Photosynthetica 2008, 46(4):481-489 | DOI: 10.1007/s11099-008-0083-z

Toxic metal ions in photoautotrophic organisms

T. Kučera1, H. Horáková1, A. Šonská1,*
1 Department of Biochemistry, Faculty of Science, Charles University in Prague, Prague, Czech Republic

We summarize the contemporary understanding of the effects of metal stress on various photosynthetic processes in photoautotrophic organisms and of the defence strategies employed by these organisms to avoid such stress. Cadmium is in the centre of interest of this review, as a non-essential element and important environmental pollutant, but Al, Pb, Hg, As, Cu, and Zn are also considered. Toxic metal ions pollute the environment through anthropogenic activities and affect the quality of plant crop. They represent one of the main abiotic stress factors influencing the health of plants and, as a secondary effect, of animals including man. The review summarizes the generally accepted answers to the questions: How do the toxic metal ions enter the photosynthetic organisms? How are they accumulated in plants? Which mechanisms do plants develop to tolerate metal stress and protect themselves?

Additional key words: abiotic stress; Al; As; Cd; Cu; Hg; photosynthesis; phytoremediation; toxic metals; Zn

Received: August 13, 2008; Accepted: October 8, 2008; Published: December 1, 2008  Show citation

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Kučera, T., Horáková, H., & Šonská, A. (2008). Toxic metal ions in photoautotrophic organisms. Photosynthetica46(4), 481-489. doi: 10.1007/s11099-008-0083-z
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References

  1. Abd-El-Monem, H.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. Go to original source...
  2. Aravind, P., Prasad, M.N.V.: Zinc protects chloroplasts and associated photochemical functions in cadmium exposed Ceratophyllum demersum L., a freshwater macrophyte.-Plant Sci. 166: 1321-1327, 2004. Go to original source...
  3. Backor, M., Vaczi, P.: Copper tolerance in the lichen photobiont Trebouxia erici (Chlorophyta).-Environ. exp. Bot. 48: 11-20, 2002. Go to original source...
  4. Bertrand, M., Poirier, I.: Photosynthetic organisms and excess of metals.-Photosynthetica 43: 345-353, 2005. Go to original source...
  5. Burzyński, M., Żurek, A.: Effects of copper and cadmium on photosynthesis in cucumber cotyledons.-Photosynthetica 45: 239-244, 2007. Go to original source...
  6. Cho, U.H., Seo, N.H.: Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation.-Plant Sci. 168: 113-120, 2005. Go to original source...
  7. Clemens, S., Palmgren, M.G., Kramer, U.: A long way ahead: understanding and engineering plant metal accumulation.-Trends Plant Sci. 7: 309-315, 2002. Go to original source...
  8. de la Fuente, J.M., Ramírez-Rodríguez, V., Cabrera-Ponce, J. L., Herrera-Estrella, L.: Aluminum tolerance in transgenic plants by alteration of citrate synthesis.-Science 276: 1566-1568, 1997. Go to original source...
  9. Drazkiewicz, M., Skorzynska-Polit, E., Krupa, Z.: Response of the ascorbate-glutathione cycle to excess copper in Arabidopsis thaliana (L.).-Plant Sci. 164: 195-202, 2003. Go to original source...
  10. Ebbs, S., Uchil, S.: Cadmium and zinc induced chlorosis in Indian mustard [Brassica juncea (L.) Czern] involves preferential loss of chlorophyll b.-Photosynthetica 46: 49-55, 2008. Go to original source...
  11. Ernst, W.H.O., Nelissen, 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. Go to original source...
  12. Faller, P., Kienzler, K., Krieger-Liszkay, A.: Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site.-Biochim. biophys. Acta 1706: 158-164, 2005. Go to original source...
  13. Gorinova, N., Nedkovska, M., Todorovska, E., Simova-Stoilova, L., Stoyanova, Z., Georgieva, K., Demirevska-Kepova, K., Atanassov, A., Herzig, R.: Improved phytoaccumulation of cadmium by genetically modified tobacco plants (Nicotiana tabacum L.). Physiological and biochemical response of the transformants to cadmium toxicity.-Environ. Pollut. 145: 161-170, 2007. Go to original source...
  14. Graeme, K.A., Pollack, C.V., Jr.: Heavy metal toxicity, part II: lead and metal fume fever.-J. Emerg. Med. 16: 171-177, 1998. Go to original source...
  15. Hall, J.L.: Cellular mechanisms for heavy metal detoxification and tolerance.-J. exp. Bot. 53: 1-11, 2002. Go to original source...
  16. Hartley-Whitaker, J., Ainsworth, G., Vooijs, R., Ten Bookum, W., Schat, H., Meharg, A.A.: Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus.-Plant Physiol. 126: 299-306, 2001. Go to original source...
  17. He, J.-Y., Ren, Y.-F., Zhu, C., Yan, Y.-P., Jiang, D.-A.: Effect of Cd on growth, photosynthetic gas exchange, and chlorophyll fluorescence of wild and Cd-sensitive mutant rice.-Photosynthetica 46: 466-470, 2008. Go to original source...
  18. Hou, W., Chen, X., Song, G., Wang, Q., Chang, C.C.: Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor).-Plant Physiol. Biochem. 45: 62-69, 2007. Go to original source...
  19. Issa, A.A., Abdel-Basset, R., Adam, M.S.: Abolition of heavy metal toxicity on Kirchneriella lunaris (Chlorophyta) by calcium.-Ann. Bot. 75: 189-192, 1995. Go to original source...
  20. Koh, E.J., Song, W.Y., Lee, Y.: Expression of yeast cadmium factor 1 (YCF1) confers salt tolerance to Arabidopsis thaliana.-Plant Sci. 170: 534-541, 2006. Go to original source...
  21. Kollmeier, M., Dietrich, P., Bauer, C.S., Horst, W.J., Hedrich, R.: Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminium-resistant cultivar.-Plant Physiol. 126: 397-410, 2001. Go to original source...
  22. Král'ová, K., Masarovičová, E., Lešíková, J., Ondrejkovičová, I.: Effects of Cd(II) and Zn(II) complexes with bioactive ligands on some photosynthesizing organisms.-Chem. Pap. 60: 149-153, 2006. Go to original source...
  23. Kramer, U.: Phytoremediation: novel approaches to cleaning up polluted soils.-Curr. Opin. Biotechnol. 16: 133-141, 2005. Go to original source...
  24. Kučera, T., Sofrová, D.: Oxygenic photoautotrophs: phosporylation and oligomeric state of photosystem 2. Responses to stress.-Collect. czech. Chem. Commun. 69: 564-588, 2004. Go to original source...
  25. Linger, P., Ostwald, A., Haensler, J.: Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis.-Biol. Plant. 49: 567-576, 2005. Go to original source...
  26. López-Bucio, J., Nieto-Jacobo, M.F., Ramírez-Rodríguez, V., Herrera-Estrella, L.: Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils.-Plant Sci. 160: 1-13, 2000. Go to original source...
  27. 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. Go to original source...
  28. Macnair, M.R.: The genetics of metal tolerance in vascular plants.-New Phytol. 124: 541-559, 1993. Go to original source...
  29. Macnair, M.R., Tilstone, G.H., Smith, S.E.: The genetics of metal tolerance and accumulation in higher plants.-In: Terry, N., Bañuelos, G. (ed.): Phytoremediation of Contaminated Soil and Water. Pp. 235-250. CRC Press, Boca Raton 2000. Go to original source...
  30. Maksymiec, W., Wojcik, M., Krupa, Z.: Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate.-Chemosphere 66: 421-427, 2007. Go to original source...
  31. Masarovičová, E., Cicák, A., Štefančík, I.: Plant responses to air pollution and heavy metal stresses.-In: Pessarakli, M. (ed.): Handbook of Plant and Crop Stress. Pp. 569-598. Marcel Dekker, New York-Basel 1999. Go to original source...
  32. Meharg, A.A.: Mechanisms of plant resistance to metal and metalloid ions and potential biotechnological applications.-Plant Soil 274: 163-174, 2005. Go to original source...
  33. Mendez-Alvarez, S., Leisinger, U., Eggen, R.I.L.: Adaptive responses in Chlamydomonas reinhardtii.-Int. Microbiol. 2: 15-22, 1999.
  34. Mendoza-Cozatl, D.G., Moreno-Sanchez, R.: Cd2+ transport and storage in the chloroplast of Euglena gracilis.-Biochim. biophys. Acta 1706: 88-97, 2005. Go to original source...
  35. Mihailovic, N., Drazic, G., Vucinic, Z.: Effects of aluminium on photosynthetic performance in Al-sensitive and Al-tolerant maize inbred lines.-Photosynthetica 46: 476-480, 2008. Go to original source...
  36. Mishra, S., Srivastava, S., Tripathi, R.D., Kumar, R., Seth, C.S., Gupta, D.K.: Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation.-Chemosphere 65: 1027-1039, 2006. Go to original source...
  37. Nagalakshmi, N., Prasad, M.N.V.: Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus.-Plant Sci. 160: 291-299, 2001. Go to original source...
  38. Nováková, M., Matějová, E., Sofrová, D.: Cd2+ effect on photosynthetic apparatus in Synechococcus elongatus and spinach (Spinacia oleracea L.).-Photosynthetica 42: 425-430, 2004. Go to original source...
  39. Patra, M., Bhowmik, N., Bandopadhyay, B., Sharma, A.: Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance.-Environ. exp. Bot. 52: 199-223, 2004. Go to original source...
  40. Pellet, D.M., Papernik, L.A., Kochian, L.V.: Multiple aluminum-resistance mechanisms in wheat. Roles of root apical phosphate and malate exudation.-Plant Physiol. 112: 591-597, 1996. Go to original source...
  41. Piñeros, M.A., Kochian, L.V.: A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al3+-induced anion channels.-Plant Physiol. 125: 292-305, 2001. Go to original source...
  42. Prasad, M.N.V.: Cadmium toxicity and tolerance in vascular plants.-Environ. exp. Bot. 35: 525-545, 1995. Go to original source...
  43. Prasad, M.N.V., Malec, P., Waloszek, A., Bojko, M., Strzałka, K.: Physiological responses of Lemna trisulca L. (duckweed) to cadmium and copper bioaccumulation.-Plant Sci. 161: 881-889, 2001. Go to original source...
  44. Qadir, S., Qureshi, M.I., Javed, S., Abdin, M.Z.: Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress.-Plant Sci. 167: 1171-1181, 2004. Go to original source...
  45. Ryan, P.R., Skerrett, M., Findlay, G.P., Delhaize, E., Tyerman, S.D.: Aluminum activates an anion channel in the apical cells of wheat roots.-Proc. nat. Acad. Sci. USA 94: 6547-6552, 1997. Go to original source...
  46. Salt, D.E., Smith, R.D., Raskin, I.: Phytoremediation.-Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 643-668, 1998. Go to original source...
  47. Seth, C.S., Chaturvedi, P.K., Misra, V.: Toxic effect of arsenate and cadmium alone and in combination on giant duckweed (Spirodela polyrrhiza L.) in response to its accumulation.-Environ. Toxicol. 22: 539-549, 2007. Go to original source...
  48. Sheoran, I.S., Singhal, H.R., Singh, R.: Effect of cadmium and nickel on photosynthesis and the enzymes of the photosynthetic carbon reduction cycle in pigeonpea (Cajanus cajan L.).-Photosynth. Res. 23: 345-351, 1990. Go to original source...
  49. Siedlecka, A., Krupa, Z.: Cd/Fe interaction in higher plants - its consequences for the photosynthetic apparatus.-Photosynthetica 36: 321-331, 1999. Go to original source...
  50. Singh, R.P., Tripathi, R.D., Sinha, S.K., Maheshwari, R., Srivastava, H.S.: Response of higher plants to lead contaminated environment.-Chemosphere 34: 2467-2493, 1997. Go to original source...
  51. Sinha, S., Mallick, S., Misra, R.K., Singh, S., Basant, A., Gupta, A.K.: Uptake and translocation of metals in Spinacia oleracea L. grown on tannery sludge-amended and contaminated soils: Effect on lipid peroxidation, morpho-anatomical changes and antioxidants.-Chemosphere 67: 176-187, 2007. Go to original source...
  52. Stiborová, M., Doubravová, M., Leblová, S.: A comparative study of the effect of heavy metal ions on ribulose-1,5-bisphosphate carboxylase and phosphoenolpyruvate carboxylase.-Biochem. Physiol. Pflanz. 181: 373-379, 1986. Go to original source...
  53. Tůmová, E., Sofrová, D.: Response of intact cyanobacterial cells and their photosynthetic apparatus to Cd2+ ion treatment.-Photosynthetica 40: 103-108, 2002. Go to original source...
  54. Vaillant, N., Monnet, F., Hitmi A., Sallanon, H., Coudret, A.: Comparative study of responses in four Datura species to a zinc stress.-Chemosphere 59: 1005-1013, 2005. Go to original source...
  55. Williams, L., Pittman, J.K., Hall, J.L.: Emerging mechanisms for heavy metal transport in plants.-Biochim. biophys. Acta 1465: 104-126, 2000. Go to original source...
  56. 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. Go to original source...
  57. Zhang, W.-H., Ryan, P.R., Tyerman, S.D.: Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots.-Plant Physiol. 125: 1459-1472, 2001. Go to original source...
  58. Zhou, W., Qiu, B.S.: Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae).-Plant Sci. 169: 737-745, 2005. Go to original source...