Miscanthus × giganteus demonstrated good phytostabilization potentials in toxic element (TE) contaminated soils. However, information about its tolerance to elevated concentrations is still scarce. Therefore, an ex-situ pot experiment was launched using three cultivars (termed B, U, and A) grown in soils with a gradient Cd, Pb and Zn concentrations. Control plants were also cultivated in non-contaminated soil. Results show that the number of tillers per plant, stem diameter as well as leaf photosynthetic pigments (chlorophyll a, b and carotenoids) were negatively impacted by soil contamination. On the other hand, phenolic compounds, flavonoids, tannins, and anthocyanins levels along with the antioxidant enzymatic activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase increased in the plants grown on contaminated soils. Altogether, these data demonstrate that miscanthus is impacted by concentrations of toxic elements yet is able to tolerate high levels of soil contamination. These results may contribute to clarifying the miscanthus tolerance strategy against high contamination levels and its efficiency in phytoremediation.

Department of Environmental Chemistry and Technology Faculty of Environment Jan Evangelista Purkyně University in Ústí nad Labem Pasteurova 3632 15 400 96 Ústí nad Labem Czech Republic

Laboratoire Écologie Fonctionnelle et Environnement Avenue de l'Agrobiopôle 31326 Castanet Tolosan France

Laboratoire Génie Civil et Géo Environnement ISA Lille Junia 48 Boulevard Vauban 59046 Lille France

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Gomez-Sagasti M.T., Alkorta I., Becerril J.M., Epelde L., Anza M., Garbisu C. Microbial Monitoring of the Recovery of Soil Quality During Heavy Metal Phytoremediation. Water Air Soil Pollut. 2012;223:3249–3262. doi: 10.1007/s11270-012-1106-8. DOI

Panagos P., van Liedekerke M., Yigini Y., Montanarella L. Contaminated Sites in Europe: Review of the Current Situation Based on Data Collected through a European Network. J. Environ. Public Health. 2013;2013:11. doi: 10.1155/2013/158764. PubMed DOI PMC

Al Souki K.S., Liné C., Louvel B., Waterlot C., Douay F., Pourrut B. Miscanthus × giganteus Culture on Soils Highly Contaminated by Metals: Modelling Leaf Decomposition Impact on Metal Mobility and Bioavailability in the Soil–Plant System. Ecotoxicol. Environ. Saf. 2020;199:110654. doi: 10.1016/j.ecoenv.2020.110654. PubMed DOI

Al Souki K.S., Burdová H., Trubač J., Štojdl J., Kuráň P., Kříženecká S., Machová I., Kubát K., Popelka J., Auer Malinská H., et al. Enhanced Carbon Sequestration in Marginal Land Upon Shift towards Perennial C4 Miscanthus × giganteus: A Case Study in North-Western Czechia. Agronomy. 2021;11:293. doi: 10.3390/agronomy11020293. DOI

Techer D., Martinez-Chois C., Laval-Gilly P., Henry S., Bennasroune A., D’Innocenzo M., Falla J. Assessment of Miscanthus × giganteus for Rhizoremediation of Long Term PAH Contaminated Soils. Appl. Soil Ecol. 2012;62:42–49. doi: 10.1016/j.apsoil.2012.07.009. DOI

Técher D., Laval-Gilly P., Henry S., Bennasroune A., Martinez-Chois C., D’Innocenzo M., Falla J. Prospects of Miscanthus × giganteus for PAH Phytoremediation: A Microcosm Study. Ind. Crop. Prod. 2012;36:276–281.

Al Souki K.S., Burdová H., Mamirova A., Kuráň P., Kříženecká S., Oravová L., Tolaszová J., Nebeská D., Popelka J., Ust’ak S., et al. Evaluation of the Miscanthus × giganteus Short Term Impacts on Enhancing the Quality of Agricultural Soils Affected by Single and/or Multiple Contaminants. Environ. Technol. Innov. 2021;24:101890. doi: 10.1016/j.eti.2021.101890. DOI

Nsanganwimana F., Pourrut B., Waterlot C., Louvel B., Bidar G., Labidi S., Fontaine J., Muchembled J., Sahraoui A.L.-H., Fourrier H., et al. Metal Accumulation and Shoot Yield of Miscanthus × giganteus Growing in Contaminated Agricultural Soils: Insights into Agronomic Practices. Agric. Ecosyst. Environ. 2015;213:61–71. doi: 10.1016/j.agee.2015.07.023. DOI

Nsanganwimana F., Waterlot C., Louvel B., Pourrut B., Douay F. Metal, Nutrient and Biomass Accumulation During the Growing Cycle of Miscanthus Established on Metal-Contaminated Soils. J. Plant Nutr. Soil Sci. 2016;179:257–269. doi: 10.1002/jpln.201500163. DOI

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. 2015;22:3043–3054. doi: 10.1007/s11356-014-3585-1. PubMed DOI

Al Souki K.S., Louvel B., Douay F., Pourrut B. Assessment of Miscanthus × giganteus Capacity to Restore the Functionality of Metal-Contaminated Soils: Ex Situ Experiment. Appl. Soil Ecol. 2017;115:44–52. doi: 10.1016/j.apsoil.2017.03.002. DOI

Küpper H., Andersen E. Mechanisms of Metal Toxicity in Plants. Metallomics. 2016;8:269–285. doi: 10.1039/C5MT00244C. PubMed DOI

Andrejić G., Šinžar-Sekulić J., Prica M., Dželetović Ž., Rakić T. Phytoremediation Potential and Physiological Response of Miscanthus × giganteus Cultivated on Fertilized and Non-Fertilized Flotation Tailings. Environ. Sci. Pollut. Res. 2019;26:34658–34669. doi: 10.1007/s11356-019-06543-7. PubMed DOI

Mazid M., Khan T.A., Mohammad F. Role of Secondary Metabolites in Defense Mechanisms of Plants. Biol. Med. 2011;3:232–249.

Lajayer B.M., Chorbanpour M., Nikabadi S. Heavy Metals in Contaminated Environment: Destiny of Secondary Metabolite Biosynthesis, Oxidative Status and Phytoextraction in Medicinal Plants. Ecotoxicol. Environ. Saf. 2017;145:377–390. doi: 10.1016/j.ecoenv.2017.07.035. PubMed DOI

Firmin S., Labidi S., Fontaine J., Laruelle F., Tisserant B., Nsanganwimana F., Pourrut B., Dalpé Y., Grandmougin A., Douay F., et al. Arbuscular Mycorrhizal Fungal Inoculation Protects Miscanthus × giganteus against Trace Element Toxicity in a Highly Metal-Contaminated Site. Sci. Total Environ. 2015;527–528:91–99. doi: 10.1016/j.scitotenv.2015.04.116. PubMed DOI

Lopareva-Pohu A., Pourrut B., Waterlot C., Garcon G., Bidar G., Pruvot C., Shirali P., Douay F. Assessment of Fly Ash-Aided Phytostabilisation of Highly Contaminated Soils After an 8-Year Field Trial: Part 1. Influence on Soil Parameters and Metal Extractability. Sci. Total Environ. 2011;409:647–654. doi: 10.1016/j.scitotenv.2010.10.040. PubMed DOI

Douay F., Pelfrêne A., Planque J., Fourrier H., Richard A., Roussel H., Girondelot B. Assessment of Potential Health Risk for Inhabitants Living Near a Former Lead Smelter. Part 1: Metal Concentrations in Soils, Agricultural Crops, and Homegrown Vegetables. Environ. Monit. Assess. 2013;185:3665–3680. doi: 10.1007/s10661-012-2818-3. PubMed DOI

Bradford M.M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Dringen R., Gutterer J.M. Glutathione Reductase from Bovine Brain. Methods Enzymol. 2002;348:281–288. PubMed

Nsanganwimana F., Al Souki K.S., Waterlot C., Douay F., Pelfrêne A., Ridošková A., Louvel B., Pourrut B. Potentials of Miscanthus × giganteus for Phytostabilization of Trace Element-Contaminated Soils: Ex Situ Experiment. Ecotoxicol. Environ. Saf. 2021;214:112125. doi: 10.1016/j.ecoenv.2021.112125. PubMed DOI

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:e0153475. PubMed PMC

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;56:1249–1258. doi: 10.1007/s11099-018-0827-3. DOI

Jiang H., Zhao X., Fang J., Xiao Y. Physiological Responses and Metal Uptake of Miscanthus Under Cadmium/Arsenic Stress. Environ. Sci. Pollut. Res. 2018;25:28275–28284. doi: 10.1007/s11356-018-2835-z. PubMed DOI

Zhang J., Yang S., Huang Y., Zhou S. The Tolerance and Accumulation of Miscanthus Sacchariflorus (Maxim.) Benth., an Energy Plant Species, to Cadmium. Int. J. Phytoremediat. 2015;17:538–545. doi: 10.1080/15226514.2014.922925. PubMed DOI

Fernando A., Oliveira J.S. Effects on Growth, Productivity and Biomass Quality of Miscanthus × giganteus of Soils Contaminated with Heavy Metals; Proceedings of the Biomass for Energy, Industry and Climate Protection: 2nd World Biomass Conference; Rome, Italy. 10 May 2004.

Pourrut B., Shahid M., Dumat C., Winterton P., Pinelli E. Lead Uptake, Toxicity, and Detoxification in Plants. Rev. Environ. Contam. Toxicol. 2011;213:113–136. PubMed

Suzuki N., Koussevitzky S., Mittler R., Miller G. ROS and Redox Signalling in the Response of Plants to Abiotic Stress. Plant Cell Environ. 2012;35:259–270. doi: 10.1111/j.1365-3040.2011.02336.x. PubMed DOI

Shahid M., Pourrut B., Dumat C., Nadeem M., Aslam M., Pinelli E. Heavy-Metal-Induced Reactive Oxygen Species: Phytotoxicity and Physicochemical Changes in Plants. Rev. Environ. Contam. Toxicol. 2014;232:1–44. PubMed

Berni R., Luyckx M., Xu X., Legay S., Sergeant K., Hausman J.-F., Lutts S., Cai G., Guerriero G. Reactive Oxygen Species and Heavy Metal Stress in Plants: Impact on the Cell Wall and Secondary Metabolism. Environ. Exp. Bot. 2019;161:98–106. doi: 10.1016/j.envexpbot.2018.10.017. DOI

Sharma A., Shahzad B., Rehman A., Bhardwaj R., Landi M., Zheng B. Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants Under Abiotic Stress. Molecules. 2019;24:2452. doi: 10.3390/molecules24132452. PubMed DOI PMC

Das S.K., Patra J.K., Thatoi H. Antioxidative Response to Abiotic and Biotic Stresses in Mangrove Plants: A Review. Int. Rev. Hydrobiol. 2016;101:3–19. doi: 10.1002/iroh.201401744. DOI

Mierziak J., Kostyn K., Kulma A. Flavonoids as Important Molecules of Plant Interactions with the Environment. Molecules. 2014;19:16240–16265. doi: 10.3390/molecules191016240. PubMed DOI PMC

Baek S.-A., Han T., Ahn S.-K., Kang H., Cho M.R., Lee S.-C., Im K.-H. Effects of Heavy Metals on Plant Growths and Pigment Contents in Arabidopsis Thaliana. Plant Pathol. J. 2012;28:446–452. doi: 10.5423/PPJ.NT.01.2012.0006. DOI

Šamec D., Karalija E., Šola I., Vujčić Bok V., Salope-Sondi B. The Role of Polyphenols in Abiotic Stress Response: The Influence of Molecular Structure. Plants. 2021;10:118. doi: 10.3390/plants10010118. PubMed DOI PMC

Martínez-Alcala I., Hernandez L.E., Esteban E., Walker D.J., Bernal M.P. Responses of Noccaea Caerulescens and Lupinus Albus in Trace Elements-Contaminated Soils. Plant Physiol. Biochem. 2013;66:47–55. doi: 10.1016/j.plaphy.2013.01.017. PubMed DOI

Singh S., Parihar P., Singh R., Singh V.P., Prasad S.M. Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics and Ionomics. Front. Plant Sci. 2016;6:1–36. doi: 10.3389/fpls.2015.01143. PubMed DOI PMC

Rezayian M., Niknam V., Ebrahimzadeh H. Oxidative Damage and Antioxidative System in Algae. Toxicol. Rep. 2019;6:1309–1313. doi: 10.1016/j.toxrep.2019.10.001. PubMed DOI PMC

Gill S.S., Khan N.A., Tuteja N. Cadmium at High Dose Perturbs Growth, Photosynthesis and Nitrogen Metabolism While at Low Dose It up Regulates Sulfur Assimilation and Antioxidant Machinery in Garden Cress (Lepidium Sativum L.) Plant Sci. 2012;182:112–120. doi: 10.1016/j.plantsci.2011.04.018. PubMed DOI

Lopez-Orenes A., Bueso M.C., Conesa H.M., Calderon A.A., Ferrer M.A. Seasonal Changes in Antioxidative/Oxidative Profile of Mining and Non-Mining Populations of Syrian Beancaper as Determined by Soil Conditions. Sci. Total Environ. 2017;575:437–447. doi: 10.1016/j.scitotenv.2016.10.030. PubMed DOI

Pandey N., Pathak G.C., Pandey D.K., Pandey R. Heavy Metals, Co, Ni, Cu, Zn and Cd, Produce Oxidative Damage and Evoke Differential Antioxidant Responses in Spinach. Braz. J. Plant Physiol. 2009;21:103–111. doi: 10.1590/S1677-04202009000200003. DOI

Gill S.S., Tuteja N. Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants. Plant Physiol. Biochem. 2010;48:909–930. doi: 10.1016/j.plaphy.2010.08.016. PubMed DOI

Fernandez R., Bertrand A., Reis R., Mourato M.P., Martins L.L., Gonzalez A. Growth and Physiological Responses to Cadmium Stress of Two Populations of Dittrichia viscosa (L.) Greuter. J. Hazard. Mater. 2013;244–245:555–562. doi: 10.1016/j.jhazmat.2012.10.044. PubMed DOI

Evaluation of Miscanthus × giganteus Tolerance to Trace Element Stress: Field Experiment with Soils Possessing Gradient Cd, Pb, and Zn Concentrations

Response of Three Miscanthus × giganteus Cultivars to Toxic Elements Stress: Part 2, Comparison between Two Growing Seasons