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Metal Chelating Peptides and Proteins in Plants

  • Chapter
Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants

Abstract

A group of metals having a density higher than 5 g cm−3 are generally termed as heavy metals (HM) and are toxic to plants when available in excess. However, a subset of them, at low concentrations, are essential micronutrients. Wild-type plants cope with HM stress (and homeostasis) by synthesizing a variety of chemically distinct metalchelating ligands (Figure 1), including organic acids, and by exploting a broad range of different response mechanisms, which may act in an additive and/or in a synergistic manner (Prasad, 2001). The main defence mechanisms involved in HM detoxification are revolved around the previously discussed “fan-shaped” model (Figure 2) (Sanità di Toppi and Gabbrielli, 1999), which is based on the “General Adaptation Syndrome” (GAS) hypothesis (Leshem and Kuiper, 1996; Selye, 1936). In this chapter, we focus on HM chelating peptides and proteins, with particular emphasis on phytochelatins. Updates on plant metallothioneins, ferritins and nicotianamine are given as well. Nonprotein metal chelators, in particular organic acids, single amino acids and phytin, not covered in this chapter, were recently reviewed by Rauser (1999).

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References

  • Abrahamson, S.L., Speiser, D.M., Ow, D.W. (1992). A gel electrophoresis assay for phytochelatin. Anal. Biochem. 200, 239–243.

    Article  PubMed  CAS  Google Scholar 

  • Aisen, P., Listowsky, I. (1980) Iron transport and storage proteins. Ann Rev Bio Chem 4, 357–393

    Article  Google Scholar 

  • Al-Lahham, A., Rohde, V., Heim, P., Leuchter, R., Veeck, J., Wunderlich, C., Wolf, K., Zimmermann, M. (1999). Biosynthesis of phytochelatins in the fission yeast. Phytochelatin synthesis: a second role for the glutathione synthetase gene of Schizosaccharomyces pombe. Yeast 15, 385–396.

    Google Scholar 

  • Anelli, G., Pelosi, P., Galoppini, C. (1973). Influence of mercury on the amino acidic composition of tobaccoleaves. Agr. Biol. Chem. 37, 1579–1582.

    Article  CAS  Google Scholar 

  • Arisi, A.-C. M., Mocquot, B., Lagriffoul, A., Mench, M., Foyer, C.H., Jouanin, L. (2000). Responses to cadmium in leaves of transformed poplars overexpressing y-glutamylcysteine synthetase. Physiol. Plant. 109, 143–149.

    Article  CAS  Google Scholar 

  • Bae, W., Chen, W., Mulchandani, A., Mehra, R. K. (2000). Enhanced bioaccumulation of heavy metals by bacterial cells displaying synthetic phytochelatins. Biotech. Bioeng. 70, 518–524.

    Article  CAS  Google Scholar 

  • Bae, W., Mehra, R.K. (1997). Metal binding characteristics of a phytochelatin analog (Glu-Cys)2-Gly. J. Inorg. Biochem. 68, 201–210.

    Article  CAS  Google Scholar 

  • Baker A.J.M., Ewart, K., Hendry, G.A.F., Thorpe, P.C., Walker, P.L. (1990). The evolutionary basis of cadmium tolerance in higher plants. In: 4th International Conference on Environmental Contamination. October 1990, Barcelona, Spain, pp. 23–29.

    Google Scholar 

  • Benet, I., Schreiber, K., Ripperger, H., Kircheiss, A. (1983). Metal complex formation by nicotianamine, a possible phytosirophore. Experientia 39, 261–262.

    Article  Google Scholar 

  • Bernhard, W.R., Kägi, J.H.R. (1987). Purification and characterization of atypical cadmium-binding polypeptides from Zea mays. Experientia 52 (suppl.), 309–315.

    CAS  Google Scholar 

  • Briat, J.-F., Lebrun, M. (1999). Plant responses to metal toxicity. C. R. Acad. Sci. Paris/Life Sci. 322, 43–54.

    Google Scholar 

  • Briat, J.-F., Lobréaux, S. (1998). Iron storage and ferritin in plants. In: H. Sigel, A. Sigel (Eds.), Iron transport and storage in microorganisms, plants and animals, vol. 35 of Metal ions in Biological Systems. Marcel Dekker, New York, pp. 563–584.

    Google Scholar 

  • Briat, J.-F. and Lobréaux, S. (1997). Iron transport and storage in plants. Trends Plant Sci. 2, 187–193.

    Article  Google Scholar 

  • Broeks, A., Gerrard, B., Allikmets, R., Dean, M., Plasterk, R.H. (1996). Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J. 15, 6132–6143.

    PubMed  CAS  Google Scholar 

  • Cataldo, D.A., McFadden, K.M., Garland, T.R., Wildung, R.E. (1988). Organic costituents and complexation of nickel, iron, cadmium and plutonium in soybean xylem exudates. Plant Physiol. 86, 734–739.

    Article  PubMed  CAS  Google Scholar 

  • Chardonnens, A.N., Koevoets, P.L.M., van Zanten, A., Schat, H., Verkleij, J. (1999). Properties of enhanced tonoplast zinc transport in naturally selected zinc-tolerant Silene vulgaris. Plant Physiol. 120, 779–785.

    Google Scholar 

  • Chardonnens, A.N., ten Bookum, W.M., Kuijper, L.D.J., Verkleij, J.A.C., Ernst, W.H.O. (1998). Distribution of cadmium in leaves of cadmium tolerant and sensitive ecotypes of Silene vulgaris. Physiol. Plant. 104, 75–80.

    Article  CAS  Google Scholar 

  • Chassaigne, H., Vacchina, V., Kutchan, T.M, Zenk, M.H. (2001). Identification of phytochelatin-related peptides in maize seedlings exposed to cadmium and obtained enzymatically in vitro. Phytochemistry 56, 657–668.

    Article  PubMed  CAS  Google Scholar 

  • Chen, J., Zhou, J., Goldsbrough, P.B. (1997). Characterization of phytochelatin synthase from tomato. Physiol. Plant. 101, 165–172.

    Article  CAS  Google Scholar 

  • Clemens, S., Antosiewicz, D.M., Ward, J.M., Schachtman, D.P., Schroeder, J.I. (1998). The plant eDNA LCT1 mediates the uptake of calcium and cadmium in yeast. Proc. Natl. Acad. Sci. USA 95, 12043–12048.

    Article  PubMed  CAS  Google Scholar 

  • Clemens, S., Kim, E.J., Neumann, D., Schroeder, J.I. (1999). Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 18, 3325–3333.

    Article  PubMed  CAS  Google Scholar 

  • Clemens, S. (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212, 475–486.

    Article  PubMed  CAS  Google Scholar 

  • Cobbet, C.S. (2000a). Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 123, 825–832.

    Article  Google Scholar 

  • Cobbet, C.S. (2000b). Phytochelatins biosynthesis and function in heavy-metal detoxification. Curr. Opin. Plant Biol. 3, 211–216.

    Google Scholar 

  • de Knecht, J.A., Koevoets, P.L.M., Verkleij, J.A.C., Ernst, W.H.O. (1992). Evidence against a role for phytochelatins in naturally selected increased cadmium tolerance in Silene vulgaris (Moench) Garcke. New Phytol. 122, 681–688.

    Article  Google Scholar 

  • de Knecht, J.A., van Baren, N., Ten Bookum, W.T., Wong Fong Sang, H.W., Koevoets, P.L.M., Schat, H., Verkleij, J.A.C. (1995). Synthesis and degradation of phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris. Plant Sci. 106, 9–18.

    Article  Google Scholar 

  • de Knecht, J.A., van Dillen, M., Koevoets, P.L.M., Scbat, H., Verkleij, J.A.C., Ernst, W.H.O. (1994). Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris. Plant Physiol. 104, 255–261.

    PubMed  Google Scholar 

  • Delhaize, E. (1996). A metal-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 111, 849–855.

    Article  PubMed  CAS  Google Scholar 

  • Delhaize, E., Jackson, P.J., Lujan, L.D., Robinson, N.J. (1989). Poly(y-glutamylcysteinyl)glycine synthesis in Datura innoxia and binding with cadmium. Plant Physiol. 89, 700–706.

    Article  PubMed  CAS  Google Scholar 

  • De Miranda, J.R., Thomas, M.A., Thurman, D.A., Tomsett, A.B. (1990). Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Lett. 260, 277–280.

    Article  PubMed  Google Scholar 

  • de Vos, C.H.R., Vonk, M.J., Vooijs, R., Schat, H. (1992). Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol. 98, 853–858.

    Article  PubMed  Google Scholar 

  • Dominguez-Solis, J.R., Gutierrez-Alcala, G., Romero, L.C., Gotor, C. (2001). Cytosolic O-acetylserine(thiol) lyase gene is regulated by heavy metals and can function in metal tolerance. J. Biol. Chem. 276 in press (manuscript M009574200).

    Google Scholar 

  • Ebbs, S.D., Lau, I., Ahner, B.A., Kochian, L.V. (2000). Phytochelatins synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Plant Biology 2000 ( The American Society of Plant Physiologists ), Abstract no. 21004.

    Google Scholar 

  • Eide, D., Broderius, M., Fett, J., Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93, 5624–5628.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Hernandez, M., Murphy, A., Taiz, L. (1998). Metallothioneins 1 and 2 have distinct but overlapping expression patterns in Arabidopsis. Plant Physiol. 118, 387–397.

    Article  PubMed  CAS  Google Scholar 

  • Gekeler, W., Grill, E., Winnacker, E.-L., Zenk, M.H. (1989). Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z. Naturforsch. 44c, 361–369.

    CAS  Google Scholar 

  • Goto, F., Yoshihara, T., Shigemoto, N., Toki, S., Takaiwa, F. (1999). Nat. Biotechnol. 17, 282–286.

    Article  PubMed  CAS  Google Scholar 

  • Gries, G.E., Wagner, G.J. (1998). Association of nickel versus transport of cadmium and calcium in tonoplast vesicles of oat roots. Planta 204, 390–396.

    Article  PubMed  CAS  Google Scholar 

  • Grill, E., Gekeler, W., Winnacker, E.-L., Zenk, M.H. (1986). Homo-phytochelatins are heavy metal-binding peptides of homo-glutathione containing Fabales. FEBS Lett. 205, 47–50.

    Article  CAS  Google Scholar 

  • Grill, E., Loeffler, S., Winnacker, E.-L., Zenk, M.H. (1989). Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific y-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA 86, 6838–6842.

    Article  PubMed  CAS  Google Scholar 

  • Grill, E., Thumann, J., Winnacker, E.-L., Zenk, M.H. (1988). Induction of heavy metal binding phytochelatins by inoculation of cell cultures in standard media. Plant cell Rep. 7, 375–378.

    CAS  Google Scholar 

  • Grill, E., Winnacker, E.-L., Zenk, M.H. (1985). Phytochelatins: the principal heavy-metal complexing peptides of higher plants. Science 230, 674–676.

    Article  PubMed  CAS  Google Scholar 

  • Grill, E., Winnacker, E.-L., Zenk, M.H. (1987). Phytochelatins, a class of heavy-metal-binding peptides from

    Google Scholar 

  • plants are functionally analogous to metallothioneins. Proc. Natl. Acad. Sci. USA 84, 439–443. Guerinot, M.L., Salt, D.E. (2001). Fortified foods and phytoremediation. Two sides of the same coin. Plant

    Google Scholar 

  • Physiol. 125 164–167.

    Google Scholar 

  • Ha, S.B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O’Connell, M.J., Goldsbrough, P.B., Cobbett, C.S. (1999). Phytochelatin synthase from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11, 1153–1163.

    PubMed  CAS  Google Scholar 

  • Harmens, H., den Hartog, P.R., Ten Hokum, W.M., Verkleij, J.A.C. (1993). Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins. Plant Physiol. 103, 1305 1309.

    Google Scholar 

  • Harris W.R., Madisen L.J. (1988) Equilibrium studies on the binding ofcadmium(II) human transferrin. Biochem J 27: 284–289

    Article  CAS  Google Scholar 

  • Harrison, P.M., Arosio, P. (1996). The ferritins: molecular properties, iron storage function and cellular regulation. Biochem. Biophys. Acta 1275, 161–203.

    Google Scholar 

  • Hayashi, Y., Nakagawa, C.W., Mutoh, N., Isobe, M., Goto, T. (1991). Two pathways in the biosynthesis of cadystins (yEC)„G in the cell-free system of the fission yeast. Biochem. Cell Biol. 69, 115–121.

    Article  PubMed  CAS  Google Scholar 

  • Heiss, S., Schäfer, H.J., Haag-Kerwer, A., Rausch, T. (1999). Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol. Biol. 39, 847–857.

    CAS  Google Scholar 

  • Howden, R., Andersen, C.S., Goldsbrough, P.B., Cobbett, C.S. (1995a). A cadmium-sensitive, glutathionedeficient mutant of Arabidopsis thaliana. Plant Physiol. 107, 1067–1073.

    Article  PubMed  CAS  Google Scholar 

  • Howden, R., Cobbett, C.S. (1992). Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 99, 100–107.

    Article  Google Scholar 

  • Howden, R., Goldsbrough, P.B., Andersen, C.S., Cobbett, C.S. (1995b). Cadmium-sensitive, cadi mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol. 107, 1059–1066.

    Article  PubMed  CAS  Google Scholar 

  • Huang, B., Hatch, E., Goldsbrough, P.B. (1987). Selection and characterization of cadmium tolerant cells in tomato. Plant Sci. 52, 211–221.

    Article  CAS  Google Scholar 

  • Hunter, T.C., Mehra, R.K. (1998). A role for HEM2 in cadmium tolerance. J. Inorg. Biochem. 69, 293–303.

    Article  PubMed  CAS  Google Scholar 

  • Imai, K., Obata, H., Shimizu, K., Komiya, T. (1996). Conversion of glutathione into cadystins and their analogs catalyzed by carboxypeptidase Y. Biosci. Biotech. Biochem. 60, 1193–1194.

    Article  CAS  Google Scholar 

  • Inouhe, M., Ito, R., Ito, S., Sasada, N., Tohoyama, H., Joho, M. (2000). Azuki bean cells are hypersensistive to cadmium and do not synthesisze phytochelatins. Plant Physiol. 123, 1029–1036.

    Article  PubMed  CAS  Google Scholar 

  • Inouhe, M., Sumiyoshi, M., Tohoyama, H., Joho, M. (1996). Resistance to cadmium ions and formation of a cadmium-binding complex in various wild-type yeasts. Plant Cell Physiol. 37, 341–346.

    Article  PubMed  CAS  Google Scholar 

  • Inzé, D., van Montagu, M. (1995). Oxidative stress in plants. Curr. Opin. Biotechnol. 6, 153–158

    Article  Google Scholar 

  • Jacob, C., Maret, W., Vallee, B.L. (1998). Control of zinc transfer between thionein, metallothionein, and zinc proteins. Proc. Natl. Acad. Sci. USA. 95, 3489–3494.

    Article  PubMed  CAS  Google Scholar 

  • Jemal, F., Didierjean, L., Ghrir, R., Ghorbal, M.H., Burkard, G. (1998). Characterization of cadmium binding peptides from pepper (Capsicum annuum). Plant Sci. 137, 143–154.

    Article  CAS  Google Scholar 

  • Johanning, J., Strasdeit, H. (1998). A coordination-chemical basis for the biological function of the phytochelatins. Angew. Chem. Int. Ed. 37, 2464–2466.

    Google Scholar 

  • Kägi, J.H.R. (1991). Overview of metallothionein. Methods Enzymol. 205, 613–626.

    Article  PubMed  Google Scholar 

  • Kille, P., Winge, D.R., Harwood, J.L., Kay, J. (1991). A Plant metallothionein produced in E. coli. FEBS Lett. 295, 171–175.

    Article  PubMed  CAS  Google Scholar 

  • Klapheck, S., Fliegner, W., Zimmer, I. (1994). Hydroxymethyl-phytochelatins are metal-induced peptides of the Poaceae. Plant Physiol. 104, 1325–1332.

    Article  PubMed  CAS  Google Scholar 

  • Klapheck, S., Schlunz, S., Bergmann, L. (1995). Synthesis of phytochelatins and homo-phytochelatins in Pisum sativum L. Plant Physiol. 107,,515–521.

    Google Scholar 

  • Kneer, R., Zenk, M.H. (1992). Phytochelatins protect plant enzymes from heavy metal poisoning. Phytochemistry, 31, 2663–2667.

    Article  CAS  Google Scholar 

  • Knauer, K.B.A., Abner, H., Sigg, L. (1998). Phytochelatin and metal content in phytoplankton from freshwater lakes with different metal concentrations. Environ. Toxicol. Chem. 17, 2444–2452.

    Article  CAS  Google Scholar 

  • Kotrba, P., Macek, T., Ruml, T. (1999). Heavy metal-binding peptides and proteins in plants. A review. Collection. Czec. Chem. Commun. 64, 1057–1086.

    Article  CAS  Google Scholar 

  • Kneer, R., Zenk, M.H. (1992). Phytochelatins protect plant enzymes from heavy metal poisoning. Phytochemistry, 31, 2663–2667.

    Article  CAS  Google Scholar 

  • Kneer, R., Zenk, M.H. (1997). The formation of Cd-phytochelatins complexes in plant cell cultures. Phytochemistry 44, 69–74.

    Article  CAS  Google Scholar 

  • Kramer, U., Cotter-Howells, J.D., Baker, A.J.M., Smith, J.A.C. (1996). Free histidine as a metal chelator in plants that accumulate nickel. Nature 379, 635–638.

    Article  CAS  Google Scholar 

  • Krotz, R.M., Evangelou, B.P., Wagner, G.J. (1989). Relationships between cadmium, zinc, Cd-binding peptide, and organic acid in tobacco suspension cells. Plant Physiol. 91, 780–787.

    Article  PubMed  CAS  Google Scholar 

  • Kubota, H, Sato, K., Yamada, T., Maitani, T. (1995). Phytochelatins (class III metallothionein) and their desglycyl peptides induced by cadmium in normal root cultures of Rubia tinctorum L. Plant Sci. 106, 157–166.

    Article  CAS  Google Scholar 

  • Kubota, H, Sato, K., Yamada, T., Maitani, T. (2000). Phytochelatin homologs induced in hairy roots of horseradish. Phytochem. 53, 239–245.

    Google Scholar 

  • Lane, B., Kajoika, R., Kennedy, R. (1987). The wheat-germ Ec protein is a zinc-containing metallothionein. Biochem. Cell Biol. 65, 1001–1005.

    Google Scholar 

  • Lasat, M.M., Pence, N.S., Garvin, D.F., Ebbs, S.D., Kochian, L.V. (2000). Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J. Exp. Bot. 51, 71–79.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S., Leustek, T. (1999). The affect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci. 141, 201–207.

    Article  CAS  Google Scholar 

  • Leopold, I., Günther, D. (1997). Investigation of the binding properties of heavy-metal-peptide complexes in plant cell cultures using HPLC-ICP-MS. Fresenius J. Anal. Chem. 359, 364–370.

    Article  CAS  Google Scholar 

  • Leopold, I., Günther, D., Schmidt, J., Neumann, D. (1999). Phytochelatins and heavy metal tolerance. Phytochem. 50, 1323–1328.

    Article  CAS  Google Scholar 

  • Leshem, Y.Y., Kuiper, P.J.C. (1996). Is there a GAS (general adaptation syndrome) response to various types of environmental stress? Biol. Plant. 38, 1–18.

    Google Scholar 

  • Leustek, T., Martin, M.L., Bick, J.A., Davies, J.P. (2000). Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu. Rev. Plant Physiol. Mol. Biol. 51, 141–165.

    Article  CAS  Google Scholar 

  • Li, Z.S., Lu, Y.P., Zhen, R.G., Szczypka, M., Thiele, D.J., Rea, P.A. (1997). A new pathway for vacuolar sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato) cadmium. Proc. Natl. Acad. Sci. USA 94, 42–47.

    Article  PubMed  CAS  Google Scholar 

  • Lichtenberger, O., Neumann, D. (1997). Analytical electron microscopy as a powerful tool in plant cell biology: examples using electron energy loss spectroscopy and X-ray microanalysis. Eur. J., Cell Biol. 73, 378–386.

    CAS  Google Scholar 

  • Lin, S.L., Wu, L. (1994). Effects of copper concentration on mineral nutrient uptake and copper accumulation in protein of copper-tolerant and nontolerant Lotus purshianus L. Ecotoxicol. Environ. Saf. 29, 214–228.

    Article  PubMed  CAS  Google Scholar 

  • Loeffler, S., Hochberger, A., Grill, E., Gekeler, W., Winnacker, E.-L., Zenk, M.H. (1989). Termination of the phytochelatin synthase reaction through sequestration of heavy metals by the reaction product. FEBS Lett. 258, 42–46.

    Article  CAS  Google Scholar 

  • Ma, L.Q., Komar, K.M., Tu, C., Zhang, W., Cai, Y., Kennelley, E.D. (2001). A fern that hyperaccumulates arsenic. Nature 409, 579.

    Article  PubMed  CAS  Google Scholar 

  • Maitani, T., Kubota, H., Sato, K., Yamada, I. (1996). The composition of metals bound to class III metallothionein (phytochelatin and its desglycyl peptide) induced by various metals in root cultures of Rubia tinctorum. Plant Physiol. 110, 1145–1150.

    Google Scholar 

  • Margoshes, M., Vallee, B.L. (1957). A cadmium protein from equine kidney cortex. J. Am. Chem. Soc. 79, 4813–4814.

    Article  CAS  Google Scholar 

  • Mazen, A.M.A., El Maghraby, O.M.O. (1997/98). Accumulation of cadmium, lead and strontium, and a role of calcium oxalate in water hyacinth tolerance. Biol. Plant. 40, 411–417.

    Google Scholar 

  • Mehra, R.K., Kodati, V.R., Abdullah, R. (1995). Chain length-dependent Pb(II)-coordination in phytochelatins. Biochem. Biophys. Res: Commun. 215, 730–736.

    Article  CAS  Google Scholar 

  • Mehra, R.K., Miclat, J., Kodati, V.R., Abdullah, R., Hunter, T.C., Mulchandani, P. (1996a). Optical spectroscopic and reverse-phase HPLC analyses of Hg(II) binding to phytochelatins. Biochem. J. 314, 7382.

    Google Scholar 

  • Mehra, R.K., Tarbet, E.B., Gray, W.R., Winge, D.R. (1988). Metal-specific synthesis of two metallothioneins and gamma-glutamyl peptides in Candida glabrata. Proc. Natl. Acad. Sci. USA 85, 8815–8819.

    Article  PubMed  CAS  Google Scholar 

  • Mehra, R.K., Tran, K., Scott, G.W., Mulchandani, P., Saini, S.S. (1996b). J. Ag(I)-binding to phytochelatins. J. Inorg. Biochem. 61, 125–142.

    Google Scholar 

  • Mehra, R.K., Mulchandani, P. (1995). Glutathione-mediated transfer of Cu(I) into phytochelatins. Biochem. J. 307, 697–705.

    PubMed  CAS  Google Scholar 

  • Meuwly, P., Thibault, P., Rauser, W.E. (1993). y-glutamylcysteinyl-glutamic acid–a new homologue of glutathione in maize seedlings exposed to cadmium. FEBS Lett. 336, 472–476.

    Google Scholar 

  • Meuwly, P., Thibault, P., Schwan, A.L., Rauser, W.E. (1995). Three families of thiol peptides are induced by cadmium in maize. Plant J. 7, 391–400.

    Article  PubMed  CAS  Google Scholar 

  • Mewes, H.W., Albermann, K., Bahr, M., Frishman, D., Gleissner, A., Hani, J., Heumann, K., Kleine, K., Maierl, A., Oliver, S.G., Pfeiffer, F., Zollner, A. (1997). Overview of the yeast genome. Nature 387 (6632 Suppl), 7–65.

    PubMed  Google Scholar 

  • Mori, A., Leita, L. (1998). Application of capillary electrophoresis on the characterization of cadmium-induced polypeptides in roots of pea plants. J. Plant Nutr. 21, 2335–2341.

    Article  CAS  Google Scholar 

  • Murasugi, A., Wada, C., Hayashi, Y. (1981). Cadmium-binding peptide induced in fission yeast, Schizosaccharomyces pombe. J. Biochem. 90, 1561–1564.

    PubMed  CAS  Google Scholar 

  • Murguia, J.R. Belles, J.M., Serrano, R. (1996). The yeast HAL2 nucleotidase is an in vivo target of salt toxicity. J. Biol. Chem. 271 29029–29033.

    Google Scholar 

  • Murphy, A., Taiz, L. (1995). Comparison of metallothionein gene expression and nonprotein thiols in ten Arabidopsis ecotypes. Correlation with copper tolerance. Plant Physiol. 109, 945–954.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, A., Zhou, J., Goldsbrough, P.B., Taiz, L. (1997). Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiol. 113, 1293–1301.

    Article  PubMed  CAS  Google Scholar 

  • Nagalakshmi, N., Prasad, M.N.V. (2001). Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scendesmus bijugatus. Plant Sci. 160, 291–299.

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa, R., Ikawa, M., Yasuda, K., Takenaga, H. (2000). Synergistic inhibition of the growth of suspension cultured tobacco cells by simultaneous treatment with cadmium and arsenic in relation to phytochelatin synthesis. Soil Sci. Plant Nutrition 46, 271–275.

    Article  CAS  Google Scholar 

  • Nelson, K.B., Winge, D.R. (1983). Order of metal binding in metallothionein. J. Biol. Chem. 258, 13063–13069.

    Google Scholar 

  • Noctor, G., Arisi., A.-C. M., Jouanin, L., Kunert, K.-J., Rennenberg, H., Foyer, C.H. (1998). Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J. Exp. Bot. 49, 623–647.

    Google Scholar 

  • Nussbaum, S., Schmutz, D., Brunold, C. (1988). Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. Plant Physiol. 88, 1407–1410.

    Article  PubMed  CAS  Google Scholar 

  • Ortiz, D.F., Kreppel, L., Speiser, D.M., Scheel, G., McDonald, G., Ow, D.W. (1992). Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. EMBO J. 11, 3491–3499.

    PubMed  CAS  Google Scholar 

  • Ortiz, D.F., Ruscitti, T., McCue, K., Ow, D.W. (1995). Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 270, 4721–4728.

    Article  PubMed  CAS  Google Scholar 

  • Ow, D.W. (1996). Heavy metal tolerance genes: prospective tools for bioremediations. Res. Conserv. Recycl. 18, 135–149.

    Google Scholar 

  • Panda, K. K., Patra, J., Panda, B. B. (1997). Persistence of cadmium-induced adaptive response against genotoxicity of maleic hydrazide and methyl mercuric chloride in root meristem cells of Allium cepa L. Differential inhibition by cycloheximide and buthionine sulfoximine. Mutat. Res. 389, 129–139.

    Google Scholar 

  • Pelosi, P., Galoppini, C. (1973). Sulla natura dei composti mercurio-organici nelle foglie di tabacco. Atti Soc. Tosc. Sci. Nat. Mem. 80, 215–220.

    Google Scholar 

  • Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D., Kochian, L.V., (2000). The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 97, 4956–4960.

    Google Scholar 

  • Pich, A., Hillmer, S., Manteuffel, R., Scholz, G. (1997). First immunohistochemical localization of the endogenous Fee+-chelator nicotianamine. J. Exp. Bot. 48, 759–767.

    Google Scholar 

  • Pich, A., Scholz, G. (1996). Translocation of copper and other micronutrients in tomato plants (Lycopersicon esculentum Mill.): nicotianamine-stimulated copper transport in the xylem. J. Exp. Bot. 47, 41–47.

    Google Scholar 

  • Pickering, I.J., Prince, R.C., George, G.N., Rauser, W.E., Wickramasinge, W.A., Watson, A.A., Dameron, C.T., Dance, I.G., Firlie, D.P., Salt, D.E. (1999). X-ray absorption spectroscopy of cadmium phytochelatin and model systems. Biochim. Biophys. Acta 1429, 351–364.

    Google Scholar 

  • Pickering, I.J., Prince, R.C., George, M.J., Smith, R.D., George, G.M., Salt, D.E. (2000). Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 122, 1171–1177.

    Article  PubMed  CAS  Google Scholar 

  • Pilon-Smits, E.A.H., Hwang, S., Lytle, C.M., Zhu, Y.L., Tay, J.C., Bravo, R.C., Chen, Y., Leustek, T., Terry, N. (1999a). Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol. 119, 123–132.

    Article  PubMed  CAS  Google Scholar 

  • Pilon-Smits, E.A.H., Zhu, Y.L., Pilon, M., Terry, N. (1999b). Overexpression of glutathione synthesizing enzymes enhances cadmium accumulation in Brassica juncea. Proceedings of the 55 International Conference on the Biogeochemistry of Trace Elements, Vienna, July 11–15, pp 890–891.

    Google Scholar 

  • Polette, L.A., Gardea-Torresdey, J.L., Chianelli, R.R., George, G.N., Pickering, I.J., Arenas, J. (2000). XAS and microscopy studies of the uptake and bio-transformation of copper in Larrea tridentate (creosote bush). Microchem. J. 65, 227–236.

    Google Scholar 

  • Price DJ, Joshi JG (1982) Ferritin: a zinc detoxicant and a zinc ion donor. Proc Natl Acad Sci (USA) 79: 3116–3119

    Article  CAS  Google Scholar 

  • Price DJ, Joshi JG (1983) Ferritin: Binding of beryllium and other divalent metal ions. J Biol Chem 258: 1087310880

    Google Scholar 

  • Prasad, M.N.V. (1997). Trace metals. In: M.N.V.Prasad (Ed.), Plant ecophysiology. John Wiley and Sons. Inc., New York, pp. 207–249.

    Google Scholar 

  • Prasad, M.N.V. (1999). Metallothioneins and metal binding complexes in plants. In: M.N.V. Prasad, J. Hagemeyer (Eds.), Heavy metal stress in plants: from molecules to ecosystems. Springer-Verlag, Berlin Heidelberg, pp. 51–72.

    Chapter  Google Scholar 

  • Prasad, M.N.V. (ed) (2001) Metals in the Environment - Analysis by biodiversity. Marcel Dekker Inc. New York. pp. 504

    Google Scholar 

  • Rama Kumar, T and M.N.V. Prasad (2001) Possible involvement of calcium/ calmodulin dependent kinase(s) in phosphorylation of ferritin in Vigna mungo (L.) Hepper (Black Gram). JPlant Biology 28: 1–5

    Google Scholar 

  • Rama Kumar, T and M.N.V. Prasad (2000) Partial purification and characterization of Fen-itin from Vigna mungo (Black gram) seeds. J. Plant Biology 27: 241–246

    Google Scholar 

  • Rauser, W.E. (1990). Phytochelatins. Annu. Rev. Biochem. 59, 61–86.

    Google Scholar 

  • Rauser, W.E. (1999). Structure and function of metal chelators produced by plants. Cell Biochem. Biophys. 31, 19–48.

    Google Scholar 

  • Rauser, W.E., Meuwly, P. (1995). Retention of cadmium in roots of maize seedlings. Plant Physiol. 109, 195202.

    Google Scholar 

  • Rea, P.A., Li, Z.S., Lu, Y.P., Drozdowicz, Y., Martinoia, E. (1998). From vascular GS-X pumps to multispecific ABC transporters. Annu. Rev. Plant Physiol. Mol. Biol. 49, 727–760.

    Google Scholar 

  • Reese, R.N., Wagner, G.J. (1987). Effects of buthionine sulfoximine on Cd-binding peptide levels in suspension-cultured tobacco cells treated with Cd, Zn, or Cu. Plant Physiol. 84, 574–577.

    Google Scholar 

  • Robinson, N.J., Ratliff, R.L., Anderson, P.J., Delhaize, E., Berger, J.M., Jackson, P.J. (1988). Biosynthesis of poly(y-glutamylcysteinyl)glycines in cadmium-tolerant Datura innoxia ( Mill.) cells. Plant Sci. 56, 197–204.

    Google Scholar 

  • Robinson, N.J., Tommey, A.M., Kuske, C., Jackson, P.J. (1993). Plant metallothioneins. Biochem. J. 295, 110.

    Google Scholar 

  • Rüegsegger, A., Brunold, C. (1992). Effects of cadmium on y-glumilcysteinyl-glycine synthesis in maize seedlings. Plant Physiol. 99, 428–433.

    Article  PubMed  Google Scholar 

  • Rüegsegger, A., Schmutz, D., Brunold, C. (1990). Regulation of glutathione synthesis by cadmium in Pisum sativum L. Plant Physiol. 93, 1579–1584.

    Article  PubMed  Google Scholar 

  • Salt, D.E., Pickering, I.J., Prince, R.C., Gleba, D., Dushenkov, S., Smith, R.D., Raskin, I. (1997). Metal accumulation by aquacultured deedlings of Indian mustard. Environ. Sci. Technol. 31, 1636–1644.

    Google Scholar 

  • Salt, D.E., Prince, R.C., Pickering, I.J., Raskin, I. (1995). Mechanisms of cadmium mobility and accumulation in indian mustard. Plant Physiol. 109, 1427–1433.

    PubMed  CAS  Google Scholar 

  • Salt, D.E., Rauser, W.E. (1995). MgATP-dependent transport of phytochelatins across the tonoplast of oat roots. Plant Physiol. 107, 1293–1301.

    PubMed  CAS  Google Scholar 

  • Salt, D.E., Wagner, G.J. (1993). Cadmium transport across tonoplast of vescicles from oat roots. J. Biol. Chem. 268, 12297–12302.

    Google Scholar 

  • Sanità di Toppi, L., Favali, M.A., Gabbrielli, R., Gremigni, P. (2001). Brassicaceae. In: M.N.V. Prasad (Ed.)

    Google Scholar 

  • Metals in the environment: analysis by biodiversity. Marcel Dekker, New York, pp. 219–258.

    Google Scholar 

  • Sanità di Toppi, L., Gabbrielli, R. (1999). Response to cadmium in higher plants. Environ. Exp. Bot. 41, 105–130.

    Google Scholar 

  • Sanità di Toppi, L., Lambardi, M., Pazzagli, L., Cappugi, G., Durante, M., Gabbrielli, R. (1998). Response to cadmium in carrot in vitro plants and cell suspension cultures. Plant Sci. 137, 119–129.

    Article  Google Scholar 

  • Sanità di Toppi, L., Lambardi, M., Pecchioni, N., Pazzagli, L., Durante, M., Gabbrielli, R. (1999). Effects of cadmium stress on hairy roots of Daucus carota. J. Plant Physiol. 154, 385–391.

    Article  Google Scholar 

  • Schäfer, H.J., Haag-Kerwer, A., Rausch, T. (1998). cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cd-induction of a putative mitochondrial y-glutamylcysteine synthetase isoform. Plant Mol. Biol. 37, 87–97.

    Google Scholar 

  • Schat, H., Kalff, M.M. A. (1992). Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed strain? Plant Physiol. 99, 1475–1480.

    Article  PubMed  CAS  Google Scholar 

  • Scheller, H.V., Huang, B., Hatch, E., Goldsbrough, P.B. (1987). Phytochelatin synthesis and glutathione levels n response to heavy metals in tomato cells. Plant Physiol. 85, 1031–1035.

    Article  PubMed  CAS  Google Scholar 

  • Schmöger, M.E.V., Oven, M., Grill, E. (2000). Detoxification of arsenic by phytochelatins in plants. Plant Physiol. 122, 793–801.

    Article  PubMed  Google Scholar 

  • Sczekan SR, Joshi JG (1989) Metal binding properties of phytoferritin and synthetic iron cores. Biochim Biophys Acta 990: 8–14

    Article  CAS  Google Scholar 

  • Selye, H. (1936). A syndrome produced by various noxious agents. Nature 138, 32–34.

    Article  Google Scholar 

  • Shojima, S., Nishizawa, N.K., Fushiya, S., Nozoe, S., Irifune, T., Mori, S. (1990). Biosynthesis of phytosiderophores. In vitro biosynthesis of2’-deoxymugineic acid from L-methionine and nicotianamine. Plant Physiol. 93, 1497–1503.

    Google Scholar 

  • Speiser, D.M., Abrahamson, S.L., Banuelos, G., Ow, D.W. (1992a). Brassica juncea produces a phytochelatin-cadmium-sulfide complex. Plant Physiol. 99, 817–821.

    Google Scholar 

  • Speiser, D.M., Ortiz, D.F., Kreppel, L., Ow, D.W. (1992b). Purine biosynthetic genes are required for cadmium tolerance in Schizosaccharomyces pombe. Mol. Cell. Biol. 12, 5301–5310.

    Google Scholar 

  • Steffens, J.C. (1990). The heavy-metal binding peptides of plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 553–575.

    Google Scholar 

  • Steffens, J.C., Hunt, D.F., Williams, B.G. (1986). Accumulation of non-protein metal-binding polypeptides (yglutamyl-cysteinyl,;glycine in selected cadmium-resistant tomato cells. J. Biol. Chem. 261, 13879–13882.

    Google Scholar 

  • Stephan, U.W., Schmidke, 1., Stephan, V.W., Scholz, G. (1996). The nicotianamine molecule is made-tomeasure for complexation of metal micronutrients in plants. Biometals 9, 84–90.

    CAS  Google Scholar 

  • Stephan, U.W., Scholz, G (1993). Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol. Plant. 88, 522–529.

    Article  CAS  Google Scholar 

  • Strasdeit, H., Duhme, A.-K., Kneer, R., Zenk, M.H., Hermes, C., Notting, H.-F. (1991). Evidence for discrete Cd(SCys)4 units in cadmium phytochelatin complexes from EXAFS spectroscopy. J. Chem. Soc. Chem. Commun. 16, 1129–1130.

    Google Scholar 

  • Subhadra, A. V., Panda, B. B. (1994). Metal-induced genotoxic adaptation in barley (Hordeum vulgare L.) to maleic hydrazide and methyl mercuric chloride. Mutat. Res. 321, 93–102.

    Google Scholar 

  • Tabata, K., Kashiwagi, S., Mori, H., Ueguchi, C., Mizuno, T. (1997). Cloning of a eDNA encoding a putative metal-transporting P-type ATPase from Arabidopsis thaliana. Biochim. Biophys. Acta 1326, 1–6.

    Google Scholar 

  • Terry N., Zayed, A.M. (1994). Selenium volatilisation by plants. In: W.T. Frankenberger, S. Benson (Eds.), Selenium in the Environment. Marcel Dekker, New York.

    Google Scholar 

  • Tan AT, Woodworth RC (1969) Ultraviolet difference spectral studies of conalbumin complexes with transition metal ions. Biochemistry 8: 3711–3716

    Article  PubMed  CAS  Google Scholar 

  • Thumann, J., Grill, E., Winnacker, E.-L., Zenk, M.H. (1991). Reactivation of metal-requiring apoenzymes by phytochelatin-metal complexes. FEBS Lett. 284, 66–69.

    Article  PubMed  CAS  Google Scholar 

  • Valentine, J.S., Gralla, E.B. (1997). Delivering copper inside yeast and human cells. Science 278, 817–818.

    Article  PubMed  CAS  Google Scholar 

  • Vande Weghe, J.G., Ow, D.W. (1997). A novel mitochondrial oxidoreductase required for phytochelatin accumulation and cadmium tolerance in fission yeast. J. Exp. Bot. 48 (suppl.), 96.

    Google Scholar 

  • Vande Weghe, J.G., Ow, D.W. (1999). A fission yeast gene for mitochondrial sulfide oxidation. J. Biol. Chem. 274, 13250–13257.

    Article  Google Scholar 

  • Vatamaniuk, O.K., Mari, S., Lu, Y.P., Rea, P.A. (1999). AtPCSI, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc. Natl. Acad. Sci. USA 96, 7110–7115.

    Article  PubMed  CAS  Google Scholar 

  • Vatamaniuk, O.K., Mari, S., Lu, Y. P., Rea, P.A. (2000). Mechanism of heavy metal activation of phytochelatin (PC) synthase. J. Biol. Chem. 275, 31451–31459.

    Article  PubMed  CAS  Google Scholar 

  • Vatamaniuk, O.K., Bucher, E.A., Ward, J.T., Rea, P.A. (2001). A new pathway for heavy metal detoxification in animals. J. Biol. Chem. 276, 20817–20820.

    Article  PubMed  CAS  Google Scholar 

  • Verkleij, J.A.C., Koevoets, P., van’t Riet, J., Bark, R., Mijdam, Y., Ernst, W.H.O. (1990). Poly(yglutamylcysteinyl)-glycines or phytochelatins and their role in cadmium tolerance of Silene vulgaris. Plant Cell Environ. 13, 913–921.

    Article  CAS  Google Scholar 

  • Vögeli-Lange, R., Wagner, G.J. (1990). Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Plant Physiol. 92, 1086–1093.

    Article  PubMed  Google Scholar 

  • Vögeli-Lange, R., Wagner, G.J. (1996). Relationship between cadmium, glutathione and cadmium-binding peptides (phytochelatins) in leaves of intact tobacco seedlings. Plant Sci. 114, 11–18.

    Article  Google Scholar 

  • Wagner, G.J. (1993). Accumulation of cadmium in crop plants and its consequences to human health. Adv. Agron. 51, 173–212.

    Article  CAS  Google Scholar 

  • Wagner, G.J. (1995). Assessing cadmium partitioning in transgenic plants. In: Methods in molecular biology, vol. 44: Agrobacterium protocols, K.M.A. Gartland, M.R. Davey (Eds.). Humana Press Inc., Totowa, pp. 295–308.

    Google Scholar 

  • Xiang, C., Oliver, D.J. (1998). Glutathione metabolic genes co-ordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10, 1539–1550.

    PubMed  CAS  Google Scholar 

  • Yan, S.L., Tsay, C.C., Chen, Y.R. (2000). Isolation and characterization of phytochelatin synthase in rice seedlings. Proc. Natl. Sci. Counc. Repub. China 24, 202–207.

    CAS  Google Scholar 

  • Yen, T.-Y., Villa, J.A., DeWitt, J.G. (1999). Analysis of phytochelatin-cadmium complexes from plant tissue culture using nano-electrospray ionization tandem mass spectrometry and capillary liquid chromatography/electrophoresis ionization tandem mass spectrometry. J. Mass Spectrom. 34, 930–941.

    Article  PubMed  CAS  Google Scholar 

  • Yu, W., Santhanagopalan, V., Sewell, A.K., Jensen, L.T., Winge, D.R. (1994). Dominance of metallothionein in metal ion buffering in yeast capable of synthesis of (yEC)„G isopeptides. J. Biol. Chem. 269, 21010–21015.

    PubMed  CAS  Google Scholar 

  • Zayed, A.M., Terry, N. (1992). Selenium volatilisation in broccoli as influenced by sulphate supply. J. Plant Physiol. 140, 646–652.

    Article  CAS  Google Scholar 

  • Zenk, M.H. (1996). Heavy metal detoxification in higher plants–a review. Gene 179, 21–30.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, Y.L., Pilon-Smits, E.A.H., Jouanin, L., Terry, N. (1999a). Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol. 119, 73–79.

    Article  CAS  Google Scholar 

  • Zhu, Y.L., Pilon-Smits, E.A.H., Tarun, A.S., Weber, S.U., Jouanin, L, Terry, N. (1999b). Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing y-glutamylcysteine synthase. Plant Physiol. 121, 1169–1177.

    Google Scholar 

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Authors and Affiliations

  1. Department of Evolutionary and Functional Biology Section of Plant Biology, University of Parma, Parma, Italy

    L. Sanità Di Toppi

  2. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, India

    M. N. V. Prasad

  3. Department of Biochemistry and Molecular Biology, University of Parma, Parma, Italy

    S. Ottonello

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  1. Department of Plant Sciences, University of Hyderabad, 500046, Hyderabad, India

    M. N. V. Prasad

  2. Department of Plant Physiology and Biochemistry, The Institute of Molecular Biology, Jagiellonian University, 7 Gronostajowa Street, PL 30-387, Kraków, Poland

    Kazimierz Strzałka

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Sanità Di Toppi, L., Prasad, M.N.V., Ottonello, S. (2002). Metal Chelating Peptides and Proteins in Plants. In: Prasad, M.N.V., Strzałka, K. (eds) Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-2660-3_3

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