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The combined toxicity and mechanism of multi-walled carbon nanotubes and nano zinc oxide toward the cabbage

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Abstract

The natural environment is a complex system, and there is never only one kind of nanomaterial entering the environment. However, many studies only considered the plant toxicity of one kind of nanomaterial and do not consider the influence of two or more kinds of nanomaterials on plant toxicity. Multi-walled carbon nanotubes (MWCNTs) and zinc oxide nanoparticles (ZnO NPs) are two common and widely used nanomaterials in water environment, so these two kinds of nanomaterials were chosen to explore the effects of their combined toxicity on cabbage. This study investigated the toxicity of MWCNTs combined with ZnO NPs on cabbage by measuring the length of roots and stems, chlorophyll content, oxidative stress, antioxidant enzyme activity, metal element content, and root scanning electron microscopy. The toxicity of single MWCNTs toward cabbage was attributed to direct oxidative damage, while the toxicity of single ZnO NPs toward cabbage was due to the high level of zinc concentration. Moreover, ZnO NPs (10 mg/L) ameliorated MWCNTs toxicity toward cabbage by improving the activity of antioxidant enzymes. ZnO NPs (50 and 100 mg/L) because of the high content of zinc disrupted the balance of other metals in the plant and increased the toxicity of MWCNTs. In conclusion, the combined toxicity of different concentrations and types of nanomaterials should be considered for a more accurate assessment of environmental risks.

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References

  • Abdel-Aziz HMM, Rizwan M (2019) Chemically synthesized silver nanoparticles induced physio-chemical and chloroplast ultrastructural changes in broad bean seedlings. Chemosphere 235:1066–1072

    Article  Google Scholar 

  • Adrees M, Khan ZS, Hafeez M, Rizwan M, Hussain K, Asrar M, Alyemeni MN, Wijaya L, Ali S (2021) Foliar exposure of zinc oxide nanoparticles improved the growth of wheat (Triticum aestivum L.) and decreased cadmium concentration in grains under simultaneous Cd and water deficient stress. Ecotoxicol Environ Saf 208:111627

    Article  Google Scholar 

  • Ali S, Rizwan M, Noureen S, Anwar S, Ali B, Naveed M, Abd Allah EF, Alqarawi AA, Ahmad P (2019) Combined use of biochar and zinc oxide nanoparticle foliar spray improved the plant growth and decreased the cadmium accumulation in rice (Oryza sativa L.) plant. Environ Sci Pollut Res Int 26(11):11288–11299

    Article  Google Scholar 

  • Balazova L, Babula P, Balaz M, Backorova M, Bujnakova Z, Briancin J, Kurmanbayeva A, Sagi M (2018) Zinc oxide nanoparticles phytotoxicity on halophyte from genus Salicornia. Plant Physiol Biochem 130:30–42

    Article  Google Scholar 

  • Balazova L, Balaz M, Babula P (2020) Zinc oxide nanoparticles damage tobacco BY-2 cells by oxidative stress followed by processes of autophagy and programmed cell death. Nanomaterials (Basel) 10(6):1066

    Article  Google Scholar 

  • Bashir A, Rizwan M, Ali S, Adrees M, Rehman MZU, Qayyum MF (2020) Effect of composted organic amendments and zinc oxide nanoparticles on growth and cadmium accumulation by wheat; a life cycle study. Environ Sci Pollut Res Int 27(19):23926–23936

    Article  Google Scholar 

  • Bashir A, ur Rehman MZ, Hussaini KM, Adrees M, Qayyum MF, Sayal AU, Rizwan M, Ali S, Alsahli AA, Alyemeni MN (2021) Combined use of zinc nanoparticles and co-composted biochar enhanced wheat growth and decreased Cd concentration in grains under Cd and drought stress: A field study. Environ Technol Innov 23:101518

    Article  Google Scholar 

  • Cabral Gouveia GC, Galindo FS, Dantas Bereta Lanza MG, Caroline da Rocha Silva A, Pereira de Brito Mateus M, Souza da Silva M, Rimoldi Tavanti RF, Tavanti TR, Lavres J, Reis ARD (2020) Selenium toxicity stress-induced phenotypical, biochemical and physiological responses in rice plants: characterization of symptoms and plant metabolic adjustment. Ecotoxicol Environ Saf 202:110916

    Article  Google Scholar 

  • Cao W, Gong J, Zeng G, Song B, Zhang P, Li J, Fang S, Qin L, Ye J, Cai Z (2020a) Mutual effects of silver nanoparticles and antimony(iii)/(v) co-exposed to Glycine max (L.) Merr. in hydroponic systems: uptake, translocation, physiochemical responses, and potential mechanisms. Environ Sci Nano 7(9):2691–2707

    Article  Google Scholar 

  • Cao W, Gong J, Zeng G, Song B, Zhang P, Li J, Fang S, Tang S, Qin L, Ye J, Cai Z (2020b) Abiotic mediation of common ions on the co-exposure of CeO2 NPs with Sb (III) or Sb (V) to Glycine max (Linn.) Merrill. (Soybean): impacts on uptake, accumulation and physiochemical characters. Environ Pollut 267:115594

    Article  Google Scholar 

  • Cao W, Gong J, Zeng G, Song B, Zhang P, Li J, Fang S, Tang S, Ye J, Cai Z (2020c) Potential interactions between three common metal oxide nanoparticles and antimony(III/V) involving their uptake, distribution, and phytotoxicity to soybean. ACS Sustain Chem Eng 8(27):10125–10141

    Article  Google Scholar 

  • Chang X, Song Z, Xu Y, Gao M (2020) Effects of carbon nanotubes on growth of wheat seedlings and Cd uptake. Chemosphere 240:124931

    Article  Google Scholar 

  • Chang Y-N, Ou X-M, Zeng G-M, Gong J-L, Deng C-H, Jiang Y, Liang J, Yuan G-Q, Liu H-Y, He X (2015) Synthesis of magnetic graphene oxide–TiO2 and their antibacterial properties under solar irradiation. Appl Surf Sci 343:1–10

    Article  Google Scholar 

  • Deng C-H, Gong J-L, Zeng G-M, Jiang Y, Zhang C, Liu H-Y, Huan S-Y (2016) Graphene–CdS nanocomposite inactivation performance toward Escherichia coli in the presence of humic acid under visible light irradiation. Chem Eng J 284:41–53

    Article  Google Scholar 

  • Estrela FN, Batista Guimaraes AT, Silva FG, Marinho da Luz T, Silva AM, Pereira PS, Malafaia G (2021) Effects of polystyrene nanoplastics on Ctenopharyngodon idella (grass carp) after individual and combined exposure with zinc oxide nanoparticles. J Hazard Mater 403:123879

    Article  Google Scholar 

  • Falco WF, Scherer MD, Oliveira SL, Wender H, Colbeck I, Lawson T, Caires ARL (2020) Phytotoxicity of silver nanoparticles on Vicia faba: evaluation of particle size effects on photosynthetic performance and leaf gas exchange. Sci Total Environ 701:134816

    Article  Google Scholar 

  • Freixa A, Acuna V, Sanchis J, Farre M, Barcelo D, Sabater S (2018) Ecotoxicological effects of carbon based nanomaterials in aquatic organisms. Sci Total Environ 619-620:328–337

    Article  Google Scholar 

  • Gao M, Yujuan Y, Song Z (2019) Toxicity of cadmium to wheat seedling roots in the presence of graphene oxide. Chemosphere 233:9–16

    Article  Google Scholar 

  • Gong J-L, Zhang Y-L, Jiang Y, Zeng G-M, Cui Z-H, Liu K, Deng C-H, Niu Q-Y, Deng J-H, Huan S-Y (2015) Continuous adsorption of Pb(II) and methylene blue by engineered graphite oxide coated sand in fixed-bed column. Appl Surf Sci 330:148–157

    Article  Google Scholar 

  • Gong X, Huang D, Liu Y, Zeng G, Wang R, Wan J, Zhang C, Cheng M, Qin X, Xue W (2017) Stabilized nanoscale zerovalent iron mediated cadmium accumulation and oxidative damage of Boehmeria nivea (L.) Gaudich cultivated in cadmium contaminated sediments. Environ Sci Technol 51(19):11308–11316

    Article  Google Scholar 

  • Gong X, Liu Y, Huang D, Zeng G, Liu S, Tang H, Zhou L, Hu X, Zhou Y, Tan X (2016) Effects of exogenous calcium and spermidine on cadmium stress moderation and metal accumulation in Boehmeria nivea (L.) Gaudich. Environ Sci Pollut Res Int 23(9):8699–8708

    Article  Google Scholar 

  • Haghighat F, Kim Y, Sourinejad I, Yu IJ, Johari SA (2021) Titanium dioxide nanoparticles affect the toxicity of silver nanoparticles in common carp (Cyprinus carpio). Chemosphere 262:127805

    Article  Google Scholar 

  • Hao Y, Xu B, Ma C, Shang J, Gu W, Li W, Hou T, Xiang Y, Cao W, Xing B, Rui Y (2019) Synthesis of novel mesoporous carbon nanoparticles and their phytotoxicity to rice (Oryza sativa L.). J Saudi Chem Soc 23(1):75–82

    Article  Google Scholar 

  • Hao Y, Yu F, Lv R, Ma C, Zhang Z, Rui Y, Liu L, Cao W, Xing B (2016) Carbon nanotubes filled with different ferromagnetic alloys affect the growth and development of rice seedlings by changing the C:N ratio and plant hormones concentrations. PLoS One 11(6):e0157264

    Article  Google Scholar 

  • Hayes KL, Mui J, Song B, Sani ES, Eisenman SW, Sheffield JB, Kim B (2020) Effects, uptake, and translocation of aluminum oxide nanoparticles in lettuce: a comparison study to phytotoxic aluminum ions. Sci Total Environ 719:137393

    Article  Google Scholar 

  • Huang B, Wei ZB, Yang LY, Pan K, Miao AJ (2019) Combined toxicity of silver nanoparticles with hematite or plastic nanoparticles toward two freshwater algae. Environ Sci Technol 53(7):3871–3879

    Article  Google Scholar 

  • Hussain A, Ali S, Rizwan M, Zia Ur Rehman M, Javed MR, Imran M, Chatha SAS, Nazir R (2018) Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environ Pollut 242(Pt B):1518–1526

    Article  Google Scholar 

  • Jahani S, Saadatmand S, Mahmoodzadeh H, Khavari-Nejad RA (2019) Effect of foliar application of cerium oxide nanoparticles on growth, photosynthetic pigments, electrolyte leakage, compatible osmolytes and antioxidant enzymes activities of Calendula officinalis L. Biologia 74(9):1063–1075

    Article  Google Scholar 

  • Jain N, Bhargava A, Pareek V, Sayeed Akhtar M, Panwar J (2017) Does seed size and surface anatomy play role in combating phytotoxicity of nanoparticles? Ecotoxicology 26(2):238–249

    Article  Google Scholar 

  • Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. Methods Mol Biol 639:292–298

    Google Scholar 

  • Jordan JT, Oates RP, Subbiah S, Payton PR, Singh KP, Shah SA, Green MJ, Klein DM, Canas-Carrell JE (2020) Carbon nanotubes affect early growth, flowering time and phytohormones in tomato. Chemosphere 256:127042

    Article  Google Scholar 

  • Keller AA, Lazareva A (2013) Predicted releases of engineered nanomaterials: from global to regional to local. Environ Sci Technol Lett 1(1):65–70

    Article  Google Scholar 

  • Klaine SJ, Alvarez PJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environ Toxicol Chem 7(9):1825–1851

    Article  Google Scholar 

  • Khan ZS, Rizwan M, Hafeez M, Ali S, Javed MR, Adrees M (2019) The accumulation of cadmium in wheat (Triticum aestivum) as influenced by zinc oxide nanoparticles and soil moisture conditions. Environ Sci Pollut Res Int 26(19):19859–19870

    Article  Google Scholar 

  • Li WQ, Qing T, Li CC, Li F, Ge F, Fei JJ, Peijnenburg W (2020) Integration of subcellular partitioning and chemical forms to understand silver nanoparticles toxicity to lettuce (Lactuca sativa L.) under different exposure pathways. Chemosphere 258:127349

    Article  Google Scholar 

  • Lian J, Wu J, Xiong H, Zeb A, Yang T, Su X, Su L, Liu W (2020a) Impact of polystyrene nanoplastics (PSNPs) on seed germination and seedling growth of wheat (Triticum aestivum L.). J Hazard Mater 385:121620

    Article  Google Scholar 

  • Lian J, Wu J, Zeb A, Zheng S, Ma T, Peng F, Tang J, Liu W (2020b) Do polystyrene nanoplastics affect the toxicity of cadmium to wheat (Triticum aestivum L.)? Environ Pollut 263:114498

    Article  Google Scholar 

  • Movafeghi A, Khataee A, Abedi M, Tarrahi R, Dadpour M, Vafaei F (2018) Effects of TiO2 nanoparticles on the aquatic plant Spirodela polyrrhiza: evaluation of growth parameters, pigment contents and antioxidant enzyme activities. J Environ Sci (China) 64:130–138

    Article  Google Scholar 

  • Nair PM, Chung IM (2015) Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.). Ecotoxicol Environ Saf 113:302–313

    Article  Google Scholar 

  • Pradas Del Real AE, Vidal V, Carriere M, Castillo-Michel H, Levard C, Chaurand P, Sarret G (2017) Silver nanoparticles and wheat roots: a complex interplay. Environ Sci Technol 51(10):5774–5782

    Article  Google Scholar 

  • Rippner DA, Green PG, Young TM, Parikh SJ (2018) Dissolved organic matter reduces CuO nanoparticle toxicity to duckweed in simulated natural systems. Environ Pollut 234:692–698

    Article  Google Scholar 

  • Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Zia Ur Rehman M, Waris AA (2019a) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277

    Article  Google Scholar 

  • Rizwan M, Ali S, Zia Ur Rehman M, Adrees M, Arshad M, Qayyum MF, Ali L, Hussain A, Chatha SAS, Imran M (2019b) Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil. Environ Pollut 248:358–367

    Article  Google Scholar 

  • Rui M, Ma C, Hao Y, Guo J, Rui Y, Tang X, Zhao Q, Fan X, Zhang Z, Hou T, Zhu S (2016) Iron oxide nanoparticles as a potential iron fertilizer for peanut (Arachis hypogaea). Front Plant Sci 7:815

    Article  Google Scholar 

  • Schmitt OJ, Brunetto G, Chassot T, Tiecher TL, Marchezan C, Tarouco CP, De Conti L, Lourenzi CR, Nicoloso FT, Kreutz MA, Andriolo JL (2020) Impact of Cu concentrations in nutrient solution on growth and physiological and biochemical parameters of beet and cabbage and human health risk assessment. Sci Hortic 272:109558

    Article  Google Scholar 

  • Scown TM, van Aerle R, Tyler CR (2010) Review: Do engineered nanoparticles pose a significant threat to the aquatic environment? Crit Rev Toxicol 40(7):653–670

    Article  Google Scholar 

  • Shah AA, Aslam S, Akbar M, Ahmad A, Khan WU, Yasin NA, Ali B, Rizwan M, Ali S (2021) Combined effect of Bacillus fortis IAGS 223 and zinc oxide nanoparticles to alleviate cadmium phytotoxicity in Cucumis melo. Plant Physiol Biochem 158:1–12

    Article  Google Scholar 

  • Sharifan H, Moore J, Ma X (2020) Zinc oxide (ZnO) nanoparticles elevated iron and copper contents and mitigated the bioavailability of lead and cadmium in different leafy greens. Ecotoxicol Environ Saf 191:110177

    Article  Google Scholar 

  • Sharma VK, Filip J, Zboril R, Varma RS (2015) Natural inorganic nanoparticles – formation, fate, and toxicity in the environment. Chem Soc Rev 44(23):8410–8423

    Article  Google Scholar 

  • Soares C, Branco-Neves S, de Sousa A, Teixeira J, Pereira R, Fidalgo F (2018) Can nano-SiO2 reduce the phytotoxicity of acetaminophen? - A physiological, biochemical and molecular approach. Environ Pollut 241:900–911

    Article  Google Scholar 

  • Song B, Chen M, Ye S, Xu P, Zeng G, Gong J, Li J, Zhang P, Cao W (2019) Effects of multi-walled carbon nanotubes on metabolic function of the microbial community in riverine sediment contaminated with phenanthrene. Carbon 144:1–7

    Article  Google Scholar 

  • Sun Y, Jing R, Zheng F, Zhang S, Jiao W, Wang F (2019) Evaluating phytotoxicity of bare and starch-stabilized zero-valent iron nanoparticles in mung bean. Chemosphere 236:124336

    Article  Google Scholar 

  • Sun Y, Wang C, Xu X, Ruan H (2020a) Responses of plants to polybrominated diphenyl ethers (PBDEs) induced phytotoxicity: a hierarchical meta-analysis. Chemosphere 240:124865

    Article  Google Scholar 

  • Sun Y, Wang W, Zheng F, Zhang S, Wang F, Liu S (2020b) Phytotoxicity of iron-based materials in mung bean: Seed germination tests. Chemosphere 251:126432

    Article  Google Scholar 

  • Wang F, Adams CA, Shi Z, Sun Y (2018) Combined effects of ZnO NPs and Cd on sweet sorghum as influenced by an arbuscular mycorrhizal fungus. Chemosphere 209:421–429

    Article  Google Scholar 

  • Wang J, Zhang X, Chen Y, Sommerfeld M, Hu Q (2008) Toxicity assessment of manufactured nanomaterials using the unicellular green alga Chlamydomonas reinhardtii. Chemosphere 73(7):1121–1128

    Article  Google Scholar 

  • Wang W, Ren Y, He J, Zhang L, Wang X, Cui Z (2020) Impact of copper oxide nanoparticles on the germination, seedling growth, and physiological responses in Brassica pekinensis L. Environ Sci Pollut Res Int 27(25):31505–31515

    Article  Google Scholar 

  • Xin JP, Ma S, Zhao C, Li Y, Tian RN (2020) Cadmium phytotoxicity, related physiological changes in Pontederia cordata: antioxidative, osmoregulatory substances, phytochelatins, photosynthesis, and chlorophyll fluorescence. Environ Sci Pollut Res Int 27(33):41596–41608

    Article  Google Scholar 

  • Yang Z, Xiao Y, Jiao T, Zhang Y, Chen J, Gao Y (2020) Effects of copper oxide nanoparticles on the growth of rice (Oryza sativa L.) seedlings and the relevant physiological responses. Int J Environ Res Public Health 17(4):1260

    Article  Google Scholar 

  • Ye N, Wang Z, Fang H, Wang S, Zhang F (2017) Combined ecotoxicity of binary zinc oxide and copper oxide nanoparticles to Scenedesmus obliquus. J Environ Sci Health A Tox Hazard Subst Environ Eng 52(6):555–560

    Article  Google Scholar 

  • Youssef MS, Elamawi RM (2020) Evaluation of phytotoxicity, cytotoxicity, and genotoxicity of ZnO nanoparticles in Vicia faba. Environ Sci Pollut Res Int 27(16):18972–18984

    Article  Google Scholar 

  • Zhang CL, Jiang HS, Gu SP, Zhou XH, Lu ZW, Kang XH, Yin L, Huang J (2019a) Combination analysis of the physiology and transcriptome provides insights into the mechanism of silver nanoparticles phytotoxicity. Environ Pollut 252(Pt B):1539–1549

    Article  Google Scholar 

  • Zhang W, Long J, Li J, Zhang M, Xiao G, Ye X, Chang W, Zeng H (2019b) Impact of ZnO nanoparticles on Cd toxicity and bioaccumulation in rice (Oryza sativa L.). Environ Sci Pollut Res Int 26(22):23119–23128

    Article  Google Scholar 

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Acknowledgements

The authors are grateful for the financial supports from National Natural Science Foundation of China (51521006, 51579095, 51378190), Ecology and Environment Department of Hunan, the Program for Changjiang Scholars and Innovative Research Team in University (IRT-13R17).

Funding

This study was financially supported by the National Natural Science Foundation of China (51521006, 51579095, 51378190), Ecology and Environment Department of Hunan, the Program for Changjiang Scholars and Innovative Research Team in University (IRT-13R17).

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MH: data curation, methodology, and writing—original draft preparation

J-LG: conceptualization, writing—review and editing

W-CC: conceptualization and supervision

RF: supervision

ZC: resources

JY: software and resources

Z-PC: formal analysis

W-WT: resources

All authors read and approved the final manuscript.

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Correspondence to Ji-Lai Gong or Wang-Wang Tang.

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Hong, ., Gong, JL., Cao, WC. et al. The combined toxicity and mechanism of multi-walled carbon nanotubes and nano zinc oxide toward the cabbage. Environ Sci Pollut Res 29, 3540–3554 (2022). https://doi.org/10.1007/s11356-021-15857-4

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