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Synergistic effect of pyrene and heavy metals (Zn, Pb, and Cd) on phytoremediation potential of Medicago sativa L. (alfalfa) in multi-contaminated soil

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Abstract

The environment in India is contaminated with polycyclic aromatic hydrocarbons (PAHs) due to the occurrence of large anthropogenic activities, i.e., fuel combustion, mineral roasting, and biomass burning. Hence, 13 toxic PAHs were detected: phenanthrene, anthracene, fluoranthene, pyrene, and benz(a) anthracene, ben-zo; (b) fluoranthene, benzo(k) fluoranthene, benzo(a) pyrene, benzo(ghi)perylene, dibenz (ah) anthracene, indeno1,2,3-(cd) pyrene, coronene and coronene in the environment (i.e., ambient particulate matter, road dust, sludge, and sewage) of the most industrialized area. Pollutants such as heavy metals and polycyclic aromatic hydrocarbons co-contaminate the soil and pose a significant hazard to the ecosystem because these pollutants are harmful to both humans and the environment. Phytoremediation is an economical plant-based natural approach for soil clean-up that has no negative impact on ecosystems. The aim of this study was to investigate the effects of pyrene (500 mg kg−1), Zn (150 mg kg−1), Pb (150 mg kg−1), and Cd (150 mg kg−1) alone and in combination on the phytoextraction efficiency of Medicago sativa growing in contaminated soil. Plant biomass, biochemical activities, translocation factors, accumulation of heavy metals, and pyrene removal were determined. After 60 days of planting, compared with those of the control plants, the growth parameters, biomass, and chlorophyll content of the M. sativa plants were significantly lower, and the reactive oxygen species activity, such as proline and polyphenol content and metallothionein protein content, was markedly greater in the pyrene and heavy metal-polluted soils. Furthermore, the combined toxicity of pyrene and all three metals on M. sativa growth and biochemical parameters was significantly greater than that of pyrene, Zn, Pb, or Cd alone, indicating the synergistic effect of pyrene and heavy metals on cytotoxicity. Pyrene stress increased Cd accumulation in M. sativa. After pyrene exposure alone or in combination with Zn-pyrene, a greater pyrene removal rate (85.5–81.44%) was observed than that in Pb-pyrene, Cd-pyrene, and Zn-Pb-Cd-pyrene polluted soils (62.78–71.27%), indicating that zinc can enhance the removal of pyrene from contaminated soil. The resulting hypotheses demonstrated that Medicago sativa can be used as a promising phytoremediation agent for co-contaminated soil.

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References

  • Abdelmigid HM, Hassan AM, El-Rab SMG (2014) Expression of metallothionein as a biomarker in response to various stress factors in different organisms. Int J Adv Res 2(10):683–695

    Google Scholar 

  • Ahammed GJ, Choudhary SP, Chen S, Xia X, Shi K, Zhou Y, Yu J (2013) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64(1):199–213

    Article  CAS  PubMed  Google Scholar 

  • Ahn YO, Kim SH, Lee J, Kim H, Lee HS, Kwak SS (2012) Three Brassica rapa metallothionein genes are differentially regulated under various stress conditions. Mol Biol Rep 39:2059–2067

    Article  CAS  PubMed  Google Scholar 

  • Alaboudi KA, Ahmed B, Brodie G (2018) Phytoremediation of Pb and Cd contaminated soils by using sunflower (Helianthus annuus) plant. Ann Agric Sci 63(1):123–127

    Article  Google Scholar 

  • Almeida CMR, Mucha AP, Delgado MF, Caçador MI, Bordalo AA, Vasconcelos MTS (2008) Can PAHs influence Cu accumulation by salt marsh plants? Mar Environ Res 66(3):311–318

    Article  CAS  PubMed  Google Scholar 

  • Araujo ASF, Miranda ARL, Oliveira MLJ, Santos VM, Nunes LAPL, Melo WJ (2015) Soil microbial properties after 5 years of consecutive amendment with composted tannery sludge. Environ Monit Assess 187:1–7

    Article  CAS  Google Scholar 

  • Bartkowiak A (2020) The accumulation of selected heavy metals in soils in the vicinity of a busy road. Soil Sci Annu 71(2):118–124

    Article  CAS  Google Scholar 

  • Bashir A, Hoffmann T, Kempf B, Xie X, Smits SH, Bremer E (2014) Plant-derived compatible solutes proline betaine and betonicine confer enhanced osmotic and temperature stress tolerance to Bacillus subtilis. Microbiology 160(10):2283–2294

    Article  CAS  PubMed  Google Scholar 

  • Basumatary B, Bordoloi S, Sarma HP (2012) Crude oil-contaminated soil phytoremediation by using Cyperus brevifolius (Rottb.) Hassk. Water Air Soil Pollut 223(6):3373–3383

    Article  CAS  Google Scholar 

  • Batty LC, Anslow M (2008) Effect of a polycyclic aromatic hydrocarbon on the phytoremediation of zinc by two plant species (Brassica juncea and Festuca arundinacea). Int J Phytoremediation 10(3):236–251

    Article  CAS  Google Scholar 

  • Benáková M, Ahmadi H, Dučaiová Z, Tylová E, Clemens S, Tůma J (2017) Effects of Cd and Zn on physiological and anatomical properties of hydroponically grown Brassica napus plants. Environ Sci Pollut Res 24:20705–20716

    Article  Google Scholar 

  • Bielská L, Kah M, Sigmund G, Hofmann T, Höss S (2017) Bioavailability and toxicity of pyrene in soils upon biochar and compost addition. Sci Total Environ 595:132–140

    Article  PubMed  Google Scholar 

  • Bray HG, Thorpe WV (1954) Analysis of phenolic compounds of interest in metabolism. Methods Biochem Anal 1:27–52

    Article  CAS  PubMed  Google Scholar 

  • Brulle F, Morgan AJ, Cocquerelle C, Vandenbulcke F (2010) Transcriptomic underpinning of toxicant-mediated physiological function alterations in three terrestrial invertebrate taxa: a review. Environ Pollut 158(9):2793–2808

    Article  CAS  PubMed  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Cachada A, da Silva EF, Duarte AC, Pereira R (2016) Risk assessment of urban soils contamination: the particular case of polycyclic aromatic hydrocarbons. Sci Total Environ 551:271–284

    Article  PubMed  Google Scholar 

  • Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157

    Article  PubMed  PubMed Central  Google Scholar 

  • Carrasco-Gil S, Estebaranz-Yubero M, Medel-Cuesta D, Millán R, Hernández LE (2012) Influence of nitrate fertilization on Hg uptake and oxidative stress parameters in alfalfa plants cultivated in a Hg-polluted soil. Environ Exp Bot 75:16–24

    Article  CAS  Google Scholar 

  • Cataldo RJ, Hidalgo LME, Neaman A, Gaete OH (2011) Use of molecular biomarkers in Eisenia foetida to assess copper toxicity in agricultural soils affected by mining activities. J Soil Sci Plant Nutr 11(3):57–70

    Google Scholar 

  • Chandran H, Meena M, Sharma K (2020) Microbial biodiversity and bioremediation assessment through omics approaches. Front Environ Chem 1:570326

    Article  Google Scholar 

  • Chauhan P, Mathur J (2020) Phytoremediation efficiency of Helianthus annuus L. for reclamation of heavy metals-contaminated industrial soil. Environ Sci Pollut Res 27:29954–29966

    Article  CAS  Google Scholar 

  • Chauhan P, Rajguru AB, Dudhe MY, Mathur J (2020) Efficacy of lead (Pb) phytoextraction of five varieties of Helianthus annuus L. from contaminated soil. Environ Technol Innov 18:100718

    Article  Google Scholar 

  • Cheema SA, Khan MI, Tang X, Shen C, Farooq M, Chen Y (2016) Surfactant enhanced pyrene degradation in the rhizosphere of tall fescue (Festuca arundinacea). Environ Sci Pollut Res 23:18129–18136

    Article  CAS  Google Scholar 

  • Chen L, Beiyuan J, Hu W, Zhang Z, Duan C, Cui Q, Fang L (2022) Phytoremediation of potentially toxic elements (PTEs) contaminated soils using alfalfa (Medicago sativa L.): a comprehensive review. Chemosphere 293:133577

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Yu C, Shen C, Zhang C, Liu L, Shen K, Chen Y (2010) Study on adverse impact of e-waste disassembly on surface sediment in East China by chemical analysis and bioassays. J Soil Sediment 10:359–367

    Article  CAS  Google Scholar 

  • Chen X, Li H, Liu X, Zhang X, Liang X, He C, Cao L (2016) Combined remediation of pyrene-contaminated soil with a coupled system of persulfate oxidation and phytoremediation with ryegrass. Environ Sci Pollut Res 23(20):20672–20679

    Article  CAS  Google Scholar 

  • Chigbo C, Batty L (2015) Chelate-assisted phytoremediation of Cu-pyrene-contaminated soil using Z. mays. Water Air Soil Pollut 226:1–10

    Article  CAS  Google Scholar 

  • Chigbo C, Batty L, Bartlett R (2013) Interactions of copper and pyrene on phytoremediation potential of Brassica juncea in copper–pyrene co-contaminated soil. Chemosphere 90(10):2542–2548

    Article  CAS  PubMed  Google Scholar 

  • Chouychai W, Swangying T, Somtrakoon K, Lee H (2018) Growth and phytoremediation efficiency of winged bean in fluorene-and pyrene-contaminated soil. Bull Environ Contam Toxicol 101(5):631–636

    Article  CAS  PubMed  Google Scholar 

  • Dai HP, Shan CJ, Zhao H, Li JC, Jia GL, Jiang H, Wang Q (2015) The difference in antioxidant capacity of four alfalfa cultivars in response to Zn. Ecotoxicol Environ Saf 114:312–317

    Article  CAS  PubMed  Google Scholar 

  • Dai Y, Liu R, Zhou Y, Li N, Hou L, Ma Q, Gao B (2020) Fire Phoenix facilitates phytoremediation of PAH-Cd co-contaminated soil through promotion of beneficial rhizosphere bacterial communities. Environ Int 136:105421

    Article  CAS  PubMed  Google Scholar 

  • De Caroli M, Furini A, DalCorso G, Rojas M, Di Sansebastiano GP (2020) Endomembrane reorganization induced by heavy metals. Plants 9(4):482

    Article  PubMed  PubMed Central  Google Scholar 

  • Decker M, Bause S, Teichmann P, Schneider M, Vonau W (2017) Development of an automatic system for the on-site pH measurement of soil samples. Tech Mess 84(10):659–671

    Article  CAS  Google Scholar 

  • D'Orazio V, Ghanem A, Senesi N (2013) Phytoremediation of pyrene contaminated soils by different plant species. CLEAN Soil Air Water 41(4):377–382

    Article  CAS  Google Scholar 

  • Energy Statistics 2022. Ministry of statistics and programme implementation. Retrieved 7 April 2022.

  • Flogeac K, Guillon E, Aplincourt M (2007) Competitive sorption of metal ions onto a north-eastern France soil. Isotherms and XAFS studies. Geoderma 139(1-2):180–189

    Article  CAS  Google Scholar 

  • Gangwar S, Singh VP, Tripathi DK, Chauhan DK, Prasad SM, Maurya JN (2014) Plant responses to metal stress: the emerging role of plant growth hormones in toxicity alleviation. In: Emerging technologies and management of crop stress tolerance. Academic Press, pp 215–248

    Chapter  Google Scholar 

  • Gao Y, Guo X, Ji H, Li C, Ding H, Briki M, Zhang Y (2016) Potential threat of heavy metals and PAHs in PM2. 5 in different urban functional areas of Beijing. Atmos Res 178:6–16

    Article  Google Scholar 

  • Gao Y, Yu XZ, Wu SC, Cheung KC, Tam NF, Qian PY, Wong MH (2006) Interactions of rice (Oryza sativa L.) and PAH-degrading bacteria (Acinetobacter sp.) on enhanced dissipation of spiked phenanthrene and pyrene in waterlogged soil. Sci Total Environ 372(1):1–11

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Zhou P, Mao L, Zhi YE, Shi WJ (2010) Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD. Environ Earth Sci 60:603–612

    Article  CAS  Google Scholar 

  • Gao Y, Zhu L (2004) Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere 55(9):1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Garba ST, Ahmed I, Akan JC, Dauda BA (2014) Distribution pattern of the heavy metals: Pb, Zn, Cd and Cu in roadside soils of Maiduguri Metropolis, Borno State Nigeria. Int Res J Pure Appl Chem 4(5):486–493

  • Ghori NH, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828

    Article  CAS  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) 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 Science 182:112–120

    Article  CAS  PubMed  Google Scholar 

  • Gou L, Zhuo C, Lu S, Guo Z (2020) A Universal Stress Protein from Medicago falcata (MfUSP1) confers multiple stress tolerance by regulating antioxidant defense and proline accumulation. Environ Exp Bot 178:104168

    Article  CAS  Google Scholar 

  • Gu HX, Hu K, Li DW, Long YT (2016) SERS detection of polycyclic aromatic hydrocarbons using a bare gold nanoparticle coupled film system. Analyst 141(14):4359–4365

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Gong Z, Miao R, Su D, Li X, Jia C, Zhuang J (2017) The influence of root exudates of maize and soybean on polycyclic aromatic hydrocarbons degradation and soil bacterial community structure. Ecol Eng 99:22–30

    Article  Google Scholar 

  • Hajabbasi MA (2016) Importance of soil physical characteristics for petroleum hydrocarbons phytoremediation: a review. Afr J Environ Sci Technol 10(11):394–405

    Article  CAS  Google Scholar 

  • Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 2019:1–25

  • Helaoui S, Boughattas I, Hattab S, Mkhinini M, Alphonse V, Livet A, Banni M (2020) Physiological, biochemical and transcriptomic responses of Medicago sativa to nickel exposure. Chemosphere 249:126121

    Article  CAS  PubMed  Google Scholar 

  • Hossain MS, Rahman GM, Solaiman ARM, Alam MS, Rahman MM, Mia MB (2020) Estimating electrical conductivity for soil salinity monitoring using various soil-water ratios depending on soil texture. Commun Soil Sci Plant Anal 51(5):635–644

    Article  CAS  Google Scholar 

  • Huang X, Jiang Y, Cheng X, Deng L, Liu X (2015) Photosynthetic performance and anti-oxidative response of Cornus controversa seedlings under cadmium and lead stress. Bangladesh J Bot 44(2):215–222

    Article  Google Scholar 

  • Ikram K, Abdelhakim RYH, Topcuoglu B, Badiaa O, Houria T (2020) Accumulation of polyphenols and flavonoids in Atriplex canescens (Pursh) Nutt stressed by heavy metals (zinc, lead and cadmium). Malays J Fundam Appl Sci 16:334–337

    Article  Google Scholar 

  • Jajoo A, Mekala NR, Tomar RS, Grieco M, Tikkanen M, Aro EM (2014) Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not related to their aromaticity. J Photochem Photobiol B 137:151–155

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Weng B, Liu T, Su Y, Liu J, Lu H, Yan C (2017) Response of phenolic metabolism to cadmium and phenanthrene and its influence on pollutant translocations in the mangrove plant Aegiceras corniculatum (L.) Blanco (Ac). Ecotoxicol Environ Saf 141:290–297

    Article  CAS  PubMed  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54(6):262–275

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, fourth edn. CRS Press, Boca Raton, USA, p 505

    Google Scholar 

  • Kang F, Chen D, Gao Y, Zhang Y (2010) Distribution of polycyclic aromatic hydrocarbons in subcellular root tissues of ryegrass (Lolium multiflorum Lam.). BMC Plant Biol 10:1–7

    Article  Google Scholar 

  • Karim SM, Sharif SI, Anik M, Rahman A (2018). Negative impact and probable management policy of E-waste in Bangladesh. arXiv preprint arXiv:1809.10021

  • Kumar S, Prasad S, Yadav KK, Shrivastava M, Gupta N, Nagar S, Malav LC (2019) Hazardous heavy metals contamination of vegetables and food chain: role of sustainable remediation approaches-a review. Environ Res 179:108792

    Article  CAS  PubMed  Google Scholar 

  • Kummerová M, Zezulka Š, Babula P, Váňová L (2013) Root response in Pisum sativum and Zea mays under fluoranthene stress: morphological and anatomical traits. Chemosphere 90(2):665–673

    Article  PubMed  Google Scholar 

  • Lee J, Choi D, Tsang YF, Oh JI, Kwon EE (2017) Employing CO2 as reaction medium for in-situ suppression of the formation of benzene derivatives and polycyclic aromatic hydrocarbons during pyrolysis of simulated municipal solid waste. Environ Pollut 224:476–483

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Kim MS, Kim JG, Kim SO (2020) Use of soil enzymes as indicators for contaminated soil monitoring and sustainable management. Sustainability 12(19):8209

    Article  CAS  Google Scholar 

  • Li L, Zhu P, Wang X, Zhang Z (2020) Phytoremediation effect of Medicago sativa colonized by Piriformospora indica in the phenanthrene and cadmium co-contaminated soil. BMC Biotechnol 20:1–14

    Article  Google Scholar 

  • Liang Q, Chen H, Gong Y, Yang H, Fan M, Kuzyakov Y (2014) Effects of 15 years of manure and mineral fertilizers on enzyme activities in particle-size fractions in a North China Plain soil. Eur J Soil Biol 60:112–119

    Article  CAS  Google Scholar 

  • Lin CC, Chen SJ, Huang KL, Lee WJ, Lin WY, Tsai JH, Chaung HC (2008) PAHs, PAH-induced carcinogenic potency, and particle-extract-induced cytotoxicity of traffic-related nano/ultrafine particles. Environ Sci Technol 42(11):4229–4235

    Article  CAS  PubMed  Google Scholar 

  • Linde A, Inacio A, Alburquerquea C, Freirea M, Moreira J (2008) Biomarkers in an invasive fish species, Oreochromis isniloticus, to assess the effects of pollution in a highly degraded Brazilian River. Sci Total Environ 399(1-3):186–192

    Article  Google Scholar 

  • Liu B, Zhao D, Zhang P, Liu F, Jia M, Liang J (2020) Seedling evaluation of six walnut rootstock species originated in China based on principal component analysis and cluster analysis. Sci Hortic 265:109212

    Article  CAS  Google Scholar 

  • Liu R, Xiao N, Wei S, Zhao L, An J (2014) Rhizosphere effects of PAH-contaminated soil phytoremediation using a special plant named Fire Phoenix. Sci Total Environ 473:350–358

    Article  PubMed  Google Scholar 

  • Lu H, Zhang Y, Liu B, Liu J, Ye J, Yan C (2011) Rhizodegradation gradients of phenanthrene and pyrene in sediment of mangrove (Kandelia candel (L.) Druce). J Hazard Mater 196:263–269

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Teng Y, Wang J, Sun Z (2010) Enhancement of pyrene removed from contaminated soils by Bidens maximowicziana. Chemosphere 81(5):645–650

    Article  CAS  PubMed  Google Scholar 

  • Lyubun Y, Muratova A, Dubrovskaya E, Sungurtseva I, Turkovskaya O (2020) Combined effects of cadmium and oil sludge on sorghum: growth, physiology, and contaminant removal. Environ Sci Pollut Res 27(18):22720–22734

    Article  CAS  Google Scholar 

  • Ma Y, Liu A, Egodawatta P, McGree J, Goonetilleke A (2017) Assessment and management of human health risk from toxic metals and polycyclic aromatic hydrocarbons in urban stormwater arising from anthropogenic activities and traffic congestion. Sci Total Environ 579:202–211

    Article  CAS  PubMed  Google Scholar 

  • Manzano R, Esteban E, Peñalosa JM, Alvarenga P (2014) Amendment application in a multi-contaminated mine soil: effects on soil enzymatic activities and ecotoxicological characteristics. Environ Sci Pollut Res 21:4539–4550

    Article  CAS  Google Scholar 

  • Mathur J, Chauhan P, Srivastava S (2022) Comparative evaluation of cadmium phytoremediation potential of five varieties of Helianthus annuus L. Int J Phytoremediation 25(6):1–12

    Google Scholar 

  • Molina L, Segura A (2021) Biochemical and metabolic plant responses toward polycyclic aromatic hydrocarbons and heavy metals present in atmospheric pollution. Plants 10(11):2305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moosavi SA, Gharineh MH, Afshari RT, Ebrahimi A (2012) Effects of some heavy metals on seed germination characteristics of canola (Barassica napus), wheat (Triticum aestivum) and safflower (Carthamus tinctorious) to evaluate phytoremediation potential of these crops. J Agric Sci 4(9):11–19

    Google Scholar 

  • Moreno B, Nogales R, Macci C, Masciandaro G, Benitez E (2011) Microbial eco-physiological profiles to estimate the biological restoration of a trichloroethylene-contaminated soil. Ecol Indic 11(6):1563–1571

    Article  CAS  Google Scholar 

  • Morillo E, Romero AS, Madrid L, Villaverde J, Maqueda C (2008) Characterization and sources of PAHs and potentially toxic metals in urban environments of Sevilla (Southern Spain). Water Air Soil Pollut 187:41–51

    Article  CAS  Google Scholar 

  • Muradoglu F, Gundogdu M, Ercisli S, Encu T, Balta F, Jaafar HZ, Zia-Ul-Haq M (2015) Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biol Res 48:1–7

    Article  Google Scholar 

  • Muratova A, Lyubun Y, Sungurtseva I, Turkovskaya O, Nurzhanova A (2022) Physiological and biochemical characteristic of Miscanthus× giganteus grown in heavy metal–oil sludge co-contaminated soil. J Environ Sci 115:114–125

    Article  CAS  Google Scholar 

  • Nikaeen M, Nafez AH, Bina B, Nabavi BF, Hassanzadeh A (2015) Respiration and enzymatic activities as indicators of stabilization of sewage sludge composting. Waste Manag 39:104–110

    Article  CAS  PubMed  Google Scholar 

  • Obrycki JF, Basta NT, Wilson RS (2017) Evaluating public and regulatory acceptance for urban soil management approaches. J Environ Qual 46(1):20–26

    Article  CAS  PubMed  Google Scholar 

  • Palmieri F, Estoppey A, House GL, Lohberger A, Bindschedler S, Chain PS, Junier P (2019) Oxalic acid, a molecule at the crossroads of bacterial-fungal interactions. Adv Appl Microbiol 106:49–77

    Article  CAS  PubMed  Google Scholar 

  • Pandey P, Tripathi AK (2011) Effect of heavy metals on morphological and biochemical characteristics of Albizia procera (Roxb.) Benth. seedlings. Int J Environ Sci 1(5):1009–1018

    CAS  Google Scholar 

  • Panwar R, Mathur J (2019) Comparative assessment of physiological and biochemical changes in the selected plant species growing under hydrocarbon stress. Plant Sci Today 6(sp1):560–567

    Article  Google Scholar 

  • Peng C, Muthusamy S, Xia Q, Lal V, Denison MS, Ng JC (2015) Micronucleus formation by single and mixed heavy metals/loids and PAH compounds in HepG2 cells. Mutagenesis 30(5):593–602

    Article  CAS  PubMed  Google Scholar 

  • Peralta-Videa JR, Gardea-Torresdey JL, Gomez E, Tiemann KJ, Parsons JG, Carrillo G (2002) Effect of mixed cadmium, copper, nickel and zinc at different pHs upon alfalfa growth and heavy metal uptake. Environ Pollut 119(3):291–301

    Article  CAS  PubMed  Google Scholar 

  • Qian H, Li J, Sun L, Chen W, Sheng GD, Liu W, Fu Z (2009) Combined effect of copper and cadmium on Chlorella vulgaris growth and photosynthesis-related gene transcription. Aquat Toxicol 94(1):56–61

    Article  CAS  PubMed  Google Scholar 

  • Ratna T, Shakya SR, Sharma A (2022) Energy transitions: trend, drivers, barriers, and policies. In: Handbook of Energy Transitions. CRC Press, pp 21–40

    Chapter  Google Scholar 

  • Reddy MS, Prasanna L, Marmeisse R, Fraissinet-Tachet L (2014) Differential expression of metallothioneins in response to heavy metals and their involvement in metal tolerance in the symbiotic basidiomycete Laccaria bicolor. Microbiology 160(10):2235–2242

    Article  CAS  PubMed  Google Scholar 

  • Saha M, Maharana D, Kurumisawa R, Takada H, Yeo BG, Rodrigues AC, Viet PH (2017) Seasonal trends of atmospheric PAHs in five Asian megacities and source detection using suitable biomarkers. Aerosol Air Qual Res 17(9):2247–2262

    Article  CAS  Google Scholar 

  • Salehi-Lisar SY, Deljoo S (2015) The physiological effect of fluorene on Triticum aestivum, Medicago sativa, and Helianthus annus. Cogent Food Agric 1(1):1020189

    Article  Google Scholar 

  • Santos JA, Nunes LAPL, Melo WJ, Araújo ASF (2011) Tannery sludge compost amendment rates on soil microbial biomass of two different soils. Eur J Soil Biol 47(2):146–151

    Article  Google Scholar 

  • Shahbazy M, Moradi P, Ertaylan G, Zahraei A, Kompany-Zareh M (2020) FTICR mass spectrometry-based multivariate analysis to explore distinctive metabolites and metabolic pathways: a comprehensive bioanalytical strategy toward time-course metabolic profiling of Thymus vulgaris plants responding to drought stress. Plant Sci 290:110257

    Article  CAS  PubMed  Google Scholar 

  • Somtrakoon K, Chouychai W, Lee H (2014) Comparing anthracene and fluorene degradation in anthracene and fluorene-contaminated soil by single and mixed plant cultivation. Int J Phytoremediation 16(4):415–428

    Article  CAS  PubMed  Google Scholar 

  • Somtrakoon K, Chouychai W, Lee H (2015) Removal of anthracene and fluoranthene by waxy corn, long bean and okra in lead-contaminated soil. Bull Environ Contam Toxicol 95(3):407–413

    Article  CAS  PubMed  Google Scholar 

  • Somtrakoon K, Chouychai W, Lee H (2018) Potential of butterfly pea (Clitoria ternatea) and yam bean (Pachyrhizus erosus) plants for phytoremediation of anthracene-and pyrene-contaminated soil. Songklanakarin J Sci Technol 40(3):725–731

  • Song H, Wang YS, Sun CC, Wu ML, Peng YL, Deng C, Li QP (2011) Effects of polycyclic aromatic hydrocarbons exposure on antioxidant system activities and proline content in Kandelia candel. Oceanol Hydrobiol Stud 40(3):9–18

    Article  CAS  Google Scholar 

  • Song X, Li C, Chen W (2022) Phytoremediation potential of Bermuda grass (Cynodon dactylon (L.) pers.) in soils co-contaminated with polycyclic aromatic hydrocarbons and cadmium. Ecotoxicol Environ Saf 234:113389

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Cang L, Zuo Y, Yang J, Zhou D, Duan T, Wang R (2020) EDTA-enhanced electrokinetic remediation of aged electroplating contaminated soil assisted by combining dual cation-exchange membranes and circulation methods. Chemosphere 243:125439

    Article  CAS  PubMed  Google Scholar 

  • Subashchandrabose SR, Megharaj M, Venkateswarlu K, Naidu R (2015) Interaction effects of polycyclic aromatic hydrocarbons and heavy metals on a soil microalga, Chlorococcum sp. MM11. Environ Sci Pollut Res 22(12):8876–8889

    Article  CAS  Google Scholar 

  • Subhashini V, Swamy AVVS (2013) Phytoremediation of zinc contaminated soils by Physalis minima Linn. Int J Innov Res Sci Eng Technol 2:4488–4492

    Google Scholar 

  • Suman J, Uhlik O, Viktorova J, Macek T (2018) Phytoextraction of heavy metals: a promising tool for clean-up of polluted environment. Front Plant Sci 9:1476

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun M, Luo Y, Christie P, Jia Z, Li Z, Teng Y (2012) Methyl-β-cyclodextrin enhanced biodegradation of polycyclic aromatic hydrocarbons and associated microbial activity in contaminated soil. J Environ Sci 24(5):926–933

    Article  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Liu Y, Gu Y, Zeng G, Hu X, Wang X, Sun Z (2015) Biochar amendment to lead-contaminated soil: effects on fluorescein diacetate hydrolytic activity and phytotoxicity to rice. Environ Toxicol Chem 34(9):1962–1968

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Liu Y, Yan K, Wang Z, Lu G, He Y, He W (2017) Differences in the response of soil dehydrogenase activity to Cd contamination are determined by the different substrates used for its determination. Chemosphere 169:324–332

    Article  CAS  PubMed  Google Scholar 

  • Teng Y, Luo Y, Sun M, Liu Z, Li Z, Christie P (2010) Effect of bioaugmentation by Paracoccus sp. strain HPD-2 on the soil microbial community and removal of polycyclic aromatic hydrocarbons from an aged contaminated soil. Bioresour Technol 101(10):3437–3443

    Article  CAS  PubMed  Google Scholar 

  • Tennstedt P, Peisker D, Bottcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149(2):938–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thavamani P, Megharaj M, Naidu R (2012) Multivariate analysis of mixed contaminants (PAHs and heavy metals) at manufactured gas plant site soils. Environ Monit Assess 184:3875–3885

    Article  CAS  PubMed  Google Scholar 

  • Trujillo-González JM, Torres-Mora MA, Keesstra S, Brevik EC, Jiménez-Ballesta R (2016) Heavy metal accumulation related to population density in road dust samples taken from urban sites under different land uses. Sci Total Environ 553:636–642

    Article  PubMed  Google Scholar 

  • Wang J, Zhan X, Zhou L, Lin Y (2010) Biological indicators capable of assessing thermal treatment efficiency of hydrocarbon mixture-contaminated soil. Chemosphere 80(8):837–844

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Zhu Z, Huang H, Li T, He Z, Yang X, Alva A (2012b) Interactive effects of Cd and PAHs on contaminants removal from co-contaminated soil planted with hyperaccumulator plant Sedum alfredii. J Soil Sediment 12:556–564

    Article  CAS  Google Scholar 

  • Wang L, Liu X, Liang M, Tan F, Liang W (2014) Proteomic analysis of salt-responsive proteins in the leaves of Mangrove Kandelia candel during short-term stress. PLoS One 9(1):1–15

    Google Scholar 

  • Wang Y, Tian Z, Zhu H, Cheng Z, Kang M, Luo C, Zhang G (2012a) Polycyclic aromatic hydrocarbons (PAHs) in soils and vegetation near an e-waste recycling site in South China: concentration, distribution, source, and risk assessment. Sci Total Environ 439:187–193

    Article  CAS  PubMed  Google Scholar 

  • Wolińska A, Stępniewska Z (2012) Dehydrogenase activity in the soil environment. Dehydrogenases 10:183–210

    Google Scholar 

  • Xu SY, Chen YX, Wu WX, Wang KX, Lin Q, Liang XQ (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363(1-3):206–215

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Xiao Z, Zhang X, Zhao C, Li Y, Che T, Hu F (2022) The nutrient preferences of rice and wheat influence fluoranthene uptake. Front Environ Sci 10:987743

    Article  Google Scholar 

  • Yang HY, Shi GX, Xu QS, Wang HX (2011) Cadmium effects on mineral nutrition and stress in Potamogeton crispus. Russ J Plant Physiol 58(2):253–260

    Article  CAS  Google Scholar 

  • Yang X, Hu Z, Liu Y, Xie X, Huang L, Zhang R, Dong B (2022) Effect of pyrene-induced changes in root activity on growth of Chinese cabbage (Brassica campestris L.), and the health risks caused by pyrene in Chinese cabbage at different growth stages. Chem Biol Technol Agric 9(1):7

    Article  CAS  Google Scholar 

  • Yang Y, Shen Q (2020) Phytoremediation of cadmium-contaminated wetland soil with Typha latifolia L. and the underlying mechanisms involved in the heavy-metal uptake and removal. Environ Sci Pollut Res 27(5):4905–4916

    Article  MathSciNet  CAS  Google Scholar 

  • Zagoskina NV, Zubova MY, Nechaeva TL, Kazantseva VV, Goncharuk EA, Katanskaya VM, Aksenova MA (2023) Polyphenols in plants: structure, biosynthesis, abiotic stress regulation, and practical applications. Int J Mol Sci 24(18):13874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zehra A, Sahito ZA, Tong W, Tang L, Hamid Y, Khan MB, Yang X (2020) Assessment of sunflower germplasm for phytoremediation of lead-polluted soil and production of seed oil and seed meal for human and animal consumption. J Environ Sci 87:24–38

    Article  CAS  Google Scholar 

  • Zhan X, Liang X, Xu G, Zhou L (2013) Influence of plant root morphology and tissue composition on phenanthrene uptake: stepwise multiple linear regression analysis. Environ Pollut 179:294–300

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Yang L, Zhou Q, Zhang X, Xing W, Wei Y, Tang N (2020) Size distribution of particulate polycyclic aromatic hydrocarbons in fresh combustion smoke and ambient air: a review. J Environ Sci 88:370–384

    Article  CAS  Google Scholar 

  • Zhang X, Chen L, Liu X, Wang C, Chen X, Xu G, Deng K (2014) Synergic degradation of diesel by Scirpus triqueter and its endophytic bacteria. Environ Sci Pollut Res 21:8198–8205

    Article  CAS  Google Scholar 

  • Zhang XF, Xia HP, Li ZA, Zhuang P, Gao B (2011) Identification of a new potential Cd-hyperaccumulator Solanum photeinocarpum by soil seed bank- metal concentration gradient method. J Hazard Mater 189:414–419

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Tao S (2009) Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos Environ 43(4):812–819

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are very thankful to the Vice Chancellor Prof. Ina Aditya Shastri, and Prof. Dipjyoti Chakraborty, Head of the Department of Bioscience and Biotechnology, Banasthali Vidyapith for providing all needed support and for their encouragement. We also acknowledge the Bioinformatics Center, Banasthali Vidyapith which is supported by DBT for providing technical and computational help. We acknowledge DST for providing equipment support of Atomic Absorption Spectrophotometer (AAS) through the FIST and CURIE programs at department of bioscience and biotechnology, Banasthali Vidyapith.

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    Jyoti Mathur & Ritu Panwar

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  1. Jyoti Mathur
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JM did the study conception and design of present research and supervised this work. RP carried out the experiment. Analysis and interpretation of results were carried out by RP. The manuscript was prepared by RP along with the help of JM. All the authors contributed and reviewed the results and approved the final manuscript.

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Correspondence to Jyoti Mathur.

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Mathur, J., Panwar, R. Synergistic effect of pyrene and heavy metals (Zn, Pb, and Cd) on phytoremediation potential of Medicago sativa L. (alfalfa) in multi-contaminated soil. Environ Sci Pollut Res 31, 21012–21027 (2024). https://doi.org/10.1007/s11356-024-32499-4

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