Photosynthetic organisms and excess of metals

Photosynthetica

Volumn 43, Issue 3, 2005, Pages 345-353

  Bertrand, M ^a   Poirier, I ^a  

^a Bioinformatique et Chimie Moléculaire   (France)

Author keywords

Chloroplast; Oxidative stress; Photosynthesis; Thylakoid membrane; Xanthophyll cycle

Indexed keywords

EID: 26444545040     PISSN: 03003604     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11099-005-0058-2     Document Type: Review

References (120)

1. Abadia, A., Lemoine, Y., Trémolières, A., Ambard-Bretteville, F., Rémy, R.: Iron deficiency in pea: effects on pigment, lipid and pigment-protein complex composition of thylakoids. - Plant Physiol. Biochem. 27: 679-687, 1989.
2. Abd-El-Monem, M., Corradi, M.G., Gorbi, G.: Toxicity of copper and zinc to two strains of Scenedesmus acutus having different sensitivity to chromium. - Environ. exp. Bot. 40: 59-66, 1998.
3. Aravind, P., Prasad, M.N.V.: Zn protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte. - Plant Sci. 166: 1321-1327, 2004.
4. Archambault, D.J., Zhang, G., Taylor, G.J.: Accumulation of Al in root mucilage of an Al-resistant and an Al-sensitive cultivar of wheat. - Plant Physiol. 112: 1471-1478, 1996.
5. Atal, N., Saradhi, P.P., Mohanty, P.: Inhibition of the chloroplast photochemical reactions by treatment of wheat seedlings with low concentrations of cadmium: Analysis of electron transport activities and changes in fluorescence yield. - Plant Cell Physiol. 32: 943-951, 1991.
6. Backor, M., Hudak, J., Backorova, M.: Comparison between growth responses of autotrophic and heterotrophic population of lichen photobiont Trebouxia (Chlorophyta) on Cu, Hg and Cd chloride treatments. - Phyton Ann. Rei bot. A 38: 239-250, 1998.
7. Backor, M., Vaczi, P.: Copper tolerance in the lichen photobiont Trebouxia erici (Chlorophyta). - Environ. exp. Bot. 48: 11-20, 2001.
8. Barceló, J., Vázquez, M.D., Poschenrieder, C.: Structural and ultrastructural disorders in cadmium-treated bush bean plants (Phaseolus vulgaris L.). - New Phytol. 108: 37-49, 1988.
9. Baryla, A., Carrier, P., Franck, F., Coulomb. C., Sahut, C., Havaux, M.: Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. - Planta 212: 696-709, 2001.
10. Baszyński, T., Wajda, L., Król, M., Wolińska, D., Krupa, Z., Tukendorf, A.: Photosynthetic activities of cadmium-treated tomato plants. - Physiol. Plant. 48: 365-370, 1980.
11. Benemann, J.: Literature review on the use of bioaccumulation for heavy metal removal and recovery. - WSRC-TR-175. Vol. 2. Westinghouse Savannah River Co., Aiken 1991.
12. 2+) on the hydrolytic activity of chloroplast ATPase. - J. Bioenerg. Biomembr. 33: 93-98, 2001.
13. Bertrand, M., Guary, J.C., Schoefs, B.: How plants adapt their physiology to an excess of metal. - In: Pessarakli, M. (ed.): Handbook of Plant and Crop Physiology. Pp. 751-761. Marcel Dekker, New York 2001a.
14. Bertrand, M., Schoefs, B., Šiffel, P., Roháček, K., Molnar, I.: Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum. - FEBS Lett. 508: 153-156, 2001b.
15. Blamey, F.P.C., Joyce, D.C., Edwards, D.G., Asher, C.J.: Role of trichomes in sunflower tolerance to manganese toxicity. - Plant Soil 91: 171-180, 1986.
16. Brune, A., Urbach, W., Dietz, K.-J.: Compartmentation and transport of zinc in barley primary leaves as basic mechanisms involved in zinc tolerance. - Plant Cell Environ. 17: 153-162, 1994.
17. Cakmak, L.: Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. - New Phytol. 146: 185-205, 2000.
18. Carrier, P., Baryla, A., Havaux, M.: Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. - Planta 216: 939-950, 2003.
19. Caspi, V., Droppa, M., Horváth, G., Malkin, S., Marder, J.B., Raskin, V.I.: The effect of copper on chlorophyll organization during greening of barley leaves. - Photosynth. Res. 62: 165-174, 1999.
20. Chettri, M.K., Cook, C.M., Vardaka, E., Sawidis, T., Larranas, T.: The effect of Cu, Zn and Pb on the chlorophyll content of the lichen Cladonia convoluta and Cladonia rangiformis. - Environ. exp. Bot. 39: 1-10, 1998.
21. Cho, U.H., Sohn, J.Y.: Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and lipid peroxidation in Arabidopsis thatliana. - J. Plant Biol. 47: 262-269, 2004.
22. Chvapil, M.: New aspects in the biological role of zinc: a stabilizer of macromolecules and biological membranes. - Life Sci. 13: 1041-1049, 1973.
23. Clijsters, H., Van Assche, F.: Inhibition of photosynthesis by heavy metals. - Photosynth. Res. 70: 31-40, 1985.
24. Cobbett, C.S.: Phytochelatins and their roles in heavy metal detoxification. - Plant Physiol. 123: 825-832, 2000.
25. Connolly, E.L., Guerinot, M.L.: Iron stress in plants. - Genome Biol. 3: 1024.1-1024.4, 2002.
26. Conway, H.L.: Sorption of arsenic and cadmium and their effects on growth, micronutrient utilization, and photosynthetic pigment composition of Asterionella formosa. - J. Fish. Res. Board Can. 35: 286-294, 1978.
27. De Filippis, L.F., Ziegler, H.: Effect of sublethal concentrations of zinc, cadmium and mercury on the photosynthetic carbon reduction cycle of Euglena. - J. Plant Physiol. 142: 167-172, 1993.
28. 2+ on ion transport systems of the plant plasmalemma. - Plant Physiol. 114: 1313-1325, 1997.
29. De Vos, C.H.R., Schat, H.: Free radicals and heavy metal tolerance. - In: Rozema, J., Verkleij, J.A.C. (ed.): Ecological Responses to Environmental Stresses. Pp. 22-30. Kluwer Academic Publ., Dordrecht 1991.
30. 2-dependent acidification of the leaf vacuole upon illumination. - Biochim. biophys. Acta 1373: 87-92, 1998.
31. Ernst, W.H.O., Neilssen, H.J.M., Ten Bookum, W.M.: Combination toxicology of metal-enriched soils: physiological responses of a Zn- and Cd-resistant ecotype of Silene vulgaris on polymetallic soils. - Environ. exp. Bot. 43: 55-71, 2000.
32. Ferro, M., Salvis, D., Brugière, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J., Rolland, N.: Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. - Mol. cell. Proteom. 2: 325-345, 2003.
33. Fodor, F., Böddi, B., Sárvári, É., Záray, G., Cseh, E., Láng, F.: Correlation of iron content, spectral forms of chlorophyll and chlorophyll-proteins in iron deficient cucumber (Cucumis sativus). - Physiol. Plant. 93: 750-756, 1995.
34. Fourest, E., Volesky, B.: Alginate properties and heavy metal biosorption by marine algae. - Appl. Biochem. Biotechnol. 61: 33-44, 1997.
35. Foy, C.D., Chaney, R.L., White, M.C.: The physiology of metal toxicity in plants. - Annu. Rev. Plant Physiol. 29: 511-566, 1978.
36. Gallego, S.M., Benavides, M.P., Tomaro, M.L.: Effect of heavy metal ion excess on suflower leaves evidence for involvement of oxidative stress. - Plant Sci. 121: 151-159, 1996.
37. Gekeler, W., Grill, E., Winnacker, E.L., Zenk, M.H.: Survey of the plant kingdom from the ability to bind heavy metals through phytochelatins. - Z. Naturforsch. 44c: 361-369, 1989.
38. Goyald, R., Seaward, M.R.D.: Metal uptake in terricolous lichens. I. Metal localization within the thallus. - New Phytol. 89: 631-645, 1981.
39. Goyald, R., Seaward, M.R.D.: Metal uptake in terricolous lichens. III. Translocation in the thallus of Peltigera canina. - New Phytol. 90: 85-98, 1982.
40. Hale, K.L., McGrath, S.P., Lombi, E., Stack, S.M., Terry, N., Pickering, I.J., George, G.N., Pilon-Smits, E.A.H.: Molybdenum sequestration in Brassica species. A role for anthocyanins? - Plant Physiol. 126: 1391-1402, 2001.
41. Hernandez, E., Olguin, E.J.: Biosorption of heavy metals influenced by the chemical composition of Spirulina sp. (Arthrospira) biomass. - Environ. Technol. 23: 1369-1377, 2002.
42. Jorge, R.A., Arruda, P.: Aluminium-induced organic acids exudation by roots of an aluminium-tolerant tropical maize. - Phytochemistry 45: 675-681, 1997.
43. Kobayashi, J.S., Kakizono, T., Nishio, N., Nagai, S., Kurimara, Y., Tsuji, Y.: Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. - Appl. Microbiol. Biotechnol. 48: 351-356, 1997.
44. Kochian, L.V., Pence, N.S., Letham, D.L.D., Pineros, M.A., Jurandir, V.M., Hoekenga, O.A., Garvin, D.F.: Mechanisms of metal resistance in plants: aluminium and heavy metals. - Plant Soil 247: 109-119, 2002.
45. Kroth, P.G.: Protein transport into secondary plastids and the evolution of primary and secondary plastids. - Int. Rev. Cytol. 221: 191-255, 2002.
46. Krupa, Z., Skórzyńska, E., Maksymiec, W., Baszyński, T.: Effect of cadmium treatment on the photosynthetic apparatus and its photochemical activities in greening radish seedlings. - Photosynthetica 21: 156-164, 1987.
47. Küpper, H., Küpper, F., Spiller, M.: Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. - J. exp. Bot. 47: 259-266, 1996.
48. Küpper, H., Küpper, F., Spiller, M.: In situ detection of heavy metal substituted chlorophylls in water plants. - Photosynth. Res. 58: 123-133, 1998.
49. Lu, C.M., Chau, C.W., Zhang, J.H.: Acute toxicity of excess mercury on the photosynthetic performance of cyanobacterium, S. platensis - assessment by chlorophyll fluorescence analysis. - Chemosphere 41: 191-196, 2000.
50. Luna, C.M., Gonzalez, C.A., Trippi, V.S.: Oxidative damage caused by an excess of copper in oat leaves. - Plant Cell Physiol. 35: 11-15, 1994.
51. Luo, H., Lu, Y., Shi, X., Mao, Y., Delal, N.S.: Chromium (IV)-mediated Fenton-like reaction causes DNA damage: implication to genotoxicity of chromate. - Ann. clin. lab. Sci. 26: 85-191, 1996.
52. Ma, J.F., Ryan, P.R., Delhaize, E.: Aluminium tolerance in plants and the complexing role of organic acids. - Trends Plant Sci. 6: 273-278, 2001.
53. Macfie, S.M., Wellbourn, P.M.: The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). - Arch. environ. Contam. Toxicol. 39: 413-419, 2000.
54. Malaga, G., Calmanovici, G., Puntarulo, S.: Oxidative damage to chloroplasts from Chlorella vulgaris exposed to ultraviolet-b radiation. - Physiol. Plant. 101: 455-462, 1997.
55. Malik, D., Sheoran, I.S., Singh, R.: Carbon metabolism in leaves of cadmium treated wheat seedlings. - Plant Physiol. Biochem. 30: 223-229, 1992.
56. Mallick, N.: Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris: response of the antioxidant system. - J. Plant Physiol. 161: 591-597, 2004.
57. Mallick, N., Mohn, F.H.: Reactive oxygen species: response of algal cells. - J. Plant Physiol. 157: 183-193, 2000.
58. Mallick, N., Rai, L.C.: Responses of the antioxidant systems of the nitrogen fixing cyanobacterium Anabaena doliolum to copper. - J. Plant Physiol. 155: 146-149, 1999.
59. Mascher, R., Lippmann, B., Holzinger, S., Bergmann, H.: Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. - Plant Sci. 163: 961-969, 2002.
60. Meharg, A.A.: Integrated tolerance mechanisms - constitutive and adaptative plant-responses to elevated metal concentrations in the environment. - Plant Cell Environ. 17: 989-993, 1994.
61. 2+ transport and storage in the chloroplast of Euglena gracilis. - Biochim. biophys. Acta 1706: 88-97, 2005.
62. Mithöfer, A., Schulze, B., Boland, W.: Biotic and heavy metal stress response in plants: evidence for common signals. - FEBS Lett. 566: 1-5, 2004.
63. Mohanty, N., Mohanty, P.: Cation effects on primary processes of photosynthesis. - In: Singh, R., Sawhney, S.K. (ed.): Advances in Frontier Areas of Plant Biochemistry. Pp. 1-18. Prentice-Hall, New Delhi 1988.
64. 2 fixation, and Zn, Mn and Mg contents of Lolium perenne under zinc stress. - J. Plant Physiol. 158: 1137-1144, 2001.
65. Mullineaux, P., Karpinski, S.: Signal transduction in response to excess light: getting out of the chloroplast. - Curr. Opin. Plant Biol. 5: 43-48, 2002.
66. nd Ed. Pp. 146-181. Springer-Verlag, Heidelberg 2003.
67. Myśliwa-Kurdziel, M., Strzałka, K.: Influence of metals on the biosynthesis of photosynthetic pigments. - In: Prasad, M.N.V., Strzałka, K. (ed.): Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Pp. 201-228. Kluwer Academic Publ., Dordrecht 2002.
68. Myśliwa-Kurdziel, B., Strzałka, K.: Influence of Cd(II), Cr(VI) and Fe(III) on early steps of deetiolation process in wheat: fluorescence spectral changes of protochlorophyllide and newly formed chlorophyllide. - Agr. Ecosys. Environ. 106: 199-207, 2004.
69. Nagel, K., Adelmeier, U., Voigt, J.: Subcellular distribution of cadmium in the unicellular green alga Chlamydomonas reinhardtii. - J. Plant Physiol. 149: 86-90, 1996.
70. Navari-Izzo, F., Quartacci, M.F.: Phytoremediation of metals. - Minerva Biotech. 13: 73-83, 2001.
71. Ochiai, E.I.: General Principles of Biochemistry of the Elements. - Plenum Press, New York 1987.
72. Olmos, E., Martinez-Solano, J.R., Piqueras, A., Hellin, E.: Early steps in oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). - J. exp. Bot. 54: 291-301, 2003.
73. Ouzounidou, G., Eleftheriou, E.P., Karataglis, S.: Ecophysiological and ultrastructural effects of copper in Thlapsi ochroleucum (Cruciferae). - Can. J. Bot. 70: 947-957, 1992.
74. Päivöke, A.E.A.: Soil pollution alters ATP and chlorophyll contents in Pisum sativum seedlings. - Biol. Plant. 46: 145-148, 2003.
75. Parker, D.L., Mihalick, J.E., Plude, J.L., Plude, M.J., Clark, T.P., Egan, L., Flom, J.J., Rai, L.C., Kumar, H.D.: Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f. flos-aquae strain C3-40. - J. appl. Phycol. 12: 219-224, 2000.
76. Pätsikkä, E., Kairavuo, M., Šeršen, F., Aro, E.M., Tyystijärvi, E.: Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. - Plant Physiol. 129: 1-9, 2002.
77. Pellet, D.M., Papernik, L.A., Kochian, L.V.: Multiple aluminium-resistance mechanisms in wheat. - Plant Physiol. 112: 591-597, 1996.
78. Pistocchi, R., Mormile, A.M., Guerrini, F., Isani, G., Boni, L.: Increased production of extra- and intracellular metal-ligands in phytoplankton exposed to copper and cadmium. - J. appl. Phycol. 12: 469-477, 2000.
79. Prasad, M.N.V.: Cadmium toxicity and tolerance to vascular plants. - Environ. exp. Bot. 35: 525-545, 1995.
80. Prasad, M.N.V., Strzałka, K.: Impact of heavy metals on photosynthesis. - In: Prasad, M.N.V., Hagenmeyer, J. (ed.): Heavy Metal Stress in Plants - From Molecules to Ecosystems. Pp. 117-138. Springer-Verlag, Berlin 1999.
81. Quartacci, M.F., Pinzino, C., Sgherri, C.L.M., Dalla Vecchia, F., Navari-Izzo, F.: Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. - Physiol. Plant. 108: 87-93, 2000.
82. Ralph, P.J., Burchett, M.D.: Photosynthesis response of Halophila ovalis to heavy metal stress. - Environ. Pollut. 103: 91-101, 1998.
83. Rauser, W.E.: Structure and function of metal chelators produced by plants. - Cell Biochem. Biophys. 31: 1-30, 1999.
84. Roháček, K., Barták, M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. - Photosynthetica 37: 339-363, 1999.
85. Romero-Puertas, M.C., Palma, J.M., Gómez, M., Del Río, L.A., Sandalio, L.M.: Cadmium causes the oxidative modification of proteins in pea plants. - Plant Cell Environ. 25: 677-686, 2002.
86. Salt, D.E., Prince, R.C., Pichering, I.J., Raskin, I.: Mechanisms of cadmium immobilization and accumulation in Indian mustard. - Plant Physiol. 109: 427-433, 1995.
87. Sanità di Toppi, L., Gabbrielli, R.: Response to cadmium in higher plants. - Environ. exp. Bot. 41: 105-130, 1999.
88. Sanità di Toppi, L., Gremigni, P., Pawlik-Skowronska, B., Prasad, M.N.V., Cobbett, C.S.: Responses to heavy metals in plant molecular approach. - In: Sanità di Toppi, L., Pawlik-Skowronska, B. (ed.): Abiotic Stresses in Plants. Pp. 33-156. Kluwer Academic Publ., Dordrecht 2003.
89. Sárvári, É., Fodor, F., Cheh, E., Varga, A., Záray, G., Zolla, L.: Relationship between changes in ion content of leaves and chlorophyll-protein composition in cucumber under Cd and Pb stress. - Z. Naturforsch. 54c: 746-753, 1999.
90. Schmidt, W.: Mechanisms and regulation of reduction-based iron uptake in plants. - New Phytol. 141: 1-26, 1999.
91. nd Ed. Pp. 37-54. Taylor & Francis, Boca Raton - London - New York 2005.
92. Schoefs, B., Franck, F.: Protochlorophyllide reduction: Mechanisms and evolution. - Photochem. Photobiol. 78: 543-557, 2003.
93. Shukla, U.C., Singh, J., Joshi, P.C., Kakkar, P.: Effect of bioaccumulation of cadmium on biomass productivity, essential trace elements, chlorophyll biosynthesis, and macromolecules of wheat seedlings. - Biol. Trace Elem. Res. 92: 257-273, 2003.
94. Sicko-Goad, L.: A morphometric analysis of algal response to low dose, short term heavy metal exposure. - Protoplasma 110: 75-86, 1982.
95. Siedlecka, A.: Some aspects of interactions between heavy metals and plant mineral nutrients. - Acta Soc. Bot. Pol. 3: 265-272, 1995.
96. Sobkowiak, R., Rymer, K., Rucińska, R., Deckert, J.: Cadmium-induced changes in antioxidant enzymes in suspension culture of soybean cells. - Acta biochim. pol. 51: 219-222, 2004.
97. 2+ reacts with different components of the NADPH:protochlorophyllide oxidoreductase macrodomains. - Plant Biol. 6: 358-363, 2004.
98. Souza, J.F., Rauser, W.E.: Maize and radish sequester excess cadmium and zinc in different ways. - Plant Sci. 65: 1009-1022, 2003.
99. Stiborová, M., Ditrichová, M., Březinová, A.: Effect of heavy metal ions on growth and biochemical characteristics of photosynthesis of barley and maize seedlings. - Biol. Plant. 29: 453-467, 1987.
100. Stohs, S.J., Bagchi, D.: Oxidative mechanisms in the toxicity of metal ions. - Free Rad. Biol. Med. 18: 321-336, 1995.
101. Stoyanova, D., Tchakalova, T.: Cadmium induced ultrastructural changes in shoot apical meristem of Elodea canadensis Rich. - Photosynthetica 37: 47-52, 1999.
102. Subrahmanyam, D., Rathore, V.S.: Influence of manganese toxicity on photosynthesis in ricebean (Vigna umbellata) seedlings. - Photosynthetica 38: 449-453, 2000.
103. Teige, M., Huchzermeyer, B., Schultz, G.: Inhibition of chloroplast ATPsynthase/ATPase is a primary effect of heavy metal toxicity in spinach plants. - Biochem. Physiol. Pflanzen 186: 165-168, 1990.
104. Tewari, R.K., Kumar, P., Sharma, P.N., Bisht, S.S.: Modulation of oxidative stress responsive enzymes by excess cobalt. - Plant Sci. 162: 381-388, 2002.
105. 2+ ion treatment. - Photosynthetica 40: 103-108, 2002.
106. Vaillant, N., Monnet, F., Hitmi, A., Sallanon, H., Coudret, A.: Comparative study of responses in four Datura species to a zinc stress. - Chemosphere (in press), 2004.
107. Van Duijvendijk-Matteoli, M.A., Desmet, G.M.: On the inhibitory action of cadmium on the donor side of Photosystem II in isolated chloroplasts. - Biochim. biophys. Acta 408: 164-168, 1975.
108. Vangronsveld, J., Clijsters, H.: Toxic effect of metals. - In: Farango, M.E. (ed.): Plants and the Chemical Elements. Pp. 149-177. VCH Verslagsgesellschaft, Weinheim 1994.
109. Vassilev, A., Iordanov, I., Chakalova, E., Derin, V.: Effect of cadmium stress on growth and photosynthesis of young barley (Hordeum vulgare) plants. 2. Structural and functional changes in the photosynthetic apparatus. - Bulg. J. Plant Physiol. 21: 12-21, 1995.
110. Vazquez, M.D., Poschenrieder, C., Barcelo, J.: Ultrastructural effects and localization of low cadmium concentrations in bean roots. - New Phytol. 120: 215-226, 1992.
111. Vazquez, M.D., Poschenrieder, C., Barcelo, J., Baker, A.J.M., Hatton, P., Cope, G.H.: Compartmentation of zinc in roots and leaves of the zinc hyperaccumulator Thlaspi caerulescens. - Bot. Acta 107: 243-250, 1994.
112. Vögeli-Lange, R., Wagner, G.L.: Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves. Implication of a transport function for cadmium-binding peptides. - Plant Physiol. 92: 1086-1093, 1990.
113. 2+-tolerant mutant strain of the unicellular green alga Chlamydomonas reinhardtii. - J. Plant Physiol. 159: 941-950, 2002.
114. Voigt, J., Nagel, K., Wrann, D.: A cadmium-tolerant Chlamydomonas mutant strain impaired in photosystem II activity. - J. Plant Physiol. 153: 566-573, 1998.
115. Wallace, A., Wallace, G.A., Cha, J.W.: Some modifications in trace metal toxicities and deficiencies in plants resulting from interactions with other elements and chelating agents: the special case of iron. - J. Plant Nutr. 15: 1589-1598, 1992.
116. Williams, L.E., Pittman, J.K., Hall, J.L.: Emerging mechanisms for heavy metal transport in plants. - Biochim. biophys. Acta 1465: 104-126, 2000.
117. Wisniewski, L., Dickinson, N.M.: Toxicity of copper to Quercus robur (English Oak) seedlings from a copper-rich soil. - Environ. exp. Bot. 50: 99-107, 2003.
118. Wu, F., Zhang, G., Dominy, P.: Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. - Environ. exp. Bot. 50: 67-78, 2003.
119. Yruela, I., Montoya, G., Picorel, R.: The inhibitory mechanism of Cu(II) on the Photosystem II electron transport from higher plants. - Photosynth. Res. 33: 227-233, 1992.
120. Zenk, M.H.: Heavy metal detoxification in plants - A review. - Gene 179: 21-30, 1996.