The Morphophysiological Responses of Free-Floating Aquatic Macrophytes to a Supra-optimal Supply of Manganese
- 230 Downloads
- 1 Citations
Abstract
Among the many anthropogenic abiotic stresses, manganese (Mn) toxicity has been recognized for its impact on aquatic ecosystems as well as on the biological components of these ecosystems, including aquatic plants. The objective of this study was to determine the Mn accumulation ability of aquatic macrophytes (Azolla caroliniana, Salvinia minima and Spirodela polyrhiza) and evaluate the morphophysiological responses of the species that gather the highest amount of Mn when exposed to a supra-optimal supply of manganese. The experiments were conducted in the laboratory, and the effects of Mn were evaluated based on plant growth; the concentration of total chlorophyll, carotenoids, and anthocyanins; the enzymatic activity of catalase and peroxidase; and leaf anatomy. All of the studied species accumulated Mn in their tissues. Moreover, it was observed that this accumulation was dependent on the concentration of the metal in solution. S. polyrhiza showed higher concentrations of Mn in its tissues (17.062 mg g−1 dry weight (DW)), followed by S. minima (4.283 mg g−1 DW) and A. caroliniana (1.341 mg g−1 DW). Despite the Mn accumulation in all species, S. polyrhiza was the only one selected for further analyses because of its greater ability to accumulate Mn. The high Mn concentration found in tissues of S. polyrhiza suggests that this species has the potential to sequester and accumulate this metal. However, a sensitive response in the plants exposed to higher Mn concentrations (0.4 mM) was observed. The phytotoxicity effects of this accumulation were responsible for a decrease in the plant growth, a reduction in the pigment content (total chlorophyll, carotenoids, and anthocyanins), a low activity of catalase, and the disarrangement of the leaf aerenchyma.
Keywords
Aquatic macrophytes Exposure to manganese Toxicity effectsNotes
Acknowledgments
The study has been supported by a scholarship granted by the National Counsel of Technological and Scientific Development. We thank Professor Aristéa A. Azevedo and Professor Juraci A. Oliveira of the Federal University of Viçosa for the contribution toward the realization of this work.
References
- Alvarado, S., Guédez, M., Lué-Merú, M. P., Nelson, G., Alvaro, A., Jesús, A. C., & Gyula, Z. (2008). Arsenic removal from waters by bioremediation with the aquatic plants water hyacinth (Eichhornia crassipes) and lesser duckweed (Lemna minor). Bioresource Technology, 99, 8436–8440.CrossRefGoogle Scholar
- Anderson, M. D., Prasad, T. K., & Stewart, C. R. (1995). Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology, 109, 1247–1257.Google Scholar
- Arnon, D. I. (1949). Copper enzymes in isolated chloroplast polyphenol-oxidases in Beta vulgaris. Plant Physiology, 24, 1–15.CrossRefGoogle Scholar
- Asrar, Z., Khavari-Nejad, R. A., & Heidari, H. (2005). Excess manganese effects on pigments of Mentha spicata at flowering stage. Archives of Agronomy and Soil Science, 51, 101–107.CrossRefGoogle Scholar
- Baldisserotto, C., Ferroni, L., Anfuso, E., Pagnoni, A., Fasulo, M. P., & Pancaldi, S. (2007). Responses of Trapa natans L. floating laminae to high concentrations of manganese. Protoplasma, 231, 65–82.CrossRefGoogle Scholar
- Banks, D., Younger, P. L., Arnesen, R. T., Iversen, E. R., & Banks, S. B. (1997). Minewater chemistry: the good, the bad and the ugly. Environmental Geology, 32, 157–174.CrossRefGoogle Scholar
- Beale, S. I. (1999). Enzymes of chlorophyll biosynthesis. Photosynthesis Research, 60, 43–73.CrossRefGoogle Scholar
- Bowler, C., Van Camp, W., Van Montagu, M., & Inze, D. (1994). Superoxide dismutase in plants. Critical Reviews in Plant Sciences, 13, 199–218.Google Scholar
- Chance, B., & Machley, A. L. (1955). Assays of catalases and peroxidases. Methods in Enzymology, 2, 764–775.CrossRefGoogle Scholar
- Ciamporová, M. (2000). Diverse responses of root cell structure to aluminium stress. Plant and Soil, 226, 113–116.CrossRefGoogle Scholar
- Craker, L. E., & Wetherbee, P. J. (1973). Ethylene, light, and anthocyanin synthesis. Plant Physiology, 51, 436–438.CrossRefGoogle Scholar
- Csatorday, K., Gombos, Z., & Szalontai, B. (1984). Mn2+ and Co2+ toxicity in chlorophyll biosynthesis. Proceedings of the National Academy of Sciences, 81, 476–478.CrossRefGoogle Scholar
- El-Jaoual, T., & Cox, D. A. (1998). Manganese toxicity in plants. Journal of Plant Nutrition, 21, 353–386.CrossRefGoogle Scholar
- Fecht-Christoffers, M. M., Maier, P., & Horst, W. J. (2003). Apoplastic peroxidases and ascorbate are involved in manganese toxicity and tolerance of Vigna unguiculata. Plant Physiology, 177, 237–244.Google Scholar
- Fernando, D. R., Bakkaus, E. J., Perrier, N., Baker, A. J. M., Woodrow, I. E., Batianoff, G. N., & Collins, R. N. (2006). Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytologist, 171, 751–758.CrossRefGoogle Scholar
- Gonzáles, A., Steffen, K. L., & Lynch, J. P. (1998). Light and excess manganese. Plant Physiology, 118, 493–504.CrossRefGoogle Scholar
- Guimarães, F.P., Aguiar, R., Karam, D., Oliveira, J.A., Silva, J. A. A. Santos, C. L, Santanna-Santos, B.F. & Lizieri-Santos, C. (2011). Potential of macrophytes for removing atrazine from aqueous solution. Planta Daninha 29, 42/02-54.Google Scholar
- Guimarães, F.P., Aguiar, R., Oliveira, J.A., Silva, J. A. A. & Karam, D. (2012) Potential of macrophytes for removing arsenic from aqueous solution. Planta Daninha (in press).Google Scholar
- Guimarães-Silva, A. K., Machado, D. A., Nalini, H. A., & Lena, J. C. (2007). A qualidade das águas na região dos garimpos de topázio imperial na sub-bacia do rio da Ponte, Ouro Preto-MG. Revista Escola de Minas, Ouro Preto, 60, 603–611.Google Scholar
- Hagelstein, K. (2009). Globally sustainable manganese metal production and use. Journal of Environmental Management, 90, 3736–3740.CrossRefGoogle Scholar
- Hasan, S. H., Talat, M., & Rai, S. (2007). Sorption of cadmium and zinc from aqueous solutions by water hyacinth (Eichhornia crassipes). Bioresource Technology, 98, 918–928.CrossRefGoogle Scholar
- Hauck, M., Paul, A., Cross, S., & Raubuch, M. (2003). Manganese toxicity in epiphytic lichens: Chlorophyll degradation and interaction with iron and phosphorus. Environmental and Experimental Botany, 49, 181–191.CrossRefGoogle Scholar
- Havir, E. A., & McHale, N. A. (1987). Regulation of catalase activity in leaves of Nicotiana sylvestris by high CO2. Plant Physiology, 89, 952–957.CrossRefGoogle Scholar
- He, C. J., Morgan, P. W., & Drew, M. C. (1992). Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology, 98, 137–142.CrossRefGoogle Scholar
- He, C. J., Morgan, P. W., & Drew, M. C. (1996). Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology, 112, 463–472.Google Scholar
- Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. Bulletin 347 (p. 37). Berkeley: California Agricultural Experiment Station.Google Scholar
- Hoffmann, T., Kutter, C., & Santamaría, J. (2004). Capacity of Salvinia minima Baker to tolerate and accumulate As and Pb. Engineering in Life Sciences, 4, 61–65.CrossRefGoogle Scholar
- Hua, J., Zhang, C., Yin, Y., Chen, R. & Wang, X. (2011). Phytoremediation potential of three aquatic macrophytes in manganese-contaminated water. Water and Environment Journal. http://onlinelibrary.wiley.com/doi/ 10.1111/j.1747-6593.2011.00293.x/pdf. Accessed 10 Dec 2011.
- Hunt, R. (1978). Plant growth analysis (p. 67p). London: Edward Arnold.Google Scholar
- Johansen, D. A. (1940). Plant microtechnique (p. 423p). New York: McGraw-Hill Book.Google Scholar
- Kar, M., & Mishra, D. (1976). Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiology, 57, 315–319.CrossRefGoogle Scholar
- Karnovsky, M. J. (1965). A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. The Journal of Cell Biology, 27, 137–138.Google Scholar
- Kitao, M., Lei, T. T., Nakamura, T., & Koike, T. (2001). Manganese toxicity as indicated by visible foliar symptoms of Japanese white birch (Betula platyphylla var. japonica). Environmental Pollution, 111, 89–94.CrossRefGoogle Scholar
- Lei, Y., Chen, K., Tian, X., Korpelainen, H., & Li, C. (2007a). Effect of Mn toxicity on morphological and physiological changes in two Populus cathayana populations originating from different habitats. Trees, 21, 569–580.CrossRefGoogle Scholar
- Lei, Y., Korpelainen, H., & Li, C. (2007b). Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere, 68, 686–694.CrossRefGoogle Scholar
- Lichthenthaler, H. K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In S. P. Colowick & N. O. Kaplan (Eds.), Methods in enzymology (pp. 350–382). San Diego: Academic.Google Scholar
- Lidon, F. C., Barreiro, M. G., & Ramalho, J. C. (2004). Manganese accumulation in rice: Implications for photosynthetic functioning. Journal of Plant Physiology, 161, 1235–1244.CrossRefGoogle Scholar
- Ljung, K., & Vahter, M. (2007). Time to re-evaluate the guideline value for manganese in drinking water? Environmental Health Perspectives, 115, 1533–1538.CrossRefGoogle Scholar
- Macfie, S. M., Cossins, E. A., & Taylor, G. J. (1994). Effects of manganese excess on production of organic acids in Mn-tolerant an Mn-sensitive cultivars of Triticum aestivum L(wheat). Journal of Plant Physiology, 143, 135–144.CrossRefGoogle Scholar
- Morgan, P. W., Taylor, D. M., & He, C. J. (1976). Manipulation of IAA-oxidase activity and auxin-deficiency symptoms in intact content plants with manganese nutrition. Physiology Plant, 31, 149–156.CrossRefGoogle Scholar
- Mukaopadhyay, M. J., & Sharma, A. (1991). Manganese in cell metabolism of higher plants. Botany Review, 51, 117–149.CrossRefGoogle Scholar
- Nichols, P. B., Couch, J. D., & Al Hamdani, S. H. (2000). Selected physiological responses of Salvinia minima to different chromium concentrations. Aquatic Botany, 68, 313–319.CrossRefGoogle Scholar
- Noraho, N., & Gaur, J. P. (1996). Cadmium adsorption and intracellular uptake by two macrophytes, Azolla pinnata and Spirodela polyrhiza. Archives of Hydrobiology, 136, 135–144.Google Scholar
- O’brien, T. P., Feder, N., & McCully, M. E. (1964). Polychromatic staining of plant cell walls by toluidine blue. Protoplasma, 59, 368–373.CrossRefGoogle Scholar
- Olguín, E. J., Hernández, E., & Ramos, I. (2002). The effect of both different light conditions and the pH value on the capacity of Salvinia minima Baker for removing cadmium, lead and chromium. Acta Biotechnologica, 22, 121–131.CrossRefGoogle Scholar
- Panda, S., Mishra, A. K., & Biswal, U. C. (1986). Manganese-induced modification of membrane lipid peroxidation during aging of isolated wheat chloroplast. Phtobiochem Photobiophys, 13, 53–61.Google Scholar
- Paschke, M. W., Valdecantos, A., & Redente, E. F. (2005). Manganese toxicity thresholds for restoration grass species. Environmental Pollution, 135, 313–322.CrossRefGoogle Scholar
- Peixoto, P. H. P., Cambraia, J., Sant’ana, R., Mosquim, P. R., & Moreira, M. A. (1999). Aluminum effects on lipid peroxidation and on actives of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal, 11, 137–143.Google Scholar
- Pittman, J. K. (2005). Managing the manganese: Molecular mechanisms of manganese transport and homeostasis. New Phytologist, 167, 733–742.CrossRefGoogle Scholar
- Pollard, A. J., Stewart, H. L., & Roberson, C. B. (2009). Manganese hyperaccumulation in Phytolacca americana L. from the Southeastern United States. Northeastern Naturalist, 16, 155–162.CrossRefGoogle Scholar
- Quail, P. H. (1979). Plant cell fractionation. Annual Review of Plant Physiology, 30, 425–484.CrossRefGoogle Scholar
- Quartin, V. M. L., Antunes, M. L., Muralha, M. C., Sousa, M. M., & Nunes, M. A. (2001). Mineral imbalance due to manganese excess in Triticales. Journal Plant Nutrition, 24, 175–189.CrossRefGoogle Scholar
- Reichman, S. M. (2002). The responses of plants to metal toxicity: A review focusing on copper, manganese and zinc (pp. 14–59). Melbourne: Australian Minerals and Energy Environment Foundation.Google Scholar
- Santandrea, G., Schiff, S., & Bennici, A. (1998). Effects of manganese on Nicotiana species cultivated in vitro and characterization of regenerated Mn-tolerant tobacco plants. Plant Science, 132, 71–82.CrossRefGoogle Scholar
- Santandrea, G., Pandolfini, T., & Bennici, A. (2000). A physiological characterization on of Mn-tolerant tobacco plants selected by “in vitro” culture. Plant Science, 150, 163–177.CrossRefGoogle Scholar
- Shi, Q., Zhu, Z., Xu, M., Quian, Q., & Yu, J. (2006). Effect of excess manganese on the antioxidant system in Curcumis sativus L, under two light intensities. Environmental and Experimental Botany, 58, 197–205.CrossRefGoogle Scholar
- Sinha, S., Rai, U. N., & Chandra, P. (1994). Accumulation and toxicity of iron manganese in Spirodela polyrrhiza (L.) Schleiden. Environmental Contamination and Toxicology, 53, 610–617.CrossRefGoogle Scholar
- Sisinno, C. L. S. (2003). Disposição em aterros controlados de resíduos sólidos industriais não-inertes: avaliação dos componentes tóxicos e implicações para o ambiente e para a saúde humana. Caderno de Saúde Pública, Rio de Janeiro, 19, 369–374.CrossRefGoogle Scholar
- Sivaci, E. R., Sivaci, A., & Sokmen, M. (2004). Biosorption of cadmium by Myriophyllum spicatum L. and Myriophyllum triphyllum orchard. Chemosphere, 56, 1043–1048.CrossRefGoogle Scholar
- Tripathi, R. D., & Chandra, P. (1991). Chromium uptake by Spirodela polyrrhiza (L.) Schleiden in relation to metal chelators and pH. Environmental Contamination and Toxicology, 447, 767–769.Google Scholar
- Vissottiviseth, P., Francesconi, B., & Ridokchana, W. (2002). The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environmental Pollution, 118, 453–461.CrossRefGoogle Scholar
- Wilkinson, R. E., & Ohki, K. (1988). Influence of manganese deficiency and toxicity on isoprenoid syntheses. Plant Physiology, 87, 841–846.CrossRefGoogle Scholar
- Wilmouth, R. C., Turnbull, J. J., Welford, R. W. D., Clifton, I. J., Prescott, A. G., & Schofield, C. J. (2002). Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure, 10, 93–103.CrossRefGoogle Scholar
- Xue, S. G., Chen, Y. X., Baker, A. J. M., Reeves, R. D., Xu, X. H., & Lin, Q. (2005). Manganese uptake and accumulation by two populations of Phytolacca acinosa ROXB. (Phytolaccacear). Water, Air, and Soil Pollution, 160, 3–14.CrossRefGoogle Scholar
- Yang, S. X., Deng, H., & Li, M. S. (2008). Manganese uptake and accumulation in a woody hyperaccumulator, Schima superba. Plant Soil Environmental, 54, 441–446.Google Scholar