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Alleviation of Metal-Induced Toxicity in Aquatic Plants by Exogenous Compounds: a Mini-Review

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Abstract

Metals are significant environmental pollutants, and their toxicity is a problem for all living organisms. Indeed, aquatic plants are particularly sensitive to the excess of metal ions. Several researches report that aquatic plants exposed to metal-induced toxicity showed similar responses (e.g. inhibition of growth and induction of oxidative stress). Meanwhile, many studies were involved to counter these toxicities. This paper provides a brief review of the role of the exogenous supply of some compounds in the alleviation or reduction of toxicity in aquatic plants generated by metals. Particular attention is given to the role of polyamine, proline, nitric oxide, glutathione and phytochelatin.

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References

  • Alcázar, R., Marco, F., Cuevas, J. C., Patron, M., Ferrando, A., Carrasco, P., Tiburcio, A. F., & Altabella, T. (2006). Involvement of polyamines in plant response to abiotic stress. Biotechnology Letters, 28, 1867–1876.

    Article  Google Scholar 

  • Anjum, N. A., Ahmad, I., Mohmood, I., Pacheco, M., Duarte, A. C., Pereira, E., Umar, S., Ahmad, A., Khan, N. A., Iqbal, M., & Prasad, M. N. V. (2012). Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environmental and Experimental Botany, 75, 307–324.

    CAS  Google Scholar 

  • Appenroth, K. J. (2010). Definition of “heavy metals” and their role in biological systems. Soil Heavy Metals, 19, 19–29.

    Article  CAS  Google Scholar 

  • Arasimowicz, M., & Floryszak-Wieczorek, J. (2007). Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Science, 172, 876–887.

    Article  CAS  Google Scholar 

  • Batley, G. E., Apte, S. C., & Staube, J. L. (2004). Speciation and bioavailability of trace metals in water: progress since 1982. Australian Journal of Chemistry, 57, 903–919.

    Article  CAS  Google Scholar 

  • Bertrand, M., & Poirier, I. (2005). Photosynthetic organisms and excess of metals. Photosynthetica, 43, 345–353.

    Article  CAS  Google Scholar 

  • Blaylock, M. J., & Huang, J. W. (2000). Phytoextraction of metals. In I. Raskin & B. D. Ensley (Eds.), Phytoremediation of toxic metals using plants to clean up the environment (pp. 53–70). New York: Wiley.

    Google Scholar 

  • Campbell, P. G. C. (1995). Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model. In: A.T. Tessier, D.R., (Ed.), Metal speciation and bioavailability in aquatic systems (pp. 45–102). Wiley.

  • Chen, H., Chen, J., Guo, Y., Wen, Y., Liu, J., & Liu, W. (2012). Evaluation of the role of the glutathione redox cycle in Cu (II) toxicity to green algae by a chiral perturbation approach. Aquatic Toxicology, 120–121, 19–26.

    Article  Google Scholar 

  • Cirulis, J. T., Scott, J. A., & Ross, G. M. (2013). Management of oxidative stress by microalgae. Canadian Journal of Physiology and Pharmacology, 91, 15–21.

    Article  CAS  Google Scholar 

  • Cobbett, C. S. (2000). Phytochelatin biosynthesis and function in heavy-metal detoxification. Current Opinion in Plant Biology, 3, 211–216.

    Article  CAS  Google Scholar 

  • Cornish, M. L., & Garbary, D. J. (2010). Antioxidants from macroalgae: potential applications in human health and nutrition. Algae, 25, 155–171.

    Article  CAS  Google Scholar 

  • De Filippis, L. F., & Pallaghy, C. K. (1994). Heavy metals: sources and biological effects. In L. C. Rai, J. P. Gaur, & C. J. Soeder (Eds.), Algae and water pollution (pp. 31–37). Stuttgart: E. Schweizerbart_sche Verlagsbuchhandlung.

    Google Scholar 

  • Dudka, S., & Miller, W. P. (1999). Accumulation of potentially toxic elements in plants and their transfer to human food chain. Journal of Environmental Science and Health, B34, 681–708.

    Article  CAS  Google Scholar 

  • El-Enany, A. E., & Issa, A. A. (2001). Proline alleviates heavy metal stress in Scenedesmus armatus. Folia Microbiologica, 46, 227–230.

    Article  CAS  Google Scholar 

  • EL-Naggar, A. H., & EL-Sheekh, M. M. (1998). Abolishing cadmium toxicity in Chlorella vulgaris by ascorbic acid, calcium, glucose and reduced glutathione. Environmental Pollution, 101, 169–174.

    Article  CAS  Google Scholar 

  • Falasco, E., Bona, F., Baldino, G., Hoffmann, L., & Ector, L. (2009). Diatom teratological forms and environmental alterations: a review. Hydrobiologia, 623, 1–35.

    Article  CAS  Google Scholar 

  • Fargašová, A., Bumbálová, A., & Havránek, E. (1999). Ecotoxicological effects and uptake of metals (Cu+, Cu2+, Mn2+, Mo6+, Ni2+, V5+) in freshwater alga Scenedesmus quadricauda. Chemosphere, 38, 1165–1173.

    Article  Google Scholar 

  • Fourest, E., & Volesky, B. (1997). Alginate properties and heavy metal biosorption by marine algae. Applied Biochemistry and Biotechnology, 61, 33–44.

    Google Scholar 

  • Franqueira, D., Orosa, M., Torres, E., Herrero, C., & Cid, A. (2000). Potential use of flow cytometry in toxicity studies with microalgae. The Science of the Total Environment, 247, 119–126.

    Article  CAS  Google Scholar 

  • Fritioff, Å., Kautsky, L., & Greger, M. (2005). Influence of temperature and salinity on heavy metal uptake by submersed plants. Environmental Pollution, 133, 265–274.

    Article  CAS  Google Scholar 

  • Gill, S. S., & Tuteja, N. (2010). Polyamines and abiotic stress tolerance in plants. Plant Signaling & Behavior, 5(1), 26–33.

    Article  CAS  Google Scholar 

  • Greger, M., Kaytsky, L., & Sandberg, T. (1995). A tentative model of Cd uptake in Potamogeton pectinatus in relation to salinity. Environmental and Experimental Botany, 35, 215–225.

    Article  CAS  Google Scholar 

  • Groppa, M. D., & Benavides, M. P. (2008). Polyamines and abiotic stress: recent advances. Amino Acids, 34, 35.

    Article  CAS  Google Scholar 

  • Guanzon, N. G., Jr., Nakahara, H., & Yoshida, Y. (1994). Inhibitory effects of heavy metals on growth and photosynthesis of three freshwater microalgae. Fisheries Science, 60, 379–384.

    CAS  Google Scholar 

  • Gupta, K. J., Igamberdiev, A. U., Manjunatha, G., Segu, S., Moran, J. F., Neelawarne, B., Bauwe, H., & Kaiser, W. M. (2011). The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Science, 181, 520–526.

    Article  CAS  Google Scholar 

  • Guzman-Uriostegui, A., Garcia-Jimenez, P., Marian, F., Robledo, D., & Robaina, R. R. (2002). Polyamines influence maturation in reproductive structures of Gracilaria cornea (Gracilariales, Rhodophyta). Journal of Phycology, 38, 1169–1175.

    Article  CAS  Google Scholar 

  • Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53, 1–11.

    Article  CAS  Google Scholar 

  • Halliwell, B., & Gutteridge, J. M. C. (1993). Free radicals in biology and medicine. Oxford: Clarendon.

    Google Scholar 

  • Hegedüs, A., Erdei, S., & Horvath, G. (2001). Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Science, 160, 1085–1093.

    Article  Google Scholar 

  • Hossain, M.A., Piyatida, P., da Silva, J.A.T., Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany ID 872875. doi:10.1155/2012/872875

  • Janssen, C. R., Heijerick, D. G., De Schamphelaere, K. A. C., & Allen, H. E. (2003). Environmental risk assessment of metals: tools for incorporating bioavailability. Environment International, 28, 793–800.

    Article  CAS  Google Scholar 

  • Kong, F. X., Sang, W. L., Hu, W., & Li, J. J. (1999). Physiological and biochemical response of Scenedsmus obliquus to combined effects of Al, Ca, and low pH. Bulletin of Environmental Contamination and Toxicology, 62, 179–186.

    Article  CAS  Google Scholar 

  • Kotzabasis, K., Strasser, B., Navakoudis, E., Senger, H., & Dörnemann, D. (1999). The regulatory role of polyamines in structure and functioning of the photosynthetic apparatus during photoadaptation. Journal of Photochemistry and Photobiology B: Biology, 50, 45–52.

    Article  CAS  Google Scholar 

  • Krzeslowska M. (2011). The cell Wal in plant cell response to trace metals: polysaccharide remodeling and its role in defence strategy. Acta Physiol. Plant. 33, 35–51.

  • Kováčik, J., Klejdus, B., Babula, P., & Hedbavny, J. (2015). Nitric oxide donor modulates cadmium-induced physiological and metabolic changes in the green alga Coccomyxa subellipsoidea. Algal Research, 8, 45–52.

    Article  Google Scholar 

  • Kuda, T., Tsunekawa, M., Goto, H., & Araki, Y. (2005). Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. Journal of Food Composition and Analysis, 8, 625–633.

    Article  Google Scholar 

  • Kumar, M., Kumari, P., Gupta, V., Anisha, P. A., Reddy, C. R. K., & Jha, B. (2010). Differential responses to cadmium induced oxidative stress in marine macroalga Ulva lactuca (Ulvales, Chlorophyta). Biometals, 23, 315–325.

    Article  CAS  Google Scholar 

  • Kumar, M., Bijo, A. J., Baghel, R. S., Reddy, C. R. K., & Jha, B. (2012). Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiology and Biochemistry, 5, 129–138.

    Article  Google Scholar 

  • Macfie, S. M., & Welbourn, P. M. (2000). The cell wall as a barrier to uptake of metal ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae). Archives of Environmental Contamination and Toxicology, 39, 413–419.

    Article  CAS  Google Scholar 

  • Macfie, S. M., Tarmohamed, Y., & Welbourn, P. M. (1994). Effects of cadmium, cobalt, copper and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Archives of Environmental Contamination and Toxicology, 27, 454–458.

    Article  CAS  Google Scholar 

  • Mallick, N. (2004). Copper-induced oxidative stress in the chlorophycean microalga Chlorella vulgaris: response of the antioxidant system. Journal of Plant Physiology, 161, 591–597.

    Article  CAS  Google Scholar 

  • Mandal, C., Ghosh, N., Maiti, S., Das, K., Gupta, S., Dey, N., & Adak, M. K. (2013). Antioxidative responses of Salvinia (Salvinia natans Linn.) to aluminium stress and its modulation by polyamine. Physiology and Molecular Biology of Plants, 19, 91–103.

    Article  CAS  Google Scholar 

  • Mandal, C., Ghosh, N., Dey, N., & Adak, M. K. (2014). Effects of putrescine on oxidative stress induced by hydrogen peroxide in Salvinia natans L. Journal of Plant Interactions, 2009, 550–558.

    Article  Google Scholar 

  • Marschner, H. (1995). Mineral nutrition of higher plants. Cambridge: Academic.

    Google Scholar 

  • Mathur, S., Kalaji, H. M., & Jajoo, A. (2016). Investigation of deleterious effect of Chromium phytotoxicity and photosynthesis in wheat plants. Photosynthetica, 54, 1–8.

    Article  Google Scholar 

  • Mehta, S. K., & Gaur, J. P. (1999). Heavy metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris. The New Phytologist, 143, 253–259.

    Article  CAS  Google Scholar 

  • Minocha, R., Majumdar, R., & Minocha, S. C. (2014). Polyamines and abiotic stress in plants: a complex relationship. Frontiers in Plant Science, 5, 175.

    Article  Google Scholar 

  • Misra, A. N., Vladkova, R., Singh, R., Misra, M., Dobrikova, A. G., & Apostolova, E. L. (2014). Action and target sites of nitric oxide in chloroplasts. Nitric Oxide, 39, 35–45.

    Article  CAS  Google Scholar 

  • Mithöfer, A., Schulze, B., & Boland, W. (2004). Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Letters, 566, 1–5.

    Article  Google Scholar 

  • Nagalakshmi, N., & Prasad, M. N. V. (1998). Copper-induced oxidative stress in Scenedesmus bijugatus: protective role of free radical scavengers. Bulletin of Environmental Contamination and Toxicology, 61, 623–628.

    Article  CAS  Google Scholar 

  • Nagalakshmi, N., & Prasad, M. N. V. (2001). Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Science, 160, 291–299.

    Article  CAS  Google Scholar 

  • Okamoto, O. K., Pinto, E., Latorre, L. R., Bechara, E. J., & Colepicolo, P. (2001). Antioxidant modulation in response to metal- induced oxidative stress in algal chloroplasts. Archives of Environmental Contamination and Toxicology, 40, 18–24.

    Article  CAS  Google Scholar 

  • Oukarroum, A., Bras, S., Perreault, F., & Popovic, R. (2012a). Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicology and Environmental Safety, 78, 80–85.

    Article  CAS  Google Scholar 

  • Oukarroum, A., Perreault, F., & Popovic, R. (2012b). Interactive effects of temperature and copper on photosystem II photochemistry in Chlorella vulgaris. Journal of Photochemistry and Photobiology B: Biology, 110, 9–14.

    Article  CAS  Google Scholar 

  • 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. (2000). Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f. flos-aquae strain C3-40. Journal of Applied Phycology, 12, 219–224.

    Article  CAS  Google Scholar 

  • Perales-Vela, H. V., Peña-Castro, J. N., & Cañizares-Villanueva, R. O. (2006). Heavy metal detoxification in eukaryotic microalgae. Chemosphere, 64, 1–10.

    Article  CAS  Google Scholar 

  • Pereira, M. J., Resende, P., Azeiteiro, U. M., Oliveira, J., & de Figueiredo, D. R. (2005). Differences in the effects of metals on growth of two freshwater green algae (Pseudokirchneriella subcapitata (Korshikov) Hindak and Gonium pectorale Müller). Bulletin of Environmental Contamination and Toxicology, 75, 515–522.

    Article  CAS  Google Scholar 

  • Pinto, E., Sigaud-Kutner, T. C. S., Leitaõ, M. A. S., Okamoto, O. K., Morse, D., & Colepicolo, P. (2003). Heavy metal-induced oxidative stress in algae. Journal of Phycology, 39, 1008–1018.

    Article  CAS  Google Scholar 

  • Piotrowska, A., Bajguz, A., Godlewska-Zyłkiewicz, B., & Zambrzycka, E. (2010). Changes in growth, biochemical components, and antioxidant activity in aquatic plant Wolffia arrhiza (Lemnaceae) exposed to cadmium and lead. Archives of Environmental Contamination and Toxicology, 58, 594–604.

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk, A., Bajguz, A., Zambrzycka, E., & Godlewska-Zyłkiewicz, B. (2012). Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiology and Biochemistry, 52, 52–65.

    Article  CAS  Google Scholar 

  • Piotrowska-Niczyporuk, A., Bajguz, A., Talarek, M., Bralska, M., & Zambrzycka, E. (2015). The effect of lead on the growth, content of primary metabolites, and antioxidant response of green alga Acutodesmus obliquus (Chlorophyceae). Environmental Science and Pollution Research, 22, 19112–19123.

    Article  CAS  Google Scholar 

  • Pokora, W., & Tukaj, Z. (2010). The combined effect of anthracene and cadmium on photosynthetic activity of three Desmodesmus (Chlorophyta) species. Ecotoxicology and Environmental Safety, 73, 1207–1213.

    Article  CAS  Google Scholar 

  • Pospelova, V., Chmura, G. L., Boothman, W. S., & Latimer, J. S. (2002). Dinoflagellate cyst records and human disturbance in two neighboring estuaries, New Bedford Harbor and Apponagansett Bay, Massachusetts. Science of the Total Environment, 298, 81–102.

    Article  CAS  Google Scholar 

  • Quinton, J. N., & Catt, J. A. (2007). Enrichment of heavy metals in sediment resulting from soil erosion on agricultural fields. Environmental Science & Technology, 2007(41), 3495–3500.

    Article  Google Scholar 

  • Ran, X., Liu, R., Xu, S., Bai, F., Xu, J., Yang, Y., Shi, J., & Wu, Z. (2015). Assessment of growth rate, chlorophyll a fluorescence, lipid peroxidation and antioxidant enzyme activity in Aphanizomenon flos-aquae, Pediastrum simplex and Synedra acus exposed to cadmium. Ecotoxicology, 24, 468–477.

    Article  CAS  Google Scholar 

  • Randhawa, V. K., Zhou, F., Jin, X., Nalewajko, C., & Kushner, D. J. (2001). Role of oxidative stress and thiol antioxidant enzymes in nickel toxicity and resistance in strains of the green alga Scenedesmus acutus f. altewrnans. Canadian Journal of Microbiology, 47, 987–993.

    Article  CAS  Google Scholar 

  • Sabatinim, S. E., Juárezm, Á. B., Eppism, M. R., Bianchim, L., Luquetm, C. M., & Molinam, M. C. R. (2009). Oxidative stress and antioxidant defenses in two green microalgae exposed to copper. Ecotoxicology and Environmental Safety, 72, 1200–1206.

    Article  Google Scholar 

  • Sharma, S. S., & Dietz, K. J. (2006). The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57, 711–726.

    Article  CAS  Google Scholar 

  • Singh, A., Sharma, L., & Mallick, N. (2004). Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella. Ecotoxicology and Environmental Safety, 59, 223–227.

    Article  CAS  Google Scholar 

  • Siripornadulsil, S., Traina, S., Verma, D. P. S., & Sayre, R. T. (2002). Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. The Plant Cell, 14, 2837–2847.

    Article  CAS  Google Scholar 

  • Sytar, O., Kumar, A., Latowski, D., Kuczynska, P., Strzałka, K., & Prasad, M. N. V. (2013). Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiologiae Plantarum, 35, 985–999.

    Article  CAS  Google Scholar 

  • Szivak, I., Behra, R., & Sigg, L. (2009). Metal-induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). Journal of Phycology, 45, 427–435.

    Article  CAS  Google Scholar 

  • Tessier, A., & Turner, D. R. (1995). Metal speciation and bioavailability in aquatic systems. Chichester: Wiley.

    Google Scholar 

  • Tripathi, B. N., & Gaur, J. P. (2004). Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta, 219, 397–404.

    Article  CAS  Google Scholar 

  • Tripathi, B. N., Mehta, S. K., Amar, A., & Gaur, J. P. (2006). Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere, 62, 538–544.

    Article  CAS  Google Scholar 

  • Tsuji, N., Hirayanagi, N., Okada, M., Miyasaka, H., Hirata, K., Zenk, M. H., & Miyamoto, K. (2002). Enhancement of tolerance to heavy metals and oxidative stress in Dunaliella tertiolecta by Zn-induced phytochelatin synthesis. Biochemical and Biophysical Research Communications, 293, 653–659.

    Article  CAS  Google Scholar 

  • Vatamaniuk, O. K., Mari, S., Lu, Y., & Rea, P. A. (2000). Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. The Journal of Biological Chemistry, 275, 31451–31459.

    Article  CAS  Google Scholar 

  • Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids, 35, 753–759.

    Article  CAS  Google Scholar 

  • Wink, D. A., & Mitchell, J. B. (1998). Chemical biology of nitric oxide: insights into regulatory, cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radical Biology and Medicine, 25, 434–456.

    Article  CAS  Google Scholar 

  • Worms, I., Simon, D. F., Hassler, C. S., & Wilkinson, K. J. (2006). Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake. Biochimie, 88, 1721–1731.

    Article  CAS  Google Scholar 

  • Wu, J. T., Chang, S. C., & Chen, K. S. (1995). Enhancement of intracellular proline level in cells of Anacystis nidulans (cyanobacteria) exposed to deleterious concentrations of copper. Journal of Phycology, 31, 376–379.

    Article  CAS  Google Scholar 

  • Wu, J. T., Hsieh, M. T., & Kow, L. C. (1998). Role of proline accumulation in response to toxic copper in Chlorella sp. (Chlorophyceae) cells. Journal of Phycology, 34, 113–117.

    Article  Google Scholar 

  • Zhang, L. P., Mehta, S. K., Liu, Z. P., & Yang, Z. M. (2008). Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant and Cell Physiology, 49, 234–242.

    Google Scholar 

  • Zhang, S., Liu, K., Lv, X., Wang, P. F., Wang, C., Zhang, W., & He, Z. L. (2014). Effects of nitric oxide on zinc tolerance of the submerged macrophyte Hydrilla verticillata. Aquatic Biology, 23, 61–69.

    Article  Google Scholar 

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  1. Department of Chemistry and Biochemistry, University of Quebec in Montreal, C.P. 8888, Succ, Centre-Ville, Montreal, Quebec, H3C 3P8, Canada

    Abdallah Oukarroum

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Oukarroum, A. Alleviation of Metal-Induced Toxicity in Aquatic Plants by Exogenous Compounds: a Mini-Review. Water Air Soil Pollut 227, 204 (2016). https://doi.org/10.1007/s11270-016-2907-y

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