Abstract
Aims
Phragmites australis grows as a pioneer plant species in several mine and flotation tailings ponds distinguished by extremely high concentrations of metals. The main goals of this study were to estimate the effects of the specific concentrations and combinations of accumulated metals on the efficiency of antioxidative enzymes and plant oxidative status. This study is relevant to our understanding of the common reed exceptional capacity to endure extreme edaphic conditions.
Methods
Metal concentrations were determined in the sediment, roots and leaves. Antioxidative enzymes activities, amounts of pigments and phenolics, total antioxidative capacity (TAC), lipid peroxidation level (LP) were analysed in plant organs.
Results
Effects of accumulated metals depended on their concentrations and their stoichiometry. Antioxidative enzymes and TAC in roots were significantly reduced, resulting in consequent increase in LP. Pb concentration in leaves did not significantly change enzymes activities, whereas toxic level of Cu impeded activity of catalaze and ascorbate peroxidase.
Conclusions
The results indicate that in the conditions of high root metal contamination the mechanisms involved in their immobilization and detoxification cannot completely restrain their toxicity. Their effects on enzymes activities depend on the type of enzyme, metal concentrations, specific ratios and interactions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- Chl:
-
chlorophyll
- Chl (a + b) :
-
total chlorophyll
- Chl a/b :
-
Chl a / Chl b ratio
- Car:
-
total carotenoids
- GR:
-
glutathione reductase
- LP:
-
lipid peroxidation level
- POD:
-
total soluble peroxidases
- SOD:
-
superoxide dismutase
- TAC:
-
total antioxidative capacity
- Ph:
-
phenolics
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Ali MA, Fahad S, Haider I, Ahmed N, Ahmad S, Hussain S, Arshad M (2019) Oxidative Stress and Antioxidant Defense in Plants Exposed to Metal/Metalloid Toxicity. In: Hasanuzzaman M, Fotopoulos V, Nahar K, Fujita M (eds) Reactive Oxygen, Nitrogen and Sulfur Species in Plants: Production, Metabolism, Signaling and Defense Mechanisms. John-Wiley & Sons Ltd, pp 353–370
Andrejić G, Šinžar-Sekulić J, Prica M, Dželetović Ž, Rakić T (2019) Assessment of the adaptive and phytoremediation potential of Miscanthus×giganteus grown in flotation tailings. Arch Biol Sci 71(4):687–696. https://doi.org/10.2298/ABS190709051A
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidases in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Arora P, Bhardwaj R, Kanwar MK (2012) Effect of 24-epibrassinolide on growth, protein content and antioxidative defense system of Brassica juncea L. subjected to cobalt ion toxicity. Acta Physiol Plant 34:2007–2017. https://doi.org/10.1134/S1021443718040118
Ashraf MA, Maah MJ, Yusoff I (2011) Heavy metals accumulation in plants growing in ex tin mining catchment. Int J Environ Sci Technol 8(2):401–416. https://doi.org/10.1007/BF03326227
Bacchetta G, Cappai G, Carucci A, Tamburini E (2015) Use of Native Plants for the Remediation of Abandoned Mine Sites in Mediterranean Semiarid Environments. Bull Environ Contam Toxicol 94:326–333. https://doi.org/10.1007/s00128-015-1467-y
Baker AJ (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654. https://doi.org/10.1080/01904168109362867
Batty LC, Younger PL (2004) Growth of Phragmites australis (Cav.) Trin ex. Steudel in mine water treatment wetlands: effects of metal and nutrient uptake. Environ Pollut 132(1):85–93. https://doi.org/10.1016/j.envpol.2004.03.022
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bonanno G (2013) Comparative performance of trace element bioaccumulation and biomonitoring in the plant species Typha domingensis, Phragmites australis and Arundo donax. Ecotoxicol Environ Saf 97:124–130. https://doi.org/10.1016/j.ecoenv.2013.07.017
Bonanno G, Giudice RL (2010) Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecol Indic 10(3):639–645. https://doi.org/10.1016/j.ecolind.2009.11.002
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT - Food Sci Technol 28(1):25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Chaney RL (1989) Toxic element accumulation in soils and crops: protecting soil fertility and agricultural food-chains. In: Bar-Yosef B, Barrow NJ, Goldshmid J (eds) Inorganic Contaminants in the Vadose Zone. Ecological Studies (Analysis and Synthesis), vol 74. Springer, Berlin, pp 140–158
Chaoui A, El Feriani E (2005) Effect of cadmium and copper on antioxidant capacities, lignification and auxin degradation in leaves of pea (Pisum sativum L.) seedlings. C R Biol 328:23–31. https://doi.org/10.1016/j.crvi.2004.10.001
Cicero-Fernández D, Peña-Fernández M, Expósito-Camargo JA, Antizar-Ladislao B (2017) Long-term (two annual cycles) phytoremediation of heavy metal-contaminated estuarine sediments by Phragmites australis. New Biotechnol 38:56–64. https://doi.org/10.1016/j.nbt.2016.07.011
Cobett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832. https://doi.org/10.1104/pp.123.3.825
Colzi I, Doumett S, Del Bubba M, Fornaini J, Arnetoli M, Gabbrielli R, Gonnelli C (2011) On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. Environ Exp Bot 72(1):77–83. https://doi.org/10.1016/j.envexpbot.2010.02.006
Dahmani M, Van Oort HF, Gelie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109(2):231–238. https://doi.org/10.1016/S0269-7491(99)00262-6
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Deef HE-S (2007) Cupper treatments and their effects on growth, carbohydrates, minerals and essential oils contents of Rosmarinus officinalis L HE Deef. World J. Agricultur Sci 3(3):322–328. https://www.idosi.org/wjas/wjas3(3)/10.pdf
Dietz KJ, Baier M, Krämer M (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants: From Molecules to Ecosystems. Springer, Berlin, pp 73–97
Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S (2018) Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal Behav 13(8):e1460048. https://doi.org/10.1080/15592324.2018.1460048
Eller F, Skálová H, Caplan JS, Bhattarai GP, Burger MK, Cronin JT, Guo W-Y, Guo X, ELG H, Kettenring KM, Lambertini C, MK MC, Meyerson LA, Mozdzer TJ, Pyšek P, Sorrell BK, Whigham DF, Brix H (2017) Cosmopolitan Species As Models for Ecophysiological Responses to Global Change: The Common Reed Phragmites australis. Front Plant Sci 8:1833. https://doi.org/10.3389/fpls.2017.01833
Esmaeilzadeh M, Karbassi A, Moattar F (2016) Heavy metals in sediments and their bioaccumulation in Phragmites australis in the Anzali wetland of Iran. Chin J Ocean Limnol 34(4):810–820. https://doi.org/10.1007/s00343-016-5128-8
Esmaeilzadeh M, Karbassi A, Bastami KD (2017) Antioxidant response to metal pollution in Phragmites australis from Anzali wetland. Mar Pollut Bull 119(1):376–380. https://doi.org/10.1016/j.marpolbul.2017.03.030
Feldman AW, Hanks RW (1968) Phenolic content in the roots and leaves of tolerant and susceptible citrus cultivars attacked by Radopholus similis. Phytochemistry 7(1):5–12. https://doi.org/10.1016/S0031-9422(00)88198-4
Fernández S, Poschenrieder C, Marcenò C, Gallego JR, Jiménez-Gámez D, Bueno A, Afif E (2017) Phytoremediation capability of native plant species living on Pb-Zn and Hg-As mining wastes in the Cantabrian range, north Spain. J Geochem Explor 174:10–20. https://doi.org/10.1016/j.gexplo.2016.05.015
Foyer C, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/BF00386001
Gallego SM, Benavídes MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159. https://doi.org/10.1016/S0168-9452(96)04528-1
Gao GQ, Zeng KH, Ji Y, Li W, Wang Y (2019) Effects of lead stress on chlorophyll and photosynthetic fluorescence characteristics of Vallisneria natans. Appl Ecol Env Res 17(2):4171–4181. https://doi.org/10.15666/aeer/1702_41714181
Gichner T, Žnidar I, Száková J (2008) Evaluation of DNA damage and mutagenicity induced by lead in tobacco plants. Mutat Res Genet Toxicol Environ Mutagen 652(2):186–190. https://doi.org/10.1016/j.mrgentox.2008.02.009
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Ginocchio R, León-Lobos P, Arellano EC, Anic V, Ovalle JF, AJM B (2017) Soil physicochemical factors as environmental filters for spontaneous plant colonization of abandoned tailing dumps. Environ Sci Pollut Res Int 24(15):13484–13496. https://doi.org/10.1007/s11356-017-8894-8
González A, Steffen KL, Lynch JP (1998) Light and excess manganese implications for oxidative stress in common bean. Plant Physiol 118(2):493–504. https://doi.org/10.1104/pp.118.2.493
Gupta DK, Huang HG, Huang XE, Yang XE, BHN R, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177(1–3):437–444. https://doi.org/10.1016/j.jhazmat.2009.12.052
Ha NTH H, BTK A (2017) The removal of heavy metals by iron mine drainage sludge and Phragmites australis. IOP Conf. Ser.: Earth Environ Sci 71:012022 http://iopscience.iop.org/1755-1315/71/1/012022
Hasan MK, Cheng Y, Kanwar MK, Chu X-Y, Ahammed GJ, Qi Z-Y (2017) Responses of Plant Proteins to Heavy Metal Stress – A Review. Front Plant Sci 8:1492. https://doi.org/10.3389/fpls.2017.01492
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334. https://doi.org/10.1139/b79-163
Hossain MA, Piyatida P, da Silva JAT, 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. J Bot 2012:872875. https://doi.org/10.1155/2012/872875
Huang X, Yhao F, Yu G, Song C, Geng Z, Zhuang P (2017) Removal of Cu, Zn, Pb, and Cr from Yangtze Estuary Using the Phragmites australis Artificial Floating Wetlands. Biomed Res Int ID 6201048. https://doi.org/10.1155/2017/6201048
Iannelli MA, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Biochem 40(11):977–982. https://doi.org/10.1016/S0981-9428(02)01455-9
Israr M, Jewell A, Kumar D, Sahi SW (2011) Interactive effects on lead, copper, nickel and zinc on growth, metal uptake and antioxidative metabolism of Sesbania drummondii. J Hazard Mater 186(2–3):1520–1526. https://doi.org/10.1016/j.jhazmat.2010.12.021
Jiang W, Liu D (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol 10:40. https://doi.org/10.1186/1471-2229-10-40
Jones JB Jr, Case VW (1990) Sampling, handling and analyzing plant tissue samples. In: Westerman RL (ed) Soil testing and plant analysis. 3rd edn. Soil Sci Soc Am, Inc., Madison, pp 389–447
Jouili H, el Feriani E (2003) Changes in antioxidant and lignifying enzyme activities in sunflower roots (Helianthus annuus L.) stressed with copper excess. C R Biol 326(7):639–644. https://doi.org/10.1016/S1631-0691(03)00157-4
Kabata-Pendias A (2011) Trace Elements in Soils and Plants. CRC Press, London
Kalinović JV, Šerbula SM, Radojević AA, Milosavljević JS, Kalinović TS, Steharnik MM (2019) Assessment of As, Cd, Cu, Fe, Pb, and Zn concentrations in soil and parts of Rosa spp. sampled in extremely polluted environment. Environ Monit Assess 191(1):15. https://doi.org/10.1007/s10661-018-7134-0
Kasowska D, Gediga K, Spiak Z (2018) Heavy metal and nutrient uptake in plants colonizing post-flotation copper tailings. Environ Sci Pollut Res, 25 (1):824–835. https://doi.org/10.1007/s11356-017-0451-y
Kettenring KM, Whigham DF, ELG H, Gallagher SK, Weiner HM (2015) Biotic resistance, disturbance, and mode of colonization impact the invasion of a widespread, introduced wetland grass. Ecol Appl 25(2):466–480. https://doi.org/10.1890/14-0434.1
Kettenring KM, Mock KE, Zaman B, McKee M (2016) Life on the edge: reproductive mode and rate of invasive Phragmites australis patch expansion. Biol Invasions 18:2475-2495. https://doi.org/10.1007/s10530-016-1125-2
Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12(10):6894–6918. https://doi.org/10.3390/ijms12106894
Korzeniowska J, Stanislawska-Glubiak E (2015) Phytoremediation potential of Miscanthus × giganteus and Spartina pectinata in soil contaminated with heavy metals. Environ Sci Pollut Res Int 22(15):11648–11657. https://doi.org/10.1007/s11356-015-4439-1
Kumar A, Prasad MNV (2015) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89(9):1056–1065. https://doi.org/10.1016/j.chemosphere.2012.05.070
Küpper H, Šetlík I, Spiller M, Küpper FC, Prášil O (2002) Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol 38(3):429–441. https://doi.org/10.1046/j.1529-8817.2002.01148.x
Li H, Luo H (2012) Antioxidant enzyme activity and gene expression in response to lead stress in perennial ryegrass. J Amer Soc Hortic Sci 137(2):80–85. https://doi.org/10.21273/JASHS.137.2.80
Liu J, Wang J, Lee S, Wen R (2018) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13(9):e0203612. https://doi.org/10.1371/journal.pone.0203612
Lilić Ј, Cupać Ѕ, Lalević В, Andrić V, Gajić-Kvaščev М (2014) Pedological characteristics of open-pit Cu wastes and postflotation tailings (Bor, Serbia). J Soil Sci Plant Nut 14(1):161–175. https://doi.org/10.4067/S0718-95162014005000013
Lou Y, Zhao P, Wang D, Amombo E, Sun X, Wang H, Zhuge Y (2017) Germination, physiological responses and gene expression of tall fescue (Festuca arundinacea Schreb.) growing under Pb and Cd. PLoS ONE 12(1):e0169495. https://doi.org/10.1371/journal.pone.0169495
Malar S, Shivendra Vikram S, Jc Favas P, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55(1):54. https://doi.org/10.1186/s40529-014-0054-6
Markert B (1992) Presence and significance of naturally occurring chemical elements of the periodic system in the plant organism and consequences for future investigations on inorganic environmental chemistry in ecosystems. Vegetatio 103(1):1–30. https://doi.org/10.1007/BF00033413
Mazhoudi S, Chaoui A, Ghorbal MH, El Ferjani E (1997) Response of antioxidant enzymes to excess copper in tomato (Lycopersicon esculentum Mill.). Plant Sci 127(2):129–137. https://doi.org/10.1016/S0168-9452(97)00116-7
Meyers DER, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153(2):323–332. https://doi.org/10.1016/j.envpol.2007.08.029
Morari F, Dal Ferro N, Cocco E (2015) Municipal Wastewater Treatment with Phragmites australis L. and Typha latifolia L. for Irrigation Reuse. Boron and Heavy Metals. Water Air Soil Pollut 226:56. https://doi.org/10.1007/s11270-015-2336-3
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Packer JG, Meyerson LA, Skálová H, Pyšek P, Kueffer C (2017) Biological flora of the British isles: Phragmites australis. J Ecol 105(4):1123–1162. https://doi.org/10.1111/1365-2745.12797
Pansu M, Gautheyroy J (2006) Handbook of Soil Analysis. Mineralogical, Organic and Inorganic Methods. Springer, Berlin
Pidlisnyuk V, Erickson L, Trögl J, Shapoval P, Popelka J, Davis L, Stefanovska T, Hettiarachchi G (2018) Metals uptake behaviour in Miscanthus x giganteus plant during growth at the contaminated soil from the military site in Sliač, Slovakia. Pol J Chem Technol 20(2):1–7. https://doi.org/10.2478/pjct-2018-0016
Piotrowska A, Bajguz A, Godlewska-Żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66(3):507–513. https://doi.org/10.1016/j.envexpbot.2009.03.019
Polle A, Otter T, Seifert F (1994) Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60. https://doi.org/10.1104/pp.106.1.53
Prasad MNV, Freitas H, Fraenzle S, Wuenschmann S, Markert B (2010) Knowledge explosion in phytotechnologies for environmental solutions. Environ Pollut 158(1):18–23. https://doi.org/10.1016/j.envpol.2009.07.038
Prica M, Andrejić G, Šinžar-Sekulić J, Rakić T, Dželetović Ž (2019) Bioaccumulation of heavy metals in common reed (Phragmites australis) growing spontaneously on highly contaminated mine tailing ponds in Serbia and Kettenring KM43(1):85–95. https://doi.org/10.2298/BOTSERB1901085P
Quan WM, Han JD, Shen AL, Ping XY, Qian PL, Li CJ, Shi LY, Chen YQ (2007) Uptake and distribution of N, P and heavy metals in three dominant salt marsh macrophytes from Yangtze River estuary, China. Mar Environ Res 64(1):21–37. https://doi.org/10.1016/j.marenvres.2006.12.005
Ranđelović D, Mihailović N, Jovanović S (2019) Potential of Equisetum ramosissimum Desf. for remediation of antimony flotation tailings: a case study. Int J Phytoremediation 21(7):707–713. https://doi.org/10.1080/15226514.2018.1556590
Reeves R (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. NATO Science Series, vol 68. Springer, Dordrecht, pp 25–52
Rocha ACS, CMR A, MCP B, MTSD V (2014) Antioxidant response of Phragmites australis to Cu and Cd contamination. Ecotoxicol Environ Saf 109:152–160. https://doi.org/10.1016/j.ecoenv.2014.06.027
Rubino FM (2015) Toxicity of Glutathione-Binding Metals: A Review of Targets and Mechanisms. Toxics 3(1):20-62. https://doi.org/10.3390/toxics3010020
Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109(4):419–427. https://doi.org/10.1034/j.1399-3054.2000.100408.x
Seregin IV, Shpigun LK, Ivanov VB (2004) Distribution and toxic effects of cadmium and lead on maize roots. Russ J Plant Physiol 51(4):525–533. https://doi.org/10.1023/B:RUPP.0000035747.42399.84
Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contam Toxicol 232:1–44. https://doi.org/10.1007/978-3-319-06746-9_1
Shainberg O, Rubin B, Rabinowitch HD, Libal Y, Tel-Or E (2000) Acclimation of beans to oxidative stress by treatment with sublethal iron levels. J Plant Physiol 157(1):93–99. https://doi.org/10.1016/S0176-1617(00)80141-8
Shi QH, Zhu ZJ, Li J, Qian QQ (2006) Combined effects of excess Mn and low pH on oxidative stress and antioxidant enzymes in cucumber roots. Agric Sci China 5(10):767–772. https://doi.org/10.1016/S1671-2927(06)60122-3
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2015) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143
Sinha S, Saxena R (2006) Effect of iron on lipid peroxidation, and enzymatic and nonenzymatic antioxidants and bacoside-A content in medicinal plant Bacopa monnieri L. Chemosphere 62(8):1340–1350. https://doi.org/10.1016/j.chemosphere.2005.07.030
Smirnoff N (2018) Ascorbic acid metabolism and functions: A comparison of plants and mammals. Free Radic Biol Med 122:116–129. https://doi.org/10.1016/j.freeradbiomed.2018.03.033
Srivastava J, Kalra SJ, Naraian R (2014) Environmental perspectives of Phragmites australis (Cav.). Trin. Ex. Steudel. Appl Water Sci 4(3):193–202. https://doi.org/10.1007/s13201-013-0142-x
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Gupta DK (2006) Copper-induced stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (L.f.) Royle. Aquat Toxicol 80(4):405–415. https://doi.org/10.1016/j.aquatox.2006.10.006
Stoeppler M (2004) Arsenic. In: Merian E, Anke M, Ihnat M, Stoeppler M (eds) Elements and their compounds in the environment: Occurrence, analysis and biological relevance, 2nd edn. Wiley-VCH, Weinheim, pp 1321–1364
Stolz E, Greger M (2002) Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environ Exp Bot 47(3):271–280. https://doi.org/10.1016/S0098-8472(02)00002-3
Štolfa I, Žuna Pfeiffer T, Špoljarić D, Teklić T, Lončarić Z (2015) Heavy metal-induced oxidative stress in plants: response of the antioxidative system. In: Gupta D, Palma J, Corpas F (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Cham, pp 127–163
US EPA (2007) Method 3051A (SW-846): Microwave assisted acid digestion of sediments, sludges, and oils, revision 1. Washington, DC
van Reeuwijk LP (2002) Procedures for Soil Analysis, 6th Edition. Technical Paper / International Soil Reference and Information Centre, Wageningen, The Netherlands
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wińska-Krysiak M, Koropacka K, Gawroński S (2015) Determination of the tolerance of sunflower to lead-induced stress. J Elem 20(2):491–502. https://doi.org/10.5601/jelem.2014.19.4.721
Yamakura F, Kobayashi K, Ue H, Konno M (1995) The pH-dependent changes of the enzymic activity and spectroscopic properties of iron-substituted manganese superoxide dismutase. A study on the metal-specific activity of Mn-containing superoxide dismutase. Eur J Biochem 227(3):700–706. https://doi.org/10.1111/j.1432-1033.1995.tb20191.x
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50. https://doi.org/10.1016/j.chemosphere.2006.10.007
Zhao H, Wu L, Chai T, Zhang Y, Tan J, Ma S (2012) The effects of copper, manganese and zinc on plant growth and elemental accumulation in the manganese-hyperaccumulator Phytolacca americana. J Plant Physiol 169(13):1243–1252. https://doi.org/10.1016/j.jplph.2012.04.016
Acknowledgements
This work was supported by the Serbian Ministry of Education, Science and Technological Development (Grant No.451-03-68/2020-14/ 200178). The authors thank to Dr. Jasmina Šinžar-Sekulić for assistance in statistical analysis of data, and to the editor and the reviewers for helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Antony Van der Ent.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kovačević, M., Jovanović, Ž., Andrejić, G. et al. Effects of high metal concentrations on antioxidative system in Phragmites australis grown in mine and flotation tailings ponds. Plant Soil 453, 297–312 (2020). https://doi.org/10.1007/s11104-020-04598-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04598-x