Typha latifolia resilience to high metal stress: antioxidant response in plants from mine and flotation tailing ponds


  • Isidor Grdović Department of Plant Ecology and Phytogeography, University of Belgrade, Faculty of Biology, Studentski trg 16, Belgrade, Serbia
  • Milijana Kovačević Department of Plant Ecology and Phytogeography, University of Belgrade, Faculty of Biology, Studentski trg 16, Belgrade, Serbia https://orcid.org/0000-0001-6088-9866
  • Gordana Andrejić Department of Radioecology and Agrochemistry, University of Belgrade, Institute for the Application of Nuclear Energy, Banatska 31b, Belgrade, Serbia https://orcid.org/0000-0002-5515-9321
  • Željko Dželetović Department of Radioecology and Agrochemistry, University of Belgrade, Institute for the Application of Nuclear Energy, Banatska 31b, Belgrade, Serbia https://orcid.org/0000-0001-9166-7094
  • Tamara Rakić Department of Plant Ecology and Phytogeography, University of Belgrade, Faculty of Biology, Studentski trg 16, Belgrade, Serbia https://orcid.org/0000-0001-6959-3439




cattail, metal antagonism, metal tolerance, oxidative stress, phytoremediation


Paper description:

  • Typha latifolia (cattail) inhabits artificial ponds of flotation and mine tailings that are a serious source of environmental pollution by metals.
  • We assessed plant tolerance to specific edaphic conditions, the chemical properties of the substrate, metal concentrations in the plant, and antioxidant enzyme activities.
  • Cattail accumulates metals predominantly in roots. The effects of elevated metal concentrations on the antioxidant enzyme activities depend on the type of enzyme, metal concentrations, and their molar ratios in the plant.
  • Cattail could be a useful component of a biological water treatment system for removing metals from heavily contaminated wastewater, sediments, and technosols.

Abstract: Typha latifolia (cattail) forms natural stands in the transition zone of artificial flotation and mine tailings ponds and is contaminated with extremely high concentrations of metals. We assessed the absorption capacity of the plant, metal transfer to leaves, and the effects of elevated metal concentrations on antioxidant enzyme activities. Soil acidity, the pseudo-total and available metal content of the substrate, and metal concentrations in plants were examined. The effects of elevated metal concentrations in plants on antioxidant enzyme activities (superoxide dismutase, catalase, ascorbate peroxidase, guaiacol peroxidase, glutathione reductase) were assessed. Cattails exhibited high metal accumulation levels in roots and a low transfer rate to the leaves. The effects of metal concentrations on antioxidant enzyme activities were found to depend on the type of enzyme, metal concentrations in the plant and their molar ratios, as well as on the pH of the substrate. High activities of antioxidant enzymes indicate increased generation of reactive oxygen species (ROS) and show that metal detoxification mechanisms are insufficient to restrain their toxicity. Pronounced resistance to elevated metal concentrations and high efficiency in metal phytostabilization show that cattail could be a valuable component of biological treatment systems for removing metals from multi-metal and heavily contaminated substrates in the pH range from ultra-acidic to neutral.


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Malar S, Shivendra Vikram S, Jc Favas P, Perumal V. Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud. 2016;55(1):54. https://doi.org/10.1186/s40529-014-0054-6

Sharma SS, Dietz K-J. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009;14(1):43-50. https://doi.org/10.1016/j.tplants.2008.10.007

Cuypers A, Smeets K, Ruytinx J, Opdenakker K, Keunen E, Remans T, Horemans N, Vanhoudt N, Van Sanden S, Van Belleghem F, Guisez Y, Colpaert J, Vangronsveld J. The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol. 2011;168(4):309-16. https://doi.org/10.1016/j.jplph.2010.07.010

Song U, Waldman B, Park JS, Lee K, Park S-J, Lee EJ. Improving the remediation capacity of a landfill leachate channel by selecting suitable macrophytes. J Hydro-Environ Res. 2018;20:31-7. https://doi.org/10.1016/j.jher.2018.04.005

Prica M, Andrejić G, Šinžar-Sekulić J, Rakić T, Dželetović Ž. Bioaccumulation of heavy metals in common reed (Phragmites australis) growing spontaneously on highly contaminated mine tailing ponds in Serbia. Botanica serbica. 2019;43(1):85-95. https://doi.org/10.2298/BOTSERB1901085P

Kovačević M, Jovanović Ž, Andrejić G, Dželetović Ž, Rakić T. Effects of high metal concentrations on antioxidative system in Phragmites australis grown in mine and flotation tailings ponds. Plant Soil. 2020;453:297-312. https://doi.org/10.1007/s11104-020-04598-x

US EPA Method 3051A (SW-846): Microwave-assisted acid digestion of sediments, sludges, and oils, revision 1. Washington, DC: US EPA; 2007.

Pansu M, Gautheyroy J. Handbook of Soil Analysis. Mineralogical, Organic and Inorganic Methods. Berlin, Heidelberg: Springer; 2006. 993 p. https://doi.org/10.1007/978-3-540-31211-6

Jones Jr JB, Case VW. Sampling, handling and analyzing plant tissue samples. In: Westerman RL, editor. Soil testing and plant analysis. 3rd edn. Madison,WI: Soil Science Society of America, Inc; 1990. p. 389-447. https://doi.org/10.2136/sssabookser3.3ed.c15

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54. https://doi.org/10.1016/0003-2697(76)90527-3

Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971; 44(1):276-87. https://doi.org/10.1016/0003-2697(71)90370-8

Aebi HBT. [13] Catalase in vitro. In: Packer L, editor. Oxygen Radicals in Biological Systems. Academic Press; 1984. p. 121–6. (Methods in Enzymology; Vol. 105). https://doi.org/10.1016/S0076-6879(84)05016-3

Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981;22(5):867-80. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Polle A, Otter T, Seifert F. Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol. 1994;106:53-60. https://doi.org/10.1104/pp.106.1.53

Foyer C, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta. 1976;133:21-5. https://doi.org/10.1007/BF00386001

Soil Survey Division Staff. Soil Survey Manual. USDA Handbook No. 18. Washington DC, US: Government Printing Office; 2018. 603 p.

Stanković S, Moric I, Pavic A, Vasiljevic B. Investigation of the microbial diversity of an extremely acidic, metal-rich water body (Lake Robule, Bor, Serbia). J Serb Chem Soc. 2014;79 (6):729-41. https://doi.org/10.2298/JSC130605071S

Kabata-Pendias A. Trace Elements in Soils and Plants. London: CRC Press; 2011. 505 p. https://doi.org/10.1201/b10158

Bañuelos G, Aiwa H. Trace elements in soils and plants: An overview. J Environ Sci Health Part A. 1999; 34(4):951-74. https://doi.org/10.1080/10934529909376875

Marschner P. Marschner's Mineral Nutrition of Higher Plants. San Diego, USA: Academic Press, Elsevier; 2012. 651 p. https://doi.org/10.1016/C2009-0-63043-9

Manios T, Stentiford EI, Millner P. Removal of heavy metals from a metaliferous water solution by Typha latifolia plants and sewage sludge compost. Chemosphere. 2003;53:487-94. https://doi.org/10.1016/S0045-6535(03)00537-X

Sasmaz A, Obek E, Hasar H. The accumulation of heavy metals in Typha latifolia L. grown in a stream carrying secondary effluent. Ecol Eng. 2008;33:278-84. https://doi.org/10.1016/j.ecoleng.2008.05.006

Putri MP, Moersidik SS. Effectiveness of Typha latifolia for phytoremediation of cadmium in acid mine drainage. J Phys Conf Ser. 2021;1811:012025. https://doi.org/10.1088/1742-6596/1811/1/012025

Atlas of Eh-pH diagrams: Intercomparison of thermodynamic databases: Geological Survey of Japan, Open File Report No. 419. Naoto, Takeno: National Institute of Advanced Industrial Science and Technology; 2005. 285 p.

Wei B, Yu J, Cao Z, Meng M, Yang L, Chen Q. The Availability and Accumulation of Heavy Metals in Greenhouse Soils Associated with Intensive Fertilizer Application. Int J Environ Res Public Health. 2020;17:5359. https://doi.org/10.3390/ijerph17155359

Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, Raskin I. Phytoremediation: A Novel Strategy for the Removal of Toxic Metals from the Environment Using Plants. Nat Biotechnol. 1995;13:468-74. https://doi.org/10.1038/nbt0595-468

Ye ZH, Baker AJM, Wong MH, Willis AJ. Zinc, lead and cadmium tolerance, uptake and accumulation by Typha latifolia. New Phytol. 1997;136(3):469-80. https://doi.org/10.1046/j.1469-8137.1997.00759.x

Min Y, boqing T, Meizhen T, Aoyama I. Accumulation and uptake of manganese in a hyperaccumulator Phytolacca americana. Miner Eng. 2007;20:188-90. https://doi.org/10.1016/j.mineng.2006.06.003

Shanahan JO, Brummer JE, Leininger WC, Paschke MW. Manganese and Zinc Toxicity Thresholds for Mountain and Geyer Willow. Int J Phytoremediation. 2007;9:437-52. https://doi.org/10.1080/15226510701606323

Mizuno T, Emori K, Ito S-i. Manganese hyperaccumulation from non-contaminated soil in Chengiopanax sciadophylloides Franch. et Sav. and its correlation with calcium accumulation. Soil Sci Plant Nutr. 2013;59:591-602. https://doi.org/10.1080/00380768.2013.807213

Millaleo R, Reyes- Diaz M, Ivanov AG, Mora ML, Alberdi M. Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Plant Nutr Soil Sci. 2010;10:470-81. http://dx.doi.org/10.4067/S0718-95162010000200008

El-Amier Y, Elhindi K, El-Hendawy S, Al-Rashed S, Abd-ElGawad A. Antioxidant System and Biomolecules Alteration in Pisum sativum under Heavy Metal Stress and Possible Alleviation by 5-Aminolevulinic Acid. Molecules. 2019;24:4194. https://doi.org/10.3390/molecules24224194

Li H, Luo H, Li D, Hu T, Fu J. Antioxidant Enzyme Activity and Gene Expression in Response to Lead Stress in Perennial Ryegrass. J Amer Soc Hort Sci. 2012;137:80-5. https://doi.org/10.21273/JASHS.137.2.80

Shi Q-h, Zhu Z-j, Li J, Qian Q-q. Combined Effects of Excess Mn and Low pH on Oxidative Stress and Antioxidant Enzymes in Cucumber Roots. Agric Sci China. 2006;5:767-72. https://doi.org/10.1016/S1671-2927(06)60122-3

Zhang K-x, Wen T, Dong J, Ma F-w, Bai T-h, Wang K, Li C-y. Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. J Integr Agric. 2016;15:1499-509. https://doi.org/10.1016/S2095-3119(15)61325-9

Zhang YK, Zhu DF, Zhang YP, Chen HZ, Xiang J, Lin XQ. Low pH-induced changes of antioxidant enzyme and ATPase activities in the roots of rice (Oryza sativa L.) seedlings. PLoS One. 2015;10(2):e0116971. https://doi.org/10.1371/journal.pone.0116971

Verma S, Dubey RS. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 2003;164:645-55. https://doi.org/10.1016/S0168-9452(03)00022-0

Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK. Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere. 2006;65:1027-39. https://doi.org/10.1016/j.chemosphere.2006.03.033

Usman K, Abu-Dieyeh MH, Zouari N, Al-Ghouti MA. Lead (Pb) bioaccumulation and antioxidative responses in Tetraena qataranse. Sci Rep. 2020;10:17070. https://doi.org/10.1038/s41598-020-73621-z




How to Cite

Grdović I, Kovačević M, Andrejić G, Dželetović Željko, Rakić T. Typha latifolia resilience to high metal stress: antioxidant response in plants from mine and flotation tailing ponds. Arch Biol Sci [Internet]. 2023Oct.26 [cited 2024Feb.29];75(3):341-50. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/8850




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