms and arbuscular mycorrhizal fungi on establishment of leguminous shrubs on Pb/Zn mine tailings. Soil Biol Biochem 38:1403–1412
MacDiarmid CW, Gaithe LA, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845–2855
Maitani T, Kubota H, Sato K, Yamada T (1996) The composition of metals bound to class III metallothionein (phytochelatins and its desglycyl peptide) induced by various metals in root cultures off Rubia tinctorium. Plant Physiol 110:1145–1150
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London, p 889
Mendez MO, Glenn EP, Maier RM (2007) Phytostabilization potential of quailbush for mine tailings: growth, metal accumulation and microbial community changes. J Environ Qual 36:245–253
Mendoza-Cozatl DG, Butko E, Springer F, Tropey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role of thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259
Mesjazs-Przybyłowicz J, Grodzińska K, Przybyłowicz WJ, Godzik B, Szarek-Łukaszewska G (2001) Nuclear microprobe studies of elemental distribution in seeds of Biscutella laevigata L. from zinc wastes in Olkusz, Poland. Nucl Instrum Methods Phys Res B Beam Interact Mater Atoms 181:634–639
Molina AS, Nievas C, Chaca MVP, Garibotto F, Gonza′lez U, Marsa SM, Luna C, Gime′nez MS, Zirulnik F (2008) Cadmium-induced oxidative damage and antioxidative defense mechanisms in Vigna mungo L. Plant Growth Regul 56:285–295
Pal M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246
Palmgren M, Clemens S, Williams L, Krämer U, Borg S, Schjørring J, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends in Plant Sci 13:464–473
Parsons JG, Aldrich MV, Gardea-Torresdey JL (2002) Environmental and biological applications of extended X-ray absorption fine structure (EXAFS) and X-ray absorption near edge structure (XANES) spectroscopies. Appl Spectrosc Rev 37:187–222
Pavlikova D, Pavlik M, Vaščikova S, Szákova J, Tlustoš P, Vokač K, Balik J (2004) Speciation analysis and environment separation of organic compounds binding trace elements in seeds of Leuzea carthamoides (Wild.) DC. Appl Organomet Chem 18:619–625
Penner-Hahn JE (2004) X-ray absorption spectroscopy. Compr Coord Chem II 2:159–186
Pickering IJ, Wright C, Bubner B, Ellis D, Persans MW, Yu EY, George GN, Prince RC, Salt DE (2003) Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. Plant Physiol 131:1460–1467
Pocsi I, Prade RA, Penninckx MJ (2004) Glutathione, altruistic metabolite in fungi. Adv Microbiol Physiol 49:1–76
Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontome C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118
Rauser WE (1995) Phytochelatins and related peptides: structure, biosynthesis, and function. Plant Physiol 109:1141–1149
Reese RN, White CA, Winge DR (1992) Cadmium-sulfide crystallites in Cd-(γEC)nG peptide complexes from tomato. Plant Physiol 98:225–229
Richau K, Kozhevnikova A, Seregin I, Vooijs R, Koevoets PLM, Smith A, Ivanov V, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116
Rout GR, Das P (2003) Effect of metal toxicity on plant growth and metabolism: I. Zinc. Agronomie 23:3–11
Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
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 33:713–717
Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126
Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130
Sarret G, Laprade PS, Bert V, Proux O, Hazemann JL, Traverse A, Marcus MA, Manceau A (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826
Sarret G, Harada E, Choi Y, Isaure MP, Geoffroy N, Fakra S, Marcus MA, Birschwilks M, Clemens S, Manceau A (2006) Trichomes of tobacco excrete zinc as zinc-substituted calcium carbonate and other zinc-containing compounds. Plant Physiol 141:1021–1034
Sarret G, Willems G, Isaure MP, Marcus MA, Fakra SC, Frerot H, Pairis S, Geoffroy N, Manceau A, Saumitou-Laprade P (2009) Zinc distribution and speciation in Arabidopsis halleri X Arabidopsis lyrata progenies presenting various zinc accumulation capacities. New Phytol 84:581–595
Stacey SP, McLaughlin MJ, Cakmak I, Hetitiarachchi GM, Scheckel KG, Karkkainen M (2008) Root uptake of lipophilic zinc-rhamnolipid complexes. J Agric Food Chem 56:2112–2117
Straczek A, Sarret G, Manceau A, Hinsinger P, Geoffroy N, Jaillard B (2008) Zinc distribution and speciation in roots of various genotypes of tobacco exposed to Zn. Environ Exp Bot 63:80–90
Tauris B, Borg S, Gregersen PL, Holm PB (2009) A roadmap for zinc trafficking in the developing barley grain based on laser capturemicrodissection and gene expression profiling. J Exp Bot 60:1333–1347
Terzano R, Al Chami Z, Vekemans B, Janssens K, Miano T, Ruggiero P (2008) Zinc distribution and speciation within rocket plants (Eruca vesicaria L. Cavalieri) grown on a polluted soil amended with compost as determined by XRF microtomography and Micro-XANES. J Agric Food Chem 56:3222–3231
Thangavel P, Long S, Minocha R (2007) Changes in phytochelatins and their biosynthetic intermediates in red spruce (Picea rubens Sarg.) cell suspension cultures under cadmium and zinc stress. Plant Cell Tiss Organ Cult 88:201–216
Ueno D, Ma JF, Iwashita T, Zhao FJ, McGrath SP (2005) Identification of the form of Cd in the leaves of a superior Cd-accumulating ecotype of Thlaspi caerulescens using 113Cd-NMR. Planta 221:928–936
Vangronsveld J, Clijsters H (1994) Toxic effects of metals. In: Farago ME (ed) Plants and the chemical elements. Biochemistry, uptake, tolerance and toxicity. VCH Publishers, Weinheim, pp 150–177
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 Prel. Bot Acta 107:243–250
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Vogel-Mikus K, Pongrac P, Kump P, Nečemer M, Simčič J, Pelicon J, Budnar M, Povh B, Regvar M (2007) Localisation and quantification of elements within seeds of the Cd/Zn hyperaccumulator Thlaspi praecox by micro-PIXE. Environ Pollut 147:50–59
Vogel-Mikus K, Simčič J, Pelicon P, Budnar M, Kump P, Nečemer M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ, Regvar M (2008) Comparison of essential and non-essential element distribution in leaves of the Cd/Zn hyperaccumulator Thlaspi praecox as revealed by micro-PIXE. Plant Cell Environ 31:1484–1496
Vogel-Mikus K, Arčon I, Kodre A (2010) Complexation of cadmium in seeds and vegetative tissues of the cadmium hyperaccumulator Thlaspi praecox as studied by X-ray absorption spectroscopy. Plant Soil 331:439–451
Webb SM, Gaillard JF, Ma LQ, Tu C (2003) XAS speciation of arsenic in a hyperaccumulatinf fern. Environ Sci Technol 37:754–760
Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82
Wojcik M, Vangronsveld J, Tukiendorf DHJA (2005) Cadmium tolerance in Thlaspi caerulescens- II. Localization of cadmium in Thlaspi caerulescens. Environ Exp Bot 53:163–171
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 178:315–325
Xiong YH, Yang XE, Ye ZQ, He ZL (2004) Characteristics of cadmium uptake and accumulation by two contrasting ecotypes of Sedum alfredii. J Environ Sci Health 39:2925–2940
Yang XE, Yang MJ (2001) Some mechanisms of zinc and cadmium detoxification in a zinc and cadmium hyperaccumulating plant species (Thlaspi). In: Horst WJ (ed) Plant nutrition-food security and sustainability of agro-ecosystems. Kluwer, Dordrecht, pp 444–445
Zhao FJ, Lombi E, Breedon T, McGrath SP (2000) Zinc hyperaccumulation and cellular distribution in Arabidopsis halleri. Plant Cell Environ 23:507–514
Acknowledgments
The authors gratefully acknowledge the concept and literature provided on the theme by various workers and two anonymous reviewers for critically going through and providing valuable comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Saraswat, S., Rai, J.P.N. Complexation and detoxification of Zn and Cd in metal accumulating plants. Rev Environ Sci Biotechnol 10, 327–339 (2011). https://doi.org/10.1007/s11157-011-9250-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11157-011-9250-y