The cup plant (Silphium perfoliatum L.) – a viable solution for bioremediating soils polluted with heavy metals

Radu L. SUMALAN; Cornelia  MUNTEAN; Ana  KOSTOV; Daniel  KRŽANOVIĆ; Noemi L.  JUCSOR; Sorin I.  CIULCA; Renata M.  SUMALAN; Marius  GHEJU; Mariana  CERNICOVA-BUCA

doi:10.15835/nbha48412160

Authors

Radu L. SUMALAN Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania” from Timisoara, Faculty of Horticulture and Forestry, 119 Calea Aradului, 300645, Timisoara (RO) https://orcid.org/0000-0001-5252-8921
Cornelia MUNTEAN Politehnica University Timisoara, Faculty of Industrial Chemistry and Environmental Engineering, 6 Bv. Vasile Parvan, 300223, Timisoara (RO)
Ana KOSTOV Mining and Metallurgy Institute Bor, 35 Zeleni bulevar, 19210, Bor (RS)
Daniel KRŽANOVIĆ Mining and Metallurgy Institute Bor, 35 Zeleni bulevar, 19210, Bor (RS)
Noemi L. JUCSOR Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania” from Timisoara, Faculty of Horticulture and Forestry, 119 Calea Aradului, 300645, Timisoara (RO)
Sorin I. CIULCA Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania” from Timisoara, Faculty of Horticulture and Forestry, 119 Calea Aradului, 300645, Timisoara (RO)
Renata M. SUMALAN Banat’s University of Agricultural Sciences and Veterinary Medicine “King Michael I of Romania” from Timisoara, Faculty of Horticulture and Forestry, 119 Calea Aradului, 300645, Timisoara (RO)
Marius GHEJU Politehnica University Timisoara, Faculty of Industrial Chemistry and Environmental Engineering, 6 Bv. Vasile Parvan, 300223, Timisoara (RO)
Mariana CERNICOVA-BUCA Politehnica University Timisoara, Faculty of Communication Sciences, 2/A Str. Traian Lalescu, 300223, Timisoara (RO)

DOI:

https://doi.org/10.15835/nbha48412160

Keywords:

bioaccumulation factor; contaminated areas; cup plant; phytoextraction; removal efficiency translocation factor

Abstract

Heavy metal pollution, manifested by the accumulation, toxicity and persistence in soil, water, air, and living organisms, is a major environmental problem that requires energetic resolution. Mining tailing areas contain metal minerals such as Cu, Zn, Pb, Cr and Cd in high concentrations that pollute the environment and pose threats to human health. Phytoremediation represents a sustainable, long-term, and relatively inexpensive strategy, thus proving to be convenient for stabilizing and improving the environment in former heavy metal-polluted mining sites. This study presents the bioremediation potential of Silphium perfoliatum L. plants, in the vegetative stages of leaf rosette formation, grown on soil polluted with heavy metals from mining dumps in Moldova-Noua, in the Western part of Romania. The bioaccumulation factor (BAF), translocation factor (TF), metal uptake (MU) and removal efficiency (RE) of Cu, Zn, Cr and Pb by S. perfoliatum plants were determined in a potted experiment in controlled environmental conditions. The reference quantities of heavy metals have been determined in the studied soil sample. The experiment followed the dynamics of the translocation and accumulation of heavy metals in the soil, in the various organs of the silphium plants, during the formation of the leaf rosette (13-18 BBCH). The determination of the amount of heavy metals in soil and plants was achieved by the method of digestion with hydrochloric and nitric acid 3/1 (v/v) quantified by atomic absorption spectroscopy (AAS). The obtained experimental results demonstrate that the substrate has a high heavy metal content being at the alert threshold for Zn (260.01 mg kg^-1in substrate compared with alert threshold 300 mg kg^-1) and at intervention thresholds for other metals (Cu -234.66 mg kg^-1/200 mg kg^-1; 299.08 mg kg^-1/300 mg kg^-1 and Pb-175.18 mg kg^-1/100 mg kg^-1). The average concentration of the metals determined in dynamics in the dry biomass of plants varied between roots, petioles, and laminas. The root is the main accumulator for Cu and Cr (Cu – 37.32 mg kg^-1 -13 BBCH to 43.89 mg kg^-1-15 BBCH and 80.71 mg kg^-1 – 18 BBCH; Cr – 57.43 mg kg^-1 – 13 BBCH to 93.36 mg kg^-1 -18 BBCH), and for Zn and Pb the lamina seems to carry the same function. Preliminary results show that Silphium perfoliatum may be a viable alternative in the bioremediation and treatment of heavy metal-contaminated area.

References

Ali H, Khan E, Sajad MA (2013). Phytoremediation of heavy metals – Concepts and applications. Chemosphere 91(7):869-881. https://doi.org/10.1016/j.chemosphere.2013.01.075.

Alloway BJ, Zhang P, Mott C, Smith SR, Chambers BJ, Nicholson FA, … Andrews AJ (2000). The vulnerability of soils to pollution by heavy metals (Final Report for MAFF Project No. SP0127), London: MAFF.

Andra SS, Datta R, Sarkar D, Saminathan SK, Mullens CP, Bach SB (2009). Analysis of phytochelatin complexes in the lead tolerant vetiver grass [Vetiveria zizanioides (L.)] using liquid chromatography and mass spectrometry. Environmental Pollution 157:2173-2183. https://doi.org/10.1016/j.envpol.2009.02.014.

Anning AK, Korsah PE, Addo-Fordjour P (2013). Phytoremediation of wastewater with Limnocharis flava, Thalia geniculata and Typha latifolia in constructed wetlands. International Journal of Phytoremediation 15(5):452-464. https://doi.org/10.1080/15226514.2012.716098

Areco MM, Haug E, Curutchet G (2018). Studies on bioremediation of Zn and acid waters using Botryococcus braunii. Journal of Environmental Chemical Engineering 6:3849-3859. https://doi.org/10.1016/j.jece.2018.05.041.

Azimi A, Azri A, Rezkazemi M, Ansarpour M (2017). Removal of heavy metals from industrial wastewaters: a review. ChemBioEng Reviews 4:37-59. https://doi.org/10.1002/cben.201600010.

Baker AJM, Brooks RR (1989). Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81-126, http://dx.doi.org/10.1080/01904168109362867.

Bjelkova M, Gencurova V, Griga M (2011). Accumulation of cadmium by flax and linseed cultivars in field-simulated conditions:a potential for phytoremediation of Cd-contaminated soils. Industrial Crops and Products 33:761-774. https://doi.org/10.1016/j.indcrop.2011.01.020.

Bose S, Bhattacharyya AK (2008). Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70:1264-1272. https://doi.org/10.1016/j.chemosphere.2007.07.062.

Boyd RS (2010). Heavy metal pollutants and chemical ecology: Exploring new frontiers. Journal of Chemical Ecology 36:46-58. https://doi.org/10.1007/s10886-009-9730-5

Buscaroli A (2017). An overview of indexes to evaluate terrestrial plants for phytoremediation purposes (Review). Ecological Indicators 82:367-380. https://doi.org/10.1016/j.ecolind.2017.07.003.

Cao X, Wahbi A, Ma L, Li B, Yang Y (2009). Immobilization of Zn, Cu and Pb in contaminated soils using phosphate rock and phosphoric acid. Journal of Hazardous Material 164:555-564. https://doi.org/10.1016/j.jhazmat.2008.08.034.

Chirakkara RA, Cameselle C, Reddy KR (2016). Assessing the applicability of phytoremediation of soils with mixed organic and heavy metal contaminants. Reviews in Environmental Sciences and Biotechnology 15:299-326. https://doi.org/10.1007/s11157-016-9391-0.

Cho Y, Bolick JA, Butcher DJ (2009). Phytoremediation of lead with green onions (Allium fistulosum) and uptake of arsenic compounds by moonlight ferns (Pteris cretica cv Mayii). Microchemical Journal 91:6-8. http://dx.doi.org/10.1016/j.microc.2008.05.008.

Choińska-Pulita A, Sobolczyk-Bednareka J, Łaba W (2018). Optimization of copper, lead and cadmium biosorption onto newly isolated bacterium using a Box-Behnken design. Ecotoxicology and Environmental Safety 149:275-283. https://doi.org/10.1016/j.ecoenv.2017.12.008.

Ciulca S (2006). Metodologii de experimentare în agricultura şi biologie [Experimental methodologies in agriculture and biology]. Agroprint, Timisoara, Romania.

Cluis C (2004). Junk-greedy greens: phytoremediation as a new option for soil decontamination. Biotechnology Journal 2:61-67.

Demková L, Jezný T, Bobuľská L (2017). Assessment of soil heavy metal pollution in a former mining area – before and after the end of mining activities. Soil and water Research 12(4):229-236. https://doi.org/10.17221/107/2016-SWR.

Dubey S, Shri M, Gupta A, Rani V, Chakrabarty D (2018). Toxicity and detoxification of heavy metals during plant growth and metabolism. Environmental Chemistry Letters 16:1169-1192. https://doi.org/10.1007/s10311-018-0741-8

Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicology and Environmental Safety 106:164-172. https://doi.org/10.1016/j.ecoenv.2014.03.007

Energy Industry Review (2019). Mining Industry. Retrieved 2020 November 03 from https://energyindustryreview.com/metals-mining/mining-industry-left-without-miners-lamp/

Fang YY, Cao XD, Zhao L (2012). Effects of phosphorus amendments and plant growth on the mobility of Pb, Cu, and Zn in a multi-metal-contaminated soil. Environmental Science and Pollution Research 19(5):1659-1667. https://doi.org/10.1007/s11356-011-0674-2.

Feng Y, Wu Y, Zhang J, Meng Q, Wang Q, Ma L, Ma X, Yang X (2018). Ectopic expression of SaNRAMP3 from Sedum alfredii enhanced cadmium root-to-shoot transport in Brassica juncea. Ecotoxicology and Environmental Safety 156:279-286. https://doi.org/10.1016/j.ecoenv.2018.03.031.

Figas A, Rolbiecki R, Tomaszewska-Sowa M (2015). Influence of drip irrigation on the height of the biennial cup plant (Silphium perfoliatum L.) from the micropropagation seedlings. Infrastructure and Ecology of Rural Areas 3, Polska Akademia Nauk, Oddział w Krakowie pp 779-786. http://dx.medra.org/10.14597/infraeco.2015.3.2.062.

Fitzgerald EJ, Caffrey JM, Nesaratnam ST, McLoughlin P (2003). Copper and lead concentrations in salt marsh plants on the Suir Estuary, Ireland. Environmental Pollution 123(1):67-74. https://doi.org/10.1016/s0269-7491(02)00366-4.

Francis E (2017). Phytoremediation potentials of sunflower (Helianthus annuus L.) Asteraceae on contaminated soils of abandoned dumpsites. International Journal of Scientific & Engineering Research 8(1):1751-17157.

Fu W, Huang K, Cai HH, Li J, Zhai DL, Dai ZC, Du DL (2017). Exploring the potential of naturalized plants for phytoremediation of heavy metal contamination. International Journal of Environmental Research 11:515-521. https://doi.org/10.1007/s41742-017-0045-z.

Gansberger M, Montgomery LFR, Liebhard P (2015) Botanical characteristics, crop management and potential of Silphium perfoliatum L. as a renewable resource for biogas production: A review, Industrial Crops and Products 63:362-372. https://doi.org/10.1016/j.indcrop.2014.09.047.

Gavrilescu M (2004). Removal of heavy metal from environment by biosorbtion. Engineering in Life Sciences 4:219-232. https://doi.org/10.1002/elsc.200420026.

Gawronski SW, GAWRONSKA H (2007). Plant taxonomy for phytoremediation. In: Marmioli N, Samotokin B, Marmioli M (Eds). Advanced Science and Technology for Biological Decontamination of Sites Affected by Chemical and Radiological Nuclear Agents. Springer Nederlands, NATO Series IV, pp 79-88. https://doi.org/10.1007/978-1-4020-5520-1.

Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Skarzhinskaya M … Raskin I (1999). Use of plant roots for phytoremediation and molecular farming. Proceedings of National Academy of Sciences of the United States of America 96(11):5973-5977.

Greger M (1999). Metal availability and bioconcentration in plants. In: Heavy Metal Stress in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-07745-0_1.

Gupta S, Nayek S, Saha RN, Satpati S (2008). Assessment of heavy metal accumulation in macrophyte, agricultural soil, and crop plants adjacent to discharge zone of sponge iron factory. Environmental. Geology 55(4):731-739. https://doi.org/10.1007/s00254-007-1025-y.

Haag NL, Nägele HJ, Reiss K, Biertümpfel A, Oechsner H (2015). Methane formation potential of cup plant (Silphium perfoliatum). Biomass and Bioenergy 75:126-133. https://doi.org/10.1016/j.biombioe.2015.02.012.

Hanif MA, Bhatti HN (2015). Remediation of heavy metals using easily cultivable, fast growing, and highly accumulating white rot fungi from hazardous aqueous streams. Desalination and Water Treatment 53(1):238-248. https://doi.org/10.1080/19443994.2013.848413.

Hansda A, Kumar V, Anshumali V, Usmani Z (2014). Phytoremediation of heavy metals contaminated soil using plant growth promoting rhizobacteria (PGPR): a current perspective. Recent Research in Science and Technology 6(1):131-134. http://updatepublishing.com/journal/index.php/rrst/article/view/1183.

Harmanescu M, Alda LM, Bordean DM, Gogoasa I, Gergen I (2011). Heavy metals health risk assessment for population via consumption of vegetables grown in old mining area; a case study: Banat County, Romania. Chemistry Central Journal 5:64. https://doi.org/10.1186/1752-153X-5-64.

Hemen S (2011). Metal hyperaccumulation in plants: a review focusing on phytoremediation technology. Journal of Environmental Science and Technology 4(2):118-138. https://doi.org/1-.3923/jest.2011.118.138.

Huang DL, Liu LS, Zeng GM, Xu P, Huang C, Deng LJ, Wang R, Wan J (2017). The effects of rice straw biochar on indigenous microbial community and enzymes activity in heavy metal-contaminated sediment. Chemosphere 174:545-553. https://doi.org/10.1016/j.chemosphere.2017.01.130.

Hudson-Edwards KA, Jamieson HE, Lottermoser BG (2011). Mine wastes: past, present, future. Elements 7(6):375-380. https://doi.org/10.2113/gselements.7.6.375.

IPNI (2020). International plant names index. The Royal Botanic Gardens, Kew, Harvard University Herbaria & Libraries and Australian National Botanic Gardens. Retrieved 2020 November 06 from http://www.ipni.org.

ISO 11464 (2006). https://standards.iteh.ai/catalog/standards/iso/63199580-e1a0-4537-a141-ab923c298e27/iso-11464-2006.

ISO 11047 (1998). https://www.iso.org/obp/ui/#iso:std:iso:11047:ed-1:v1:en

Jadia CD, Fulekar MH (2009). Phytoremediation of heavy metals: Recent techniques. African Journal of Biotechnology 8:921-928.

Jucsor N, Sumalan R (2018). Researches concerning the potential of biomass accumulation in cup plant (Silphium perfoliatum L.). Journal of Horticulture, Forestry and Biotechnology 22(2):34-39.

Keller BEM, Lajtha K, Cristofor S (1998). Trace metal concentrations in the sediments and plants of the Danube Delta, Romania. Wetland 18(1):42-50

Klimont K (2007). Ocena przydatności wybranych gatunków roślin użytkowych do rekultywacji terenów zdewastowanych przez przemysł i gospodarkę komunalną- Assessment of the suitability of selected plant species for the remediation of land devastated by industry and municipal economy. Problemy Inżynierii Rolniczej 2(56):27-36.

Kramer U (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology 61:517-534. https://doi.org/10.1146/annurev-arplant-042809-112156.

Laghlimi M, Baghdad B, El Hadi H, Bouabdli, A (2015). Phytoremediation Mechanisms of heavy metal contaminated soils: a review. Open Journal of Ecology 5:375-388. http://dx.doi.org/10.4236/oje.2015.58031.

Li ZY, Ma ZW, van der Kuijp TJ, Yuan ZW, Huang L (2014). A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Science of the Total Environment 468:843-853. https://doi.org/10.1016/j.scitotenv.2013.08.090.

Liakopoulos A, Lemiere B, Michael K, Crouzet C, Laperche V, Romaidis I, … Lassin A (2010). Environmental impacts of unmanaged solid waste at a former base metal mining and ore processing site (Kirki, Greece). Waste Management and Research 28:996-1009. https://doi.org/10.1177%2F0734242X10375746.

Lu Y, Li X, He M, Zeng F (2013). Behavior of native species Arrhenatherum elatius (Poaceae) and Sonchus transcaspicus (Asteraceae) exposed to a heavy metal-polluted field: plant metal concentration, phytotoxicity, and detoxification responses. International Journal of Phytoremediation 15(10):924-937. https://doi.org/10.1080/15226514.2012.735288

Ma L, Sun J, Yang Z, Wang L (2015). Heavy metal contamination of agricultural soils affected by mining activities around the Gabxi River in Chenzhou Southern China. Environmental Monitoring and Assessment 187:731-740. https://doi.org/10.1007/s10661-015-4966-8.

Majtkowski W, Szulc PM, Gaca J, Mikołajczyk J (2010). Assessment of the use of Silphium perfoliatum L. in phytoremediation of sites contaminated with heavy metals. Biuletyn Instytutu Hodowli i Aklimatyzacji Roślin 256:163-169.

Martín-Lara MA, Blázquez G, Trujillo MC, Pérez A, Calero M (2014). New treatment of real electroplating wastewater containing heavy metal ions by adsorption onto olive stone. Journal of Cleaner Production 81:120-129. https://doi.org/10.1016/j.jclepro.2014.06.036.

Meers E, Ruttens A, Hopgood M, Lesage E, Tack FMG (2005). Potential of Brassica rapa, Cannabis sativa, Helianthus annuus and Zea mays for phytoextraction of heavy metals from calcareous dredged sediment derived soils. Chemosphere 61:561-572. https://doi.org/10.1016/j.chemosphere.2005.02.026.

Meier U, Bleiholder H, Buhr L, Feller C, Hacks H, Hess M, … Boom, TVD (2009) The BBCH system to coding the phenological growth stages of plants-history and publications. Journal of Cultivated Plants 2:41-52.

Nikolic M, Stevovic S (2015). Family Asteraceae as a sustainable planning tool in phytoremediation and its relevance in urban areas. Urban Forestry and Urban Greening 14:782-789. https://doi.org/10.1016/j.ufug.2015.08.002

Nouri J, Khorasani N, Lorestani B, Karami M, Hassani AH, Yousefi N (2009). Accumulation of heavy metals in soil and uptake by plant species with phytoremediation potential. Environmental Earth Science 59:315-323. https://doi.org/10.1007/s12665-009-0028-2.

Nowack B, Schulin R, Robinson BH (2006). Critical assessment of chelant-enhanced metal phytoextraction. Environmental Science and Technology 40(17):5225-5232. https://doi.org/10.1021/es0604919

Olguín EJ, Sánchez-Galván G (2012). Heavy metal removal in phytofiltration and phytoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnology 30(1):3-8. https://doi.org/10.1016/j.nbt.2012.05.020.

Order 756/1997, Environmental Pollution Assessment Regulation (1997). Ordinul nr. 756/1997 pentru aprobarea Reglementării privind evaluarea poluării mediului. Ministerul Apelor, Pădurilor și Protecţiei Mediului. Retrieved 2020 October 29 from http://www.mmediu.ro/app/webroot/uploads/files/OM-184-1997-bilant-de-mediu-si-OM-756-1997-evaluarea-poluarii-mediului.pdf .

Ostrowska A, Porebska G, Szczubiałka Z (2006). Limitation of Pb and Cd uptake by pine. Environmental Engineering Science 23:595-602. https://doi.org/10.1089/ees.2006.23.595.

Palmer CE, Warwick S, Keller W (2001). Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. International Journal of Phytoremediation 3:245-287. https://doi.org/10.1080/15226510108500059.

Pan LB, Ma J, Wang XL, Hou H (2016). Heavy metals in soils from a typical county in Shanxi Province, China: levels, sources and spatial distribution. Chemosphere 148:248-254. https://doi.org/10.1016/j.chemosphere.2015.12.049.

Pehoiu G, Radulescu C, Murarescu O, Dulama ID, Bucurica IA, Teodorescu S, Stirbescu RM (2019). Health risk assessment associated with abandoned copper and uranium mine tailings. Bulletin of Environmental Contamination and Toxicology 102(4):504-510. https://doi.org/10.1007/s00128-019-02570-9

Pehoiu G, Murarescu O, Radulescu C. Dulama ID, Teodrescu S, Stirbescu RM, … Stanescu IG (2020). Heavy metals accumulation and translocation in native plants grown on tailing dumps and human health risk. Plant and Soil 456:405-424. https://doi.org/10.1007/s11104-020-04725-8.

Pratush A, Kumar A, Hu Z (2018). Adverse effect of heavy metals (As, Pb, Hg, and Cr) on health and their bioremediation strategies: a review. International Microbiology 21: 97-106. https://doi.org/10.1007/s10123-018-0012-3

Pu W, Sun J, Zhang F, Wen X, Liu W, Huang C (2019). Effects of copper mining on heavy metal contamination in a rice agrosystem in the Xiaojiang River Basin, southwest China. Acta Geochimica 38:753-773. https://doi.org/10.1007/s11631-019-00321-5.

Rascio N, Navari-Izzo F (2011). Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Science 180(2):169-181. https://doi.org/10.1016/j.plantsci.2010.08.016.

Robinson BH, Lombi E, Zhao FJ, McGrath, SP (2003). Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytologist 158:279-285. https://doi.org/10.1046/j.1469-8137.2003.00743x.

Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47(3):339-347. https://doi.org/10.1016/S0031-9422(97)00593-1.

Sall ML, Diaw AKD, Gningue-Sall D, Aaron SE, Aaron JJ (2020) Toxic heavy metals: impact on the environment and human health, and treatment with conducting organic polymers, a review. Environ Sciences and Pollution Research 27:29927-29942. https://doi.org/10.1007/s11356-020-09354-3.

Sharma S, Singh B, Manchanda VK (2015). Phytoremediation: role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environmental Science and Pollution Research 22:946-962. https://doi.org/10.1007/s11356-014-3635-8.

Shen X, Chi Y, Xiong K (2019) The effect of heavy metal contamination on humans and animals in the vicinity of a zinc smelting facility. PLoS One 14(10):e0207423. https://doi.org/10.1371/journal.pone.0207423

Shi X, Zhang X, Chen G, Chen Y, Wang L, Shan X (2011). Seedling growth and metal accumulation of selected woody species in copper and lead/zinc mine tailings. Journal of Environmental Sciences 23(2):266-274. https://doi.org/10.1016/S1001-0742(10)60402-0

Shri M, Dave R, Diwedi S, Shukla D, Kesari R, Tripathi RD, Trivedi PK, Chakrabarty D (2014) Heterologous expression of Ceratophyllum demersum phytochelatin synthase, CdPCS1, in rice leads to lower arsenic accumulation in grain. Scientific Report 4:5784. https://doi.org/10.1038/srep05784

Singh M, Kumar J, Singh S, Singh VP, Prasad SM, Singh MPV (2015). Adaptation strategies of plants against heavy metal toxicity: a short review. Biochemistry and Pharmacology 4:161. https://doi.org/10.4172/2167-0501.1000161

Singh N, Kaur M, Katnoria JK (2017). Analysis on bioaccumulation of metals in aquatic environment of Beas River Basin: A case study from Kanjli wetland. GeoHealth 1:93-105. https://doi.org/10.1002/2017GH000062.

Sosa M, Salazar MJ, Zygadlo JA, Wannaz ED (2016). Effects of Pb in Tagetes minuta L. (Asteraceae) leaves and its relationship with volatile compounds. Industrial Crops and Products 82:37-43. https://doi.org/10.1016/j.indcrop.2015.12.011.

Stanislawska-Glubiak E, Korzeniowska J, Kocon A (2015). Effect of peat on the accumulation and translocation of heavy metals by maize grown in contaminated soils. Environmental Science and Pollution Research 22(6):4706-4714. https://doi.org/10.1007/s11356-014-3706-x

Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP, Tripathi RD (2012). Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicology and Environmental Safety 79:189-198. https://doi.org/10.1016/j.ecoenv.2011.12.019

Titei V (2014)-Biological peculiarities of cup plant (Silphium perfoliatum L.) and utilization possibilities in the Republic of Moldova. Scientific papers. Agronomy Series 57(1).

Truong P (1999). Vetiver grass technology for mine rehabilitation. In: Chamchalow N, Vessabutr S (Eds). Office of the Royal Development Board. Tech Bull No 1999/2, PRVN/RDPB, Bangkok, Thailand.

Verbruggen N, Hermans C, Schat H (2009). Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181:759-776. https://doi.org/10.1111/j.1469-8137.2008.02748.x

Von Cossel M, Amarysti C, Wilhelm H, Priya N, Winkler B, Hoerner L (2020). The replacement of maize (Zea mays L.) by cup plant (Silphium perfoliatum L.) as biogas substrate and its implications for the energy and material flows of a large biogas plant. Biofuels Bioproducts and Biorefinering 14:152-179. https://doi.org/10.1002/bbb.2084.

Wang T, Sun H (2013). Biosorption of heavy metals from aqueous solution by UV-mutant Bacillus subtilis. Environmental Science Pollution Research 20:7450-7463. https://doi.org/10.1007/s11356-013-1767-x

Wang SQ, Wei SH, Chen YQ, Mihajhov L (2017). Comparison of soybean cultivars enriching Cd and the application foreground of the low-accumulating cultivar in production. Polish Journal of Environmental Studies 26:1299-1304. https://doi.org/10.15244/pjoes/67576

Wei SH, Zhou QX (2004). Identification of weed species with hyperaccumulative characteristics of heavy metals. Progress in Natural Sciences 14:495-503. https://doi.org/10.1080/10020070412331343851.

Wei S, Li Y, Zhou Q, Srivastava M, Chiu S, Zhan J, … Sun T (2010). Effect of fertilizer amendments on phytoremediation of Cd-contaminated soil by a newly discovered hyperaccumulator Solanum nigrum L. Journal of Hazardous Material 176:269-273. https://doi.org/10.1016/j.jhazmat.2009.11.023.

Weis JS, Weis P (2004). Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environment International 30:685-700. https://doi.org/10.1016/j.envint.2003.11.002.

Xiao R, Shen F, Du J, Li R, Lahori AH, Zhang Z (2018). Screening of native plants from wasteland surrounding a Zn smelter in Feng County China, for phytoremediation. Ecotoxicology and Environmental Safety 162:178-183. https://doi.org/10.1016/j.ecoenv.2018.06.095.

Yang Q, Li Z, Lu X, Duan Q, Huang L, Bi J (2018). A review of soil heavy metal pollution from industrial and agricultural regions in China: Pollution and risk assessment. Science of The Total Environment 642(15):690-700. https://doi.org/10.1016/j.scitotenv.2018.06.068.

Yoon J, Cao X, Zhou Q, Ma LQ (2006). Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Science of the Total Environment 368:456-464. https://doi.org/10.1016/j.scitotenv.2006.01.016.

Yu JG, Zhao XH, Yu LY, Jiao FP, Jiang JH, Chen XQ (2013) Removal, recovery and enrichment of metals from aqueous solutions using carbon nanotubes. Journal of Radioanalytical Nuclear Chemistry. https://doi.org/10.1007/s10967-013-2818y.

Yu C, Peng X, Yan H, Li X, Zhou Z, Yan T (2015). Phytoremediation ability of Solanum nigrum L. to Cd-Contaminated soils with high levels of Cu, Zn, and Pb. Water Air and Soil Pollution 226:15. https://doi.org/10.1007/s11270-015-2424-4

Zhang X, Xia H, Li Z, Zhuang P, Gao B (2010). Potential of four forage grasses in remediation of Cd and Zn contaminated soils. Bioresource Technology 101:2063-2066.

Zhang Q, Li Y, Phanlavong P, Wang Z, Jiao T, Qiu H, Peng Q (2017). Highly efficient and rapid fluoride scavenger using an acid/base tolerant zirconium phosphate nanoflake: Behaviour and mechanism. Journal of Cleaner Production 161:317-326. https://doi.org/10.1016/j.jclepo.2017.05.120.

Zhang Q, Li Y, Yang Q, Chen H, Chen X, Jiao T, Peng Q (2018a). Distinguished Cr (VI) capture with rapid and superior capability using polydopamine microsphere: Behavior and mechanism. Journal of Hazardous Material 342:732. https://doi.org/10.1016/j.jhazmat.2017.08.061.

Zhang X, Li M, Yang H, Li X, Cui Z (2018b). Physiological response of Suaeda glauca and Arabidopsis thaliana in phytoremediation of heavy metals. Journal of Environmental Management 223(1):132-139. https://doi.org/10.1016/j.jenvman.2018.06.025.

Zhi-Xin N, Sun LN, Sun TH, Li YS, Wang H (2007) Evaluation of phytoextracting cadmium and lead by sunflower, ricinus, alfalfa and mustard in hydroponic culture. Journal of Environmental Sciences 19:961-967. https://doi.org/10.1016/s1001-0742(07)60158-2.

Zhu G, Xia H, Guo Q, Song B, Zheng G, Zhang Z, … Okoli CP (2018). Heavy metal contents and enrichment characteristics of dominant plants in wasteland of the downstream of a lead-zinc mining area in Guangxi, Southwest China. Ecotoxicology and Environmental Safety 151:266-271. https://doi.org/10.1016/j.ecoenv.2018.01.011