Plant Biol (Stuttg) 2003; 5(3): 315-323
DOI: 10.1055/s-2003-40801
Original Paper

Georg Thieme Verlag Stuttgart · New York

Multiple Effects of Chromate on Spirodela polyrhiza: Electron Microscopy and Biochemical Investigations

K.-J. Appenroth 1 , Á. Keresztes 2 , É. Sárvári 3 , A. Jaglarz 4 , W. Fischer 1
  • 1University of Jena, Institute of General Botany and Plant Physiology, Jena, Germany
  • 2Eötvös Loránd University, Department of Plant Anatomy, Budapest, Hungary
  • 3Eötvös Loránd University, Department of Plant Physiology, Budapest, Hungary
  • 4University of Agriculture, Department of Biochemistry, Krakow, Poland
Further Information

Publication History

Publication Date:
22 July 2003 (online)

Abstract

Growth rates of S. polyrhiza were reduced by chromate concentrations higher than 50 µM. Analysis of plant cells by transmission electron microscopy revealed the accumulation of starch grains in the chloroplasts following the application of chromate at low concentrations or for short periods (100 µM for 2 days or 500 µM for 1 day). Increasing the chromate concentration (1000 µM for 1 day) or extending the period (100 µM for 4 days) resulted in the disappearance of most of the starch grains and the extensive formation of plastoglobuli. These results were confirmed by chemical analysis of the starch content. It has been suggested that this transient accumulation of starch was caused, first, by inhibition of the export of carbohydrates out of the plastids, and then by inhibition of photosynthesis. Chromate decreased the chlorophyll content and the chlorophyll a/b ratio. The quantitative analysis of the chlorophyll protein complexes showed that the photosystem II (core complex as well as connecting antenna) was more sensitive to chromate treatment than photosystem I and the peripheral light-harvesting complex of photosystem II. This explains the previous results on time-resolved chlorophyll a fluorescence (Appenroth et al. Environ. Pollut. [2001] 115, 49 - 64). Photosynthesis is clearly an important target of chromate toxicity. Electron microscopic analysis showed damage to several membrane systems, such as that of thylakoids, chloroplast envelope, plasmalemma and, at higher concentrations, that of tonoplast and mitochondria. Thus, the membrane system is another target of chromate toxicity.

References

  • 1 Appenroth K.-J., Bischoff M., Gabrys H., Stoeckel J., Swartz H. M., Walczak T., Winnefeld K.. Kinetics of chromium (V) formation and reduction in fronds of the duckweed Spirodela polyrhiza - a low frequency EPR study.  J. Inorg. Biochem.. (2000);  78 235-242
  • 2 Appenroth K.-J., Stöckel J., Srivastava A., Strasser R. J.. Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements.  Environ. Pollut.. (2001);  115 49-64
  • 3 Appenroth K.-J., Teller S., Horn M.. Photophysiology of turion formation and germination in Spirodela polyrhiza. .  Biol. Plant.. (1996);  38 95-106
  • 4 Baccouch S., Chaoui A., El Ferjani E.. Nickel toxicity: Effects on growth and metabolism of maize.  J. Plant Nutr.. (1998);  21 577-588
  • 5 Barcelo J., Poschenrieder Ch., Gunse B.. Effect of Cr(VI) on mineral element composition of bush beans.  J. Plant Nutr.. (1985);  8 211-217
  • 6 Bassi M., Corradi M. G., Realini M.. Effects of chromium (VI) on two freshwater plants, Lemna minor and Pistia stratiotes. 1. Morphological observations.  Cytobios. (1990 a);  62 27-38
  • 7 Bassi M., Corradi M. G., Ricci A.. Effects of chromium (VI) on two freshwater plants, Lemna minor and Pistia stratiotes. 2. Biochemical and physiological observations.  Cytobios. (1990 b);  62 101-109
  • 8 Baszynski T., Krol M., Wolinska D.. Photosynthetic apparatus of Lemna minor L. as affected by chromate treatment. Akoyunoglou, G., ed. Photosynthesis II. Electron Transport and Photophosphorylation. Philadelphia, PA; Balaban International Science Services (1981)
  • 9 Cherest H., Davidian J. C., Thomas D., Benes V., Ansorge W., SurdinKerjan Y.. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. .  Genetics. (1997);  145 627-635
  • 10 Cervantes C., Campos-Garcia J., Devars S., Gutierrez-Corona F., Loza-Tavera H., Torres-Guzman J. C., Moreno-Sanchez R.. Interactions of chromium with microorganisms and plants.  FEMS Microbiol. Rev.. (2001);  25 335-347
  • 11 Cowgill U. M., Milazzo D. P., Landengberger B. D.. The sensitivity of Lemna gibba G-3 and 4 clones of Lemna minor to 8 common chemicals using a 7-day test.  Res. J. Water Pollut. C.. (1991);  63 991-998
  • 12 De Fillippis L. F., Pallaghy C. K.. Heavy metals: sources and biological effects. Rai, L. C., Gauer, J. P., and Soeder, C. J., eds. Advances in Limnology Seris: Algae and Water Pollution. Stuttgart; E. Schweizerbartsche Press (1994): 31-77
  • 13 Dixit V., Pandey W., Shyam R.. Chromium ions inactivate electron transport and enhance superoxide generation in vivo in pea (Pisum sativum L. cv. Azad) root mitochondria.  Plant Cell Enviorn.. (2002);  25 687-693
  • 14 Färber E., Kandeler R.. Significance of calcium-ions in the overcrowding effect in Spirodela polyrhiza P143.  J. Plant Physiol.. (1989);  135 94-98
  • 15 Fernandes M. A. S., Santos M. S., Alpoin M. C., Madeira V. M. C., Vicente J. A. F.. Chromium (VI) interaction with plant and animal mitochondrial bioenergetics. A comparative study.  J. Biochem. Molec. Toxicol.. (2002);  16 53-63
  • 16 Fomin A., Moser H., Pickl C., Arndt U.. Ökotoxikologische Untersuchungen saurer Tagebauwässer der Bergbaufolgelandschaft Lausitz während ihrer Sanierung. Arndt, U., Böcker, R., und Kohler, A., eds. Abbau von Bodenschätzen und Wiederherstellung der Landschaft. Ostfildern; Verlag G. Heimbach (1997)
  • 17 Fomin A., Moser H., Pickl C.. Ecotoxicological investigations of extremely acid mining lakes using bioassays suitable for testing at low pH.  Toxicol. Environm. Chem.. (2000);  76 237-254
  • 18 Giardi M. T., Mazojidek J., Godde D.. Effects of abiotic stress on the turnover of the D1 reaction center II protein.  Physiol. Plant.. (1997);  101 635-642
  • 19 Huillier L., d'Auzac J., Durand M., MichaudFerriere N.. Nickel effects on two maize (Zea mays) cultivars: Growth, structure, Ni concentration, and localization.  Can. J. Bot.. (1996);  74 1547-1554
  • 20 ISO/CD 20079 Water quality - Determination of the toxic effect of water constituents and waste water to duckweed (Lemna minor) - Duckweed growth inhibition test, ISO TC 147/SC 5/WG 5. 2001
  • 21 Laemmli U. K.. Cleavage of structural proteins during assembly of the head of bacteriophage T4.  Nature. (1970);  227 680-685
  • 22 Liu K. J., Jiang J., Shi X., Gabrys H., Walczak T., Swartz H. M.. Low-frequency EPR study of chromium(V) formation from chromium(VI) in living plants.  Biochem. Biophys. Res. Commun.. (1995);  206 829-834
  • 23 Liu K. J., Shi X. L.. In vivo reduction of chromium(VI) and its related free radical generation.  Mol. Cell. Biochem.. (2001);  222 41-47
  • 24 Magel E.. Qualitative and quantitative determination of starch by a colorimetric method.  Starch/Staerke. (1991);  43 384-387
  • 25 Millar A. A., Wrischer M., Kunst L.. Accumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology.  The Plant Cell. (1998);  11 1889-1902
  • 26 Porra R. J., Thompson W. A., Kriedemann P. E.. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.  Biochim. Biophys. Acta. (1989);  975 384-394
  • 27 Samantaray S., Rout G. R., Das P.. Role of chromium on plant growth and metabolism.  Acta Physiol. Plant. (1998);  20 201-212
  • 28 Sárvári E., Nyitrai P.. Separation of chlorophyll-protein complexes by Deriphat polyacrylamide gradient gel electrophoresis.  Electrophoresis. (1994);  15 384-394
  • 29 Spurr A. R.. A low-viscosity epoxy resin embedding medium for electron microscopy.  J. Ultrastruct. Res.. (1969);  26 31-43
  • 30 Staves R. P., Knaus R. M.. Chromium removal from water by three species of duckweeds.  Aquat. Bot.. (1985);  23 261-273
  • 31 Stoyanova D.. Ultrastructural responses of leaf mesophyll and trap wall cell of Utricularia vulgaris. .  Biol. Plant.. (1999);  42 395-400
  • 32 Sudhakar G., Jyothi B., Venkateswarlu V.. Metal pollution and its impact on algae in flowing waters in India.  Arch. Environ. Contam. Toxicol.. (1991);  21 556-566
  • 33 Susplugas S., Srivastava A., Strasser R. J.. Changes in the photosynthetic activities during several stages of vegetative growth of Spirodela polyrhiza: Effect of chromate.  J. Plant Physiol.. (2000);  157 503-512
  • 34 Vajpayee P., Tripathi R. D., Rai U. N., Ali M. B., Singh S. N.. Chromium accumulation reduced chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L.  Chemosphere. (2000);  41 1075-1082
  • 35 Vajpayee P., Rai U. N., Ali M. B., Tripathi R. D., Yadav V., Sinha S., Singh S. N.. Chromium-induced physiologic changes in Vallisneria spiralis L. and its role in phytoremediation of tannery effluent.  Bull. Environ. Contam. Toxicol.. (2001);  67 246-256
  • 36 Wang Q., Cui Y., Dong Y.. Phytoremediation of polluted waters. Potentials and prospects of wetland plants.  Acta Biotechnol.. (2002);  22 199-208
  • 37 Xyländer M., Augsten H., Appenroth K.-J.. Influence of nickel on the life cycle of the duckweed Spirodela polyrhiza (L.) Schleiden.  J. Plant Physiol.. (1993);  142 208-213

K. J. Appenroth

Universität Jena
Pflanzenphysiologie

Dornburger Straße 159

07743 Jena

Germany

Email: klaus.appenroth@uni-jena.de

Section Editor: M. Riederer