Assessment of the adaptive and phytoremediation potential of Miscanthus×giganteus grown in flotation tailings

Gordana Andrejić, Jasmina Šinžar-Sekulić, Milijana Prica, Gordana Gajić, Željko Dželetović, Tamara Rakić

Abstract


Paper description:

  • Mining activities produce enormous amounts of metal contaminated flotation tailings which are devoid of vegetation cover, prone to erosion by wind and water and cause metal pollution and degradation of neighboring ecosystems.
  • Miscanthus × giganteus plants were grown four months in flotation tailings with the aim of assessing its phytoremediation potential.
  • All plants successfully grew, accumulated and retained the major portion of metals within roots, exhibited reduced plant growth and photosynthetic rate, whilst biochemical parameters were not affected.
  • Miscanthus × giganteus is a metal excluder plant species that can be cultivated as a stabilizer of flotation tailings.


Abstract: Mining activities produce enormous amounts of metal-contaminated waste that is the source of ecosystem pollution by metals. Owing to complex adverse environmental conditions, the surface of abandoned flotation tailings is completely devoid of vegetation cover and is therefore very susceptible to fluvial erosion, wind dispersal to neighboring ecosystems and leaching of heavy metals into ground waters. The aim of this study was to estimate the adaptive potential of Miscanthus×giganteus (Poaceae) to grow on flotation tailings without any input. In this field experiment, plants were grown for four months in flotation tailings and in unpolluted control chernozem soil. Plants accumulated and retained the major part of metals within their roots, exhibiting their very low transfer to aerial parts, which all define M.×giganteus as a phytoexcluder plant species. Plants grown in flotation tailings showed significant reduction in the net CO2 assimilation rate and growth parameters, and there was no negative impact on pigment content, maximum quantum yield of PSII photochemistry, lipid peroxidation level and total antioxidative capacity in leaves. The obtained results indicate that despite reduced growth, M.×giganteus can be cultivated for phytoremediation of flotation tailings.

https://doi.org/10.2298/ABS190709051A

Received: July 9, 2019; Revised: August 14, 2019; Accepted: August 15, 2019; Published online: August 30, 2019

How to cite this article: Andrejić G, Šinžar-Sekulić J, Prica M, Gajić G, Dželetović Ž, Rakić T. Assessment of the adaptive and phytoremediation potential of Miscanthus×giganteus grown in flotation tailings. Arch Biol Sci. 2019;71(4):687-96.


Keywords


Miscanthus×giganteus; chlorophyll a fluorescence; lipid peroxidation; heavy metals; photosynthesis

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References


Barbosa B, Fernando AL. Aided Phytostabilization of mine waste. In: Prasad MNV, de Campos Favas PJ, Maiti SK, editors. Bio-Geotechnologies for Mine Site Rehabilitation. Atlanta: Elsevier Inc; 2018. p. 147-57.

Ciarkowska K, Hanus-Fajerska E, Gambuś F, Muszyńska E, Czech T. Phytostabilization of Zn-Pb ore flotation tailings with Dianthus carthusianorum and Biscutella laevigata after amending with mineral fertilizers or sewage sludge. J Environ Manage. 2017;189:75-83.

Dickinson NM, Baker AJM, Doronila A, Laidlaw S, Reeves RD. Phytoremediation of inorganics: Realism and Synergies. Int J Phytoremediation. 2009;11(2):97-114.

Berti WR, Cunningham SD. Phytostabilization of metals. In: Raskin I, Ensley BD, editors. Phytoremediation of toxic metals: using plants to clean up the environment. New York: Wiley; 2000. p. 71-88.

Smith RAH, Bradshaw AD. The use of metal tolerant plant populations for the reclamation of metalliferous wastes. J Appl Ecol. 1979;595- 612.

Küpper H, Šetlík I, Spiller M, Küpper FC, Prášil O. Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol. 2002;38(3):429-41.

Hossain MA, Piyatida P, da Silva JAT, Fujita M. 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. J Bot. 2012;2012:872875.

Singh S, Parihar P, Singh R, Singh VP, Prasad SM. Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics. Front Plant Sci. 2015;6:1143.

Sharma P, Dubey RS. Lead Toxicity in Plants. Braz. J Plant Physiol. 2015;17:1-19.

Küpper H, Andresen E. Mechanisms of metal toxicity in plants. Metallomics. 2016;8:269-85.

Sharma SS, Dietz KJ. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 2009;14(1):43-50.

Hodkinson TR, Chase MW, Lledó DM, Salamin N, Renvoize SA. Phylogenetics of Miscanthus, Saccharum and related genera (Saccharinae, Andropogoneae, Poaceae) based on DNA sequences from ITS nuclear ribosomal DNA and plastid trnL intron and trnL-F intergenic spacers. J Plant Res. 2002;115(5):381-92.

Naidu SL, Moose SP, Al-Shoaibi AK, Raines CA, Long SP. Cold tolerance of C4 photosynthesis in Miscanthus × giganteus: Adaptation in amounts and sequence of C4 photosynthetic enzymes. Plant Physiol. 2003;132(3):1688-97.

Purdy SJ, Maddison AL, Jones LE, Webster RJ, Andralojc J, Donnison I, Clifton-Brown J. Characterization of chilling-shock responses in four genotypes of Miscanthus reveals the superior tolerance of M. × giganteus compared with M. sinensis and M. sacchariflorus. Ann Bot. 2013;111(5):999-1013.

Nsanganwimana F, Pourrut B, Waterlot C, Louvel B, Bidar G, Labidi S, Fontaine J, Muchembled J, Lounès-Hadj Sahraoui A, Fourrier H, Douay F. Metal accumulation and shoot yield of Miscanthus × giganteus growing in contaminated agricultural soils: Insights into agronomic practices. Agric Ecosyst Environ. 2015;213:61-71.

Pidlisnyuk V, Stefanovska T, Lewis EE, Erickson LE, Dais LC. Miscanthus as a Productive Biofuel Crop for Phytoremediation. Crit Rev Plant Sci. 2014;33(1):1-19.

Ježovski S, Buckby S, Cerazy-Waliszewska J, Owczarzak W, Mocek A, Kaczmarek Z, McCalmont JP. Establishment, Growth, and Yield Potential of the Perennial Grass Miscanthus × Giganteus on Degraded Coal Mine Soils. Front Plant Sci. 2018;8:726.

Brosse N, Dufour A, Meng X, Sun Q, Ragauskas A. Miscanthus: a fast- growing crop for biofuels and chemicals production. Biofuel Bioprod Biorefin. 2012;6(5):580-98.

McCalmont JP, Hastings A, McNamara NP, Ricther GM, Robson P, Donnison IS, Clifton-Brown J. Environmental costs and benefits of growing Miscanthus for bioenergy in the UK. Glob Change Biol Bioenergy. 2017;9(3):489-507.

Pogrzeba M, Rusinowski S, Krzyżak J. Macroelements and heavy metals content in energy crops cultivated on contaminated soil under different fertilization- case studies on autumn harvest. Environ Sci Pollut Res Int. 2018;25(12):12096-106.

Bang J, Kamala-Kannan S, Lee KJ, Cho M, Kim CH, Kim YJ, Bae JH, Kim KH, Myung H, Oh BT. Phytoremediation of Heavy Metals in Contaminated Water and Soil Using Miscanthus sp. Goedae-Uksae 1. Int J Phytoremediation. 2015;17(6):515-20.

Figala J, Vranová V, Rejšek K, Formánek P. Giant Miscanthus (Miscanthus × giganteus Greef et Deu.) ‒ a promising plant for soil remediation: a mini review. Acta Univ Agric Fac Agron. 2015;63(6):2241-6.

Pandey V, Bajpai O, Singh N. Energy crops in sustainable phytoremediation. Renew Sust Energ Rev. 2016;54:58-73.

Pavel PB, Puschenreiter M, Wenzel WW, Diacu E, Barbu CH. Aided phytostabilization using Miscanthus sinensis × giganteus on heavy metal-contaminated soils. Sci Total Environ. 2014;479:125-31.

Pelfrêne A, Kleckerová A, Pourrut B, Nsanganwimana F, Douay F, Waterlot C. Effect of Miscanthus cultivation on metal fractionation and human bioaccessibility in metal-contaminated soils: comparison between greenhouse and field experiments. Environ Sci Pollut Res Int. 2015;22(4):3043-54.

Técher D, Laval-Gilly P, Bennasroune A, Henry S, Martinez-Chois C, D’Innocenzo M, Falla J. An appraisal of Miscanthus x giganteus cultivation for fly ash revegetation and soil restoration. Ind Crops Prod. 2012;36(1):427-33.

Wanat N, Austruy A, Joussein E, Soubrand M, Hitmi A, Gauthier-Moussard C, Lenain J-F, Vernay P, Munch JC, Pichon N. Potential of Miscanthus x giganteus grown on highly contaminated technosols. J Geochem Explor. 2013;126:78-84.

Al-Lami MK, Oustriere N, Gonzales E, Brken JG. Amendment-assisted revegetation of mine tailings: improvement of tailings quality and biomass production. Int J Phytoremediation. 2019;21(5):425-34.

FAO (Food and Agriculture Organization of the United Nations. Land and Water Development Division). Guidelines: land evaluation for rainfed agriculture / Soil Resources Management and Conservation Services, Land and Water Development Division. Soils Bulletin. 1983;52:237.

Republički hidrometeorološki zavod. Meteorološki godišnjak-klimatološki podaci 2016. Beograd: Republički hidrometeorološki zavod; 2017. 192 p.

Bel’chicova NP. Determination of the humus of soils by I.V. Tyurin’s method. In: Tyurin IV, editor. Agrochemical methods in study of soils. 4th ed. Moscow: Nauka; 1965. p. 75-102.

Jackson ML. Soil Chemical Analysis. Englewood Cliffs: Prentice-Hall; 1958.

USEPA (United States Environmental Protection Agency). Microwave assisted acid digestion of sediments, sludges and oils. In: Test Methods for Evaluating Solid Waste, SW-846 Method 3051. Washington, DC (USA): Environmental Protection Agency; 1998. p. 1997.

Bremner JM. Nitrogen - Total. In: Sparks DL, editor. Methods of Soil Analysis Part 3: Chemical Methods. Wisconsin, Madison: American Society of Agronomy; 1996. p. 1085-22.

Pansu M, Gautheyroy J. Handbook of Soil analysis: mineralogical, organic and inorganic methods. Berlin: Springer; 2007.

Egner H, Riehm H, Domingo WR. Untersuchungen über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nahrstoffzustandes der Boden, II: Chemische Extractionsmetoden zu Phosphorund Kaliumbestimmung. Kungliga Lantbrukshügskolans Annaler. 1960;26:199-215.

Baker AJ. Accumulators and excluders‐strategies in the response of plants to heavy metals. J Plant Nutr. 1981;3(1-4):643-54.

Hiscox JD, Israelstam GF. A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot. 1979;57(12):1332-4.

Arnon DI. Copper enzymes in isolated chloroplasts: polyphenoloxidases in Beta vulgaris. Plant Physiol. 1949;24(1):1.

Wellburn AR. The spectral determination of chlorophylls a and b, as well as total carotenoids using various solvents with spectrophotometers of different resolution. J Plant Physiol. 1994;144(3):307-13.

Heath RL, Packer L. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968;125(1):189-98.

Brand-Williams W, Cuvelier ME, Berset C. Use of a free radical method to evaluate antioxidant activity. LWT - Food Sci Technol. 1995;28(1):25-30.

Kabata-Pendias A. Trace Elements in Soils and Plants. 4th ed. Boca Raton (FL): Taylor and Francis; 2011.

Korzeniowska J, Stanislawska‒Glubiak E. Phytoremediation potential of Miscanthus x giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res Int. 2015;22(15):11648-57.

Guo H, Hong C, Chen X, Xu Y, Liu Y, Jiang D, Zheng B. Different Growth and Physiological Responses to Cadmium of the Three Miscanthus Species. PLoS One. 2016;11(4): e0153475.

Pidlisnyuk V, Erickson L, Trögl J, Shapoval P, Davis L, Popelka J, Stefanovska T, Hettiarachchi G. Metals uptake behaviour in Miscanthus x giganteus plant during growth at the contaminated soil from the military site in Sliač, Slovakia. Polish J Chemic Technol. 2018;20(2):1-7.

Seregin IV, Shpigun LK, Ivanov VB. Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol. 2004;51(4):525-33.

Meyers DER, Auchterlonie GJ, Webb RI, Wood B. Uptake and localization of lead in the root system of Brassica juncea. Environ Pollut. 2008;153(2):323-32.

Kloke A, Sauerbeck DR, Vetter H. The contamination of plants and soils with heavy metals and the transport of metals in terrestrial food chains. In: Changing metal cycles and human health. Berlin: Springer; 1984. p. 113-41.

Macnicol RD, Beckett PHT. Critical concentrations of potentially toxic elements. Plant Soil. 1985;85(1):107-29.

Andrejić G, Gajić G, Prica M, Dželetović Ž, Rakić T. Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus × giganteus plants. Photosynthetica. 2018;56(4):1249-58.

Ahmad MSA, Ashraf M, Tabassam Q, Hussain M, Firdous H. Lead (Pb)-induced regulation of growth, photosynthesis, and mineral nutrition in maize (Zea mays L.) plants at early growth stages. Biol Trace Elem Res. 2011;144(1-3):1229-39.

Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E. Lead uptake, toxicity, and detoxification in plants. In: Reviews of Environmental Contamination and Toxicology. Vol. 213. New York: Springer; 2011. p. 113-6.

Yang YR, Han XZ, Liang Y, Ghosh A, Chen J, Tang M. The Combined Effects of Arbuscular Mycorrhizal Fungi (AMF) and Lead (Pb) Stress on Pb Accumulation, Plant Growth Parameters, Photosynthesis, and Antioxidant Enzymes in Robinia pseudoacacia L. PLoS One. 2015;10:e0145726.

Zhou J, Zhang Z, Zhang Y, Wei Y, Jiang Z. Effects of lead stress on the growth, physiology, and cellular structure of privet seedlings. PLoS One. 2018;13(3):e0191139.

Björkman O, Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence at 77 K among vascular plants of diverse origins. Planta. 1987;170(4):489-504.

Mittler R, Vanderauwera S, Gollery M, VanBreusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9(10):490-8.

Jiang W, Liu D. Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol. 2010;10(1):40.

Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połe´c-Pawlak K, Jarosz M, Szpunar J, Szakiel A. Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma. 2007;231(1):99-111.

Nagajyoti PC, Lee KD, Sreekanth TVM. Heavy metal, occurrence and toxicity for plants: a review. Environ Chem Lett. 2010;8(3):199-216.


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