Abstract
Metal-tolerant Datura innoxia cells synthesize large amounts of cadystin, [poly(γ-glutamylcysteinyl) glycines, (γ-EC)nG, n=2–5], a class of metal-binding polypeptides, when exposed to Cd. These polypeptides have a high affinity for Cd (II) and certain other metal ions and are thought to play a role in metal tolerance in higher plants. Cells rapidly synthesize these metal-binding polypeptides when exposed to Cd and cellular concentrations of glutathione and cysteine, precursors for the synthesis of these compounds, are initially depleted then rapidly replenished. The time-frame of de novo polypeptide, glutathione and cysteine biosynthesis suggests that this pathway is, at least initially, regulated at the enzyme level. Significant amounts of Fe are associated with Cd: polypeptide complexes isolated from D. innoxia. Exposure of cultures to Cd results in an increased Fe accumulation by the cells. All the additional Fe found in the soluble portion of cell extracts is associated with the Cd: polypeptide complexes. The physiological significance of the synthesis of these polypeptides and their precursors and its relevance to Cd tolerance and metal homeostasis are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Cheblowski J F and Coleman J E 1976 Zinc and its role in enzymes. In Metal Ions in Biological Systems. Vol. 6, Biological Action of Metal Ions. Ed. H Sigel. pp 1–140. Marcel Dekker, Inc., New York.
Gaitonde M K 1967 A spectroscopic method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem. J. 104, 627–633.
Gekeler W, Grill E, Winnacker E-L and Zenk M H 1989 Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins. Z. Naturforsch. 44, 361–369.
Grill E, Löffler S, Winnacker E-L and Zenk M H 1989 Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc. Natl. Acad. Sci. USA 86, 6838–6842.
Grill E, Winnacker E-L and Zenk M H 1987 Phytochelatins, a class of heavy-metal-binding peptides from plants are functionally analogous to metallothioneins. Proc. Natl. Acad. Sci. USA. 84, 439–443.
Hayashi Y, Nakagawa C W, Mutoh N, Isobe M and Goto T 1991 Two pathways in the biosynthesis of cadystins (γ-EC)nG in the cell-free system of the fission yeast. Biochem. Cell Biol. 69, 115–121.
Jackson P J, Naranjo C M, McClure P R and Roth E J 1985 The molecular response of cadmium resistant Datura innoxia cells to heavy metal stress. In Cellular and Molecular Biology of Plant Stress. Eds. J L Key and T Kosuge. pp 145–160. Alan R. Liss, New York.
Jackson P J, Roth E J, McClure P R and Naranjo C M 1984 Selection, isolation, and characterization of cadmium-resistant Datura innoxia suspension cultures. Plant Physiol. 75, 914–918.
Jackson P J, Unkefer C J, Doolen J A, Watt K and Robinson N J 1987 Poly(γ-glutamylcysteinyl)glycine: Its role in cadmium resistance in plant cells. Proc. Natl. Acad. Sci. USA. 84, 6619–6623.
Jackson P J, Unkefer P J, Delhaize E and Robinson N J 1990 Mechanisms of trace metal tolerance in plants. In Environmental Injury to Plants. Ed. F Katterman. pp 231–255. Academic Press, New York.
Kondo N, Isobe M, Imai K, Goto T and Murasugi A. 1983 Structure of cadystin, the unit-peptide of cadmium-binding peptides induced in a fission yeast, Schizosaccharomyces pombe. Tetrahderon Lett. 24, 925–928.
Kondo N, Imai K, Isobe M and Goto T 1984 Cadystin A and B major unit peptides comprising cadmium binding peptides induced in a fission yeast — Separation, revision of structures and synthesis. Tetrahedron Lett. 25, 3869–3872.
Lindberg S and Wingstrand O 1985 Mechanism for Cd2+ inhibition of (K++Mg2+) ATPase activity and K+ (86Rb+) uptake in roots of sugar beet (Beta vulgaris). Physiol. Plant. 63, 181–186.
Natusch D F S, Wallace J R and Evans C A 1974 Toxic trace elements: Preferential concentration in respirable particles. Science 183, 202–204.
Nieboer E, Richardson D H S, Lavoie P and Padovan D 1979 The role of metal-ion binding in modifying the toxic effects of sulfur dioxide on the lichen Umbilicaria muhlenbergii: 1. Potassium efflux studies. New Phytol. 82, 621–632.
Okumura N, Nishizawa N-K, Umehara Y and Mori S 1991 An iron deficiency-specific cDNA from barley roots having two homologous cysteine-rich MT domains. Plant Molec. Biol. 17, 531–533.
Perrin D D and Watt A E 1971 Complex formation of zinc and cadmium with glutathione. Biochim. Biophys. Acta 230, 96–104.
Petolino J F and Collins G B 1985 Manganese toxicity in tobacco (Nicotiana tabacum L.) callus and seedlings. J. Plant Physiol. 118, 139–144.
Reese N R and Roberts L W 1985 Effects of cadmium on whole cell and mitochondrial respiration in tobacco cell suspension cultures (Nicotiana tabacum L. var. xanthi). J. Plant Physiol. 120, 123–130.
Robinson N J 1989 Algal metallothioneins: Secondary metabolites and proteins. J. Appl. Phycol. 1, 5–18.
Robinson N J and Jackson P J 1986 ‘Metallothionein-like’ metal complexes in angiosperms: Their structure and function. Physiol. Plant. 67, 499–506.
Robinson N J, Ratliff R L, Anderson P J, Delhaize E, Berger J M and Jackson P J 1988 Biosynthesis of poly(γ-glutamylcysteinyl)glycines in cadmium-tolerant Datura innoxia (Mill.) cells. Plant Science 56, 197–204.
Singhai R K, Anderson M E and Meister A 1987 Glutathione, a first line of defense against cadmium toxicity. FASEB J. 1, 220–223.
Steffens J C, Hunt D F and Williams B G 1986 Accumulation of non-protein metal-binding polypeptides (γ-glutamylcysteinyl)nglycine in selected cadmium-resistant tomato cells. J. biol. Chem. 261, 13879–13882.
Stobart A K, Griffiths W T, Ameen-Bukhari I and Sherwood R P 1985 The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol. Plant. 63, 293–298.
Street J J, Sabey B R and Lindsay W L 1978 Influence of pH, phosphorus, cadmium, sewage sludge, and incubation time on the solubility and plant uptake of cadmium. J. Environ. Qual. 7, 286–290.
Takijima Y and Katsumi F 1973a Cadmium contamination of soils and rice plants caused by zinc mining: Production of high cadmium rice on the paddy fields in lower reaches of the mine station. Soil Sci. Plant Nutr. 19, 29–38.
Takijima Y and Katsumi F 1973b Cadmium contamination of soils and rice plants caused by zinc mining. IV. Use of Soil amendment materials for the control of Cd uptake by plants. Soil Sci. Plant Nutr. 19, 235–244.
VanBruwaene R, Kirchmann R and Impens R 1984 Cadmium contamination in agriculture and zootechnology. Experientia 40, 43–52.
Verkleij J A C, Koevoets P, Van't Riet J, Bank R, Nijdam Y and Ernst W H O 1991 Poly(γ-glutamylcysteinyl)glycines or phytochelatins and their role in cadmium tolerance of Silene vulgaris. Plant Cell Environ. 13, 913–922.
Vlamis J, Williams D E, Corey J E, Page A L and Ganje T J 1985 Zinc and cadmium uptake by barley in field plots fertilized seven years with urban and suburban sludge. Soil Sci. 139, 81–87.
Weigel H J 1985 Inhibition of photosynthetic reactions of isolated intact chloroplasts by cadmium. J. Plant Physiol. 119, 179–189.
Wikfors G H, Neeman A and Jackson P J 1991 Cadmiumbinding polypeptides in microalgal strains with laboratory-induced cadmium tolerance. Mar. Ecol. Prog. Ser. 79, 163–170.
Yoshimura E, Kabuyama Y, Yamazaki S and Toda S 1990 Activity of poly(γ-glutamylcysteinyl)-glycine synthesis in crude extract of fission yeast, Schizosaccharomyces pombe. Agric. Biol. Chem. 54, 3025–3026.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jackson, P.J., Delhaize, E. & Kuske, C.R. Biosynthesis and metabolic roles of cadystins (γ-EC)nG and their precursors in Datura innoxia . Plant Soil 146, 281–289 (1992). https://doi.org/10.1007/BF00012022
Issue Date:
DOI: https://doi.org/10.1007/BF00012022