The positive impact on restoring soil functionality, decreasing toxic elements (TE) bioaccessibility, and enhancing soil physicochemical and biological parameters established a consensus on considering a Miscanthus × giganteus convenient species for phytomanaging wide TE contaminated areas. Nevertheless, information about the plant's mode of reaction to elevated soil multi-TE concentrations is still scarce. For the sake of investigating the miscanthus response to stressful TE concentrations, an ex-situ pot experiment was initiated for 18 months, with three miscanthus cultivars referred to as B, U, and A planted in soils with gradient Cd, Pb, and Zn concentrations. A non-contaminated control soil was introduced as well, and plants were cultivated within. Results revealed that the long exposure to increasing soil TE concentrations caused the number of tillers per plant to decline and the TE concentrations in the leaves to boost progressively with the soil contamination. The photosynthetic pigments (chlorophyll a, b, and carotenoids) were negatively affected as well. However, the phenolic compounds, flavonoids, tannins, and anthocyanins, along with the antioxidant enzymatic activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase elevated progressively with the TE concentration and exposure duration. Conclusively, miscanthus plants demonstrated an intensified and synchronized antioxidative activity against the TE concentration.

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

Department of the Environment Faculty of Environment Jan Evangelista Purkyně University in Ústí nad Labem Pasteurova 3632 15 400 96 Usti nad Labem Czech Republic

Laboratoire Écologie Fonctionnelle et Environnement Université de Toulouse CNRS INPT UPS ENSAT Avenue de l'Agrobiopôle F 31326 Castanet Tolosan France

Laboratoire Génie Civil et géo Environnement ISA Lille Junia 48 Boulevard Vauban CEDEX F 59046 Lille France

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Antoniadis V., Golia E.E., Liu Y.-T., Wang S.-L., Shaheen S.M., Rinklebe J. Soil and Maize Contamination by Trace Elements and Associated Health Risk Assessment in the Industrial Area of Volos, Greece. Environ. Int. 2019;124:79–88. doi: 10.1016/j.envint.2018.12.053. PubMed DOI

Agyeman P.C., John K., Kebonye N.M., Borůvka L., Vašát R., Drábek O., Němeček K. Human Health Risk Exposure and Ecological Risk Assessment of Potentially Toxic Element Pollution in Agricultural Soils in the District of Frydek Mistek, Czech Republic: A Sample Location Approach. Environ. Sci. Eur. 2021;33:137. doi: 10.1186/s12302-021-00577-w. 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

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

Hu Y., Nan Z., Su J., Wang N. Heavy Metal Accumulation by Poplar in Calcareous Soil with Various Degrees of Multi-Metal Contamination: Implications for Phytoextraction and Phytostabilization. Environ. Sci. Pollut. Res. 2013;20:7194–7203. doi: 10.1007/s11356-013-1711-0. PubMed 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

Dary M., Chamber-Perez M.A., Palomares A.J., Pajuelo E. “In Situ” Phytostabilisation of Heavy Metal Polluted Soils Using Lupinus Luteus Inoculated with Metal Resistant Plant-Growth Promoting Rhizobacteria. J. Hazard. Mater. 2010;177:323–330. doi: 10.1016/j.jhazmat.2009.12.035. PubMed DOI

Epelde L., Becerril J.M., Mijangos I., Garbisu C. Evaluation of the Efficiency of a Phytostabilization Process with Biological Indicators of Soil Health. J. Environ. Qual. 2009;38:2041–2049. doi: 10.2134/jeq2009.0006. PubMed DOI

Bidar G., Pruvot C., Garcon G., Verdin A., Shirali P., Douay F. Seasonal and Annual Variations of Metal Uptake, Bioaccumulation, and Toxicity in Trifolium Repens and Lolium Perenne Growing in a Heavy Metal-Contaminated Field. Environ. Sci. Pollut. Res. 2009;16:42–53. doi: 10.1007/s11356-008-0021-4. PubMed DOI

Bidar G., Garcon G., Pruvot C., Dewaele D., Cazier F., Douay F., Shirali P. Behavior of Trifolium Repens and Lolium Perenne Growing in a Heavy Metal Contaminated Field: Plant Metal Concentration and Phytotoxicity. Environ. Pollut. 2007;147:546–553. doi: 10.1016/j.envpol.2006.10.013. 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

Pourrut B., Lopareva-Pohu A., Pruvot C., Garcon G., Verdin A., Waterlot C., Bidar G., Shirali P., Douay F. Assessment of Fly Ash-Aided Phytostabilisation of Highly Contaminated Soils after an 8-Year Field Trial—Part 2. Influence on Plants. Sci. Total Environ. 2011;409:4504–4510. doi: 10.1016/j.scitotenv.2011.07.047. PubMed DOI

Bidar G., Waterlot C., Verdin A., Proix N., Courcot D., Detriche S., Fourrier H., Richard A., Douay F. Sustainability of an in Situ Aided Phytostabilisation on Highly Contaminated Soils Using Fly Ashes: Effects on the Vertical Distribution of Physicochemical Parameters and Trace Elements. J. Environ. Manage. 2016;171:204–216. doi: 10.1016/j.jenvman.2016.01.029. PubMed DOI

Nsanganwimana F., Pourrut B., Mench M., Douay F. Suitability of Miscanthus Species for Managing Inorganic and Organic Contaminated Land and Restoring Ecosystem Services. A Review. J. Environ. Manage. 2014;143:123–134. doi: 10.1016/j.jenvman.2014.04.027. PubMed 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

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

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., 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

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

Arduini I., Masoni A., Mariotti M., Ercoli L. Low Cadmium Application Increase Miscanthus Growth and Cadmium Translocation. Environ. Exp. Bot. 2004;52:89–100. doi: 10.1016/j.envexpbot.2004.01.001. 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. doi: 10.1371/journal.pone.0153475. PubMed DOI PMC

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. Phytoremediation. 2015;17:538–545. doi: 10.1080/15226514.2014.922925. PubMed DOI

Al Souki K.S., Liné C., Douay F., Pourrut B. Response of Three Miscanthus × Giganteus Cultivars to Toxic Elements Stress: Part 1, Plant Defence Mechanisms. Plants. 2021;10:2035. doi: 10.3390/plants10102035. PubMed DOI PMC

Sterckeman T., Douay F., Proix N., Fourrier H., Perdrix E. Assessment of the Contamination of Cultivated Soils by Eighteen Trace Elements around Smelters in the North of France. Water Air Soil Pollut. 2002;135:173–194. doi: 10.1023/A:1014758811194. DOI

Waterlot C., Bidar G., Pelfrêne A., Roussel H., Fourrier H., Douay F. Contamination, Fractionation and Availability of Metals in Urban Soils in the Vicinity of Former Lead and Zinc Smelters, France. Pedosphere. 2013;23:143–159. doi: 10.1016/S1002-0160(13)60002-8. 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

Giannopolitis C.N., Ries S.K. Superoxide Dismutases: I. Occurrence in Higher Plants. Plant Physiol. 1977;59:309–314. doi: 10.1104/pp.59.2.309. PubMed DOI PMC

Nakano Y., Asada K. Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant Cell Physiol. 1981;22:867–880.

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

Lichtenthaler H.K. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods Enzymol. 1987;148:350–382.

Fernando A., Oliveira J.S. Effects on Growth, Productivity and Biomass Quality of Miscanthus × giganteus of Soils Contaminated with Heavy Metals; Proceedings of the 2nd World Conference on Biomass for Energy, Industry and Climate Protection; Rome, Italy. 10–14 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

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

Scebba F., Arduini I., Ercoli L., Sebastiani L. Cadmium Effects on Growth and Antioxidant Enzymes Activities in Miscanthus Sinensis. Biol. Plant. 2006;50:688–692. doi: 10.1007/s10535-006-0107-0. DOI

Akula R., Ravishankar G.A. Influence of Abiotic Stress Signals on Secondary Metabolites in Plants. Plant Signal. Behav. 2011;6:1720–1731. doi: 10.4161/psb.6.11.17613. PubMed DOI PMC

Arduini I., Ercoli L., Mariotti M., Masoni A. Response of Miscanthus to Toxic Cadmium Applications during the Period of Maximum Growth. Environ. Exp. Bot. 2006;55:29–40. doi: 10.1016/j.envexpbot.2004.09.009. DOI

Pajević S., Borišev M., Nikolić N., Arsenov D.D., Orlović S., Župunski M. Phytoremediation, Management of Environmental Contaminants. Volume 3 Springer; Berlin/Heidelberg, Germany: 2016. Phytoextraction of Heavy Metals by Fast-Growing Trees: A Review.

Vijayaraghavan K., Arockiaraj J., Kamala-Kannan S. Portulaca Grandiflora as Green Roof Vegetation: Plant Growth and Phytoremediation Experiments. Int. J. Phytoremediation. 2017;19:537–544. doi: 10.1080/15226514.2016.1267699. PubMed DOI

Kumar A., Prasad M.N.V., Sytar O. Lead Toxicity, Defense Strategies and Associated Indicative Biomarkers in Talinum Triangulare Grown Hydroponically. Chemosphere. 2012;89:1056–1065. doi: 10.1016/j.chemosphere.2012.05.070. PubMed DOI

Hamels F., Malevé J., Sonnet P., Kleja D.B., Smolders E. Phytotoxicity of Trace Metals in Spiked and Field-Contaminated Soils: Linking Soil-Extractable Metals with Toxicity. Environ. Toxicol. Chem. 2014;33:2479–2487. doi: 10.1002/etc.2693. PubMed DOI

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