Abstract
The present article aims to assess the phytotoxic effects of copper and zinc oxide nanoparticles (Cu NPs, ZnO NPs) on mung bean (Vigna radiata L.) and their possible risk on food quality and safety. We also study the molecular mechanisms underlying the toxicity of nanosized Cu and ZnO. Seeds of mung bean were germinated under increasing concentrations of Cu NPs and ZnO NPs (10, 100, 1000, 2000 mg/L). We analyzed levels of free amino acids, total soluble sugars, minerals, polyphenols and antioxidant capacity. Our results showed that depending on the concentrations used of Cu NPs and ZnO NPs, the physiology of seed germination and embryo growth were modified. Both free metal ions and nanoparticles themselves may impact plant cellular and physiological processes. At 10 mg/L, an improvement of the nutritive properties, in terms of content in free amino acids, total soluble sugars, essential minerals, antioxidant polyphenols and flavonoids, was shown. However, higher concentrations (100–2000 mg/L) caused an alteration in the nutritional balance, which was revealed by the decrease in contents and quality of phenolic compounds, macronutrients (Na, Mg, Ca) and micronutrients (Cu, Fe, Mn, Zn, K). The overall effects of Cu and ZnO nanoparticles seem to interfere with the bioavailability of mineral and organic nutrients and alter the beneficial properties of the antioxidant phytochemicals, mineral compounds, phenolic acids and flavonoids. This may result in a potential hazard to human food and health, at some critical doses of nanofertilizers. This study may contribute in the guidelines to the safe use of nanofertilizers or nanosafety, for more health benefit and less potential risks.
Similar content being viewed by others
References
Aebi, H. (1984). [13] Catalase in Vitro. Methods in Enzymology, 105(C), 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Afrayeem, S., & Chaurasia, A. (2017). Effect of zinc oxide nanoparticles on seed germination and seed vigour in chilli (Capsicum annuum L.). undefined.
Ajouri, A., Asgedom, H., & Becker, M. (2004). Seed priming enhances germination and seedling growth of barley under conditions of P and Zn deficiency. Journal of Plant Nutrition and Soil Science, 167(5), 630–636. https://doi.org/10.1002/jpln.200420425
Arfaoui, H., Karmous, I., Mahjoubi, Y., Kharbech, O., Tlahig, S., Loumerem, M., & Chaoui, A. (2021). Screening of the effects of Zinc oxide based nanofertilizers on the germination of Lathyrus sativa L. seeds. Journal of Applied Botany and Food Quality, 94, 53–60. https://doi.org/10.5073/JABFQ.2021.094.007
Ashe, B. (2011). A detail investigation to observe the effect of zinc oxide and Silver nanoparticles in biological system. Thesis. Master of Technology (Research). Biotechnology and Medical Engineering., p85, Roll NO- 607bm004.
Bagawade, J. A., & Jagtap, S. S. (2018). Effect of zinc oxide nanoparticles on Germination and Growth Characteristics in Wheat Plants (Triticum aestivum L.). International Journal of Advance Engineering and Research Development, 5(04), e-ISSN: 2348 - 4470, print-ISSN: 2348-6406.
Bashir, A., Rizwan, M., Ali, S., Zia ur Rehman, M., Ishaque, W., Atif Riaz, M., & Maqbool, A. (2018). Effect of foliar-applied iron complexed with lysine on growth and cadmium (Cd) uptake in rice under Cd stress. Environmental Science and Pollution Research, 25(21), 20691–20699. https://doi.org/10.1007/s11356-018-2042-y
Behlau, F., Belasque, J., Graham, J. H., & Leite, R. P. (2010). Effect of frequency of copper applications on control of citrus canker and the yield of young bearing sweet orange trees. Crop Protection, 29(3), 300–305. https://doi.org/10.1016/j.cropro.2009.12.010
Bindraban, P. S., Dimkpa, C. O., White, J. C., Franklin, F. A., Melse-Boonstra, A., Koele, N., et al. (2020). Safeguarding human and planetary health demands a fertilizer sector transformation. Plants, People, Planet, 2(4), 302–309. https://doi.org/10.1002/ppp3.10098
Bradfield, S. J., Kumar, P., White, J. C., & Ebbs, S. D. (2017). Zinc, copper, or cerium accumulation from metal oxide nanoparticles or ions in sweet potato: Yield effects and projected dietary intake from consumption. Plant Physiology and Biochemistry, 110, 128–137. https://doi.org/10.1016/j.plaphy.2016.04.008
Buzea, C., Pacheco, I. I., & Robbie, K. (2007). Nanomaterials and nanoparticles: Sources and toxicity. Biointerphases, 2(4), MR17–MR71. https://doi.org/10.1116/1.2815690
Chen, C., Wang, C., Liu, Z., Liu, X., Zou, L., Shi, J., et al. (2018). Variations in physiology and multiple bioactive constituents under salt stress provide insight into the quality evaluation of apocyni veneti folium. International Journal of Molecular Sciences, 19(10), 3042. https://doi.org/10.3390/ijms19103042
Chitra, U., Vimala, V., Singh, U., & Geervani, P. (1995). Variability in phytic acid content and protein digestibility of grain legumes. Plant Foods for Human Nutrition, 47(2), 163–172. https://doi.org/10.1007/BF01089266
Da Costa, M. V. J., & Sharma, P. K. (2016). Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica, 54(1), 110–119. https://doi.org/10.1007/s11099-015-0167-5.
Dahiya, P. K., Linnemann, A. R., Van Boekel, M. A. J. S., Khetarpaul, N., Grewal, R. B., & Nout, M. J. R. (2015). Mung bean: Technological and nutritional potential. Critical Reviews in Food Science and Nutrition, 55(5), 670–688. https://doi.org/10.1080/10408398.2012.671202
Das, B., Khan, M. I., Jayabalan, R., Behera, S. K., Yun, S. I., Tripathy, S. K., & Mishra, A. (2016). Understanding the antifungal mechanism of Ag@ZnO core-shell nanocomposites against Candida krusei. Scientific Reports, 6(1), 1–12. https://doi.org/10.1038/srep36403
de la Rosa, G., López-Moreno, M. L., de Haro, D., Botez, C. E., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2013). Effects of ZnO nanoparticles in alfalfa, tomato, and cucumber at the germination stage: Root development and X-ray absorption spectroscopy studies. Pure and Applied Chemistry, 85(12), 2161–2174. https://doi.org/10.1351/PAC-CON-12-09-05
Dimkpa, C. O., Andrews, J., Sanabria, J., Bindraban, P. S., Singh, U., Elmer, W. H., et al. (2020). Interactive effects of drought, organic fertilizer, and zinc oxide nanoscale and bulk particles on wheat performance and grain nutrient accumulation. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2020.137808
Dimkpa, C. O., Latta, D. E., McLean, J. E., Britt, D. W., Boyanov, M. I., & Anderson, A. J. (2013). Fate of CuO and ZnO nano- and microparticles in the plant environment. Environmental Science and Technology, 47(9), 4734–4742. https://doi.org/10.1021/es304736y
Dimkpa, C., Singh, U., Adisa, I., Bindraban, P., Elmer, W., Gardea-Torresdey, J., & Whit e, J. (2018). Effects of manganese nanoparticle exposure on nutrient acquisition in wheat (Triticum aestivum L.). Agronomy, 8(9), 158. https://doi.org/10.3390/agronomy8090158
Effect of Nanoparticles on Wheat Seed Germination and Seedling Growth. (n.d.). https://publications.waset.org/10008498/effect-of-nanoparticles-on-wheat-seed-germination-and-seedling-growth. Accessed from 14 Dec 2020.
Elmer, W. H., & White, J. C. (2016). The use of metallic oxide nanoparticles to enhance growth of tomatoes and eggplants in disease infested soil or soilless medium. Environmental Science: Nano, 3(5), 1072–1079. https://doi.org/10.1039/c6en00146g
Elmer, W., & White, J. C. (2018). The future of nanotechnology in plant pathology. Annual Review of Phytopathology. https://doi.org/10.1146/annurev-phyto-080417-050108
Fielding, J. L., & Hall, J. L. (1978). A biolchemical and cytochemical study of peroxidase activity in roots of Pisum sativum: I. A comparison of dab-peroxidase and guaiacol-peroxidase with particular emphasis on the properties of cell wall activity. Journal of Experimental Botany, 29(4), 969–981. https://doi.org/10.1093/jxb/29.4.969
Fujiki, H., Sueoka, E., Watanabe, T., & Suganuma, M. (2015). Primary cancer prevention by green tea, and tertiary cancer prevention by the combination of green tea catechins and anticancer compounds. Journal of Cancer Prevention, 20(1), 1–4. https://doi.org/10.15430/jcp.2015.20.1.1
Hafizi, Z., & Nasr, N. (2018). the effect of zinc oxide nanoparticles on safflower plant growth and physiology. Engineering, Technology & Applied Science Research, 8(1), 2508–3251. https://doi.org/10.48084/etasr.1571
Haigney, M. C., Zareba, W., Gentlesk, P. J., Goldstein, R. E., Illovsky, M., McNitt, S., et al. (2004). QT interval variability and spontaneous ventricular tachycardia or fibrillation in the Multicenter Automatic Defibrillator Implantation Trial (MADIT) II patients. Journal of the American College of Cardiology, 44(7), 1481–1487. https://doi.org/10.1016/j.jacc.2004.06.063
Heuzé, V., Tran, G., & Bastianelli, D. (2012). Mung bean (Vigna radiata) | Feedipedia Datasheet citation. http://www.feedipedia.org/node/235 [08/12/201618:02:20]. Accessed from 23 May 2021.
Jakobek, L. (2015). Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chemistry. https://doi.org/10.1016/j.foodchem.2014.12.013
Jiang, H., Wang, J., Rogers, J., & Xie, J. (2017). Brain Iron Metabolism Dysfunction in Parkinson’s Disease. Molecular Neurobiology. https://doi.org/10.1007/s12035-016-9879-1
Khurana, S., Venkataraman, K., Hollingsworth, A., Piche, M., & Tai, T. (2013). Polyphenols: Benefits to the cardiovascular system in health and in aging. Nutrients, 5(10), 3779–3827. https://doi.org/10.3390/nu5103779
Konate, A., He, X., Zhang, Z., Ma, Y., Zhang, P., Alugongo, G., & Rui, Y. (2017). Magnetic (Fe3O4) nanoparticles reduce heavy metals uptake and mitigate their toxicity in wheat seedling. Sustainability, 9(5), 790. https://doi.org/10.3390/su9050790
Laila, O., & Murtaza, I. (2014). Seed sproutıng: A way to health promotıng treasure. International Journal of Current Research and Review, 6(23), 75–79.
Lawre, S., Raskar, S. V., & Laware, S. L. (2014). Effect of zinc oxide nanoparticles on cytology and seed germination in onion. International Journal of Current Microbiology Applied Science, 3(2), 467–473.
Lee, C. W., Mahendra, S., Zodrow, K., Li, D., Tsai, Y. C., Braam, J., & Alvarez, P. J. J. (2010). Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environmental Toxicology and Chemistry, 29(3), 669–675. https://doi.org/10.1002/etc.58
McCready, R. M., Guggolz, J., Silviera, V., & Owens, H. S. (1950). Determination of starch and amylose in vegetables. Analytical Chemistry, 22(9), 1156–1158. https://doi.org/10.1021/ac60045a016
Meydani, M., & Hasan, S. T. (2010). Dietary polyphenols and obesity. Nutrients, 2(7), 737–751. https://doi.org/10.3390/nu2070737
Minh, L. T., Khang, D. T., Thu Ha, P. T., Tuyen, P. T., Minh, T. N., Quan, N. V., & Xuan, T. D. (2016). Effects of salinity stress on growth and phenolics of rice (Oryza sativa L.). International Letters of Natural Sciences, 57, 1–10. https://doi.org/10.18052/www.scipress.com/ilns.57.1
Moore, S., & Stein, W. H. (1954). Procedures for the chromatographic determination of amino acids on four per cent cross-linked sulfonated polystyrene resins. Journal of Biological Chemistry, 211, 893–906.
Munir, T., Rizwan, M., Kashif, M., Shahzad, A., Ali, S., Amin, N., et al. (2018). Effect of zinc oxide nanoparticles on the growth and Zn uptake in wheat (Triticum aestivum L.) by seed priming method. Digest Journal of Nanomaterials and Biostructures, 13(1), 315–323.
Nair, P. M. G., & Chung, I. M. (2014). Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion, and molecular level changes. Environmental Science and Pollution Research, 21(22), 12709–12722. https://doi.org/10.1007/s11356-014-3210-3
Nair, P. M. G., & Chung, I. M. (2015). Study on the correlation between copper oxide nanoparticles induced growth suppression and enhanced lignification in Indian mustard (Brassica juncea L.). Ecotoxicology and Environmental Safety, 113, 302–313. https://doi.org/10.1016/j.ecoenv.2014.12.013
Nair, P. M. G., & Chung, I. M. (2017). Regulation of morphological, molecular and nutrient status in Arabidopsis thaliana seedlings in response to ZnO nanoparticles and Zn ion exposure. Science of the Total Environment, 575, 187–198. https://doi.org/10.1016/j.scitotenv.2016.10.017
Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nunes, I., Jacquiod, S., Brejnrod, A., Holm, P. E., Johansen, A., Brandt, K. K., et al. (2016). Coping with copper: legacy effect of copper on potential activity of soil bacteria following a century of exposure. FEMS Microbiology Ecology, 92(11), fiw175. https://doi.org/10.1093/femsec/fiw175
Paliyath, G., Bakovic, M., & Shetty, K. (2011). Functional foods, nutraceuticals, and degenerative disease prevention. Functional Foods, Nutraceuticals, and Degenerative Disease Prevention. https://doi.org/10.1002/9780470960844
Pandey, K. B., & Rizvi, S. I. (2009). Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Medicine and Cellular Longevity, 2(5), 270–278. https://doi.org/10.4161/oxim.2.5.9498
Rajput, V. D., Minkina, T. M., Behal, A., Sushkova, S. N., Mandzhieva, S., Singh, R., et al. (2018a). Effects of zinc-oxide nanoparticles on soil, plants, animals and soil organisms: A review. Environmental Nanotechnology, Monitoring and Management. https://doi.org/10.1016/j.enmm.2017.12.006
Raliya, R., Nair, R., Chavalmane, S., Wang, W. N., & Biswas, P. (2015). Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics, 7(12), 1584–1594. https://doi.org/10.1039/c5mt00168d
Rawat, M., Yadukrishnan, P., & Kumar, N. (2018). Mechanisms of action of nanoparticles in living systems. Microbial Biotechnology in Environmental Monitoring and Cleanup, 221–236. https://doi.org/10.4018/978-1-5225-3126-5.ch014.
Rizwan, M., Ali, S., Ali, B., Adrees, M., Arshad, M., Hussain, A., et al. (2019). Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere, 214, 269–277. https://doi.org/10.1016/j.chemosphere.2018.09.120
Romeo, S., Trupiano, D., Ariani, A., Renzone, G., Scippa, G. S., Scaloni, A., & Sebastiani, L. (2014). Proteomic analysis of Populus×euramericana (clone I-214) roots to identify key factors involved in zinc stress response. Journal of Plant Physiology, 171(12), 1054–1063. https://doi.org/10.1016/j.jplph.2014.03.016
Ruotolo, R., Maestri, E., Pagano, L., Marmiroli, M., White, J. C., & Marmiroli, N. (2018). Plant response to metal-containing engineered nanomaterials: an omics-based perspective. Environmental Science and Technology. https://doi.org/10.1021/acs.est.7b04121
Sathe, S. K. (1996). The nutritional value of selected Asiatic pulses: chickpea, black gram, mung bean and pigeon pea. Food and Feed from Legumes and Oilseeds (pp. 12–32). Springer.
Sergiev, I., Alexieva, V., Karanov, E. N., Karanov, E., Sergiev, L. M., Karanova E., & Alexieva, V. (1997). Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de l'Academie Bulgare des Sciences, 51(3), 121–124.
Shen, X., Huo, B., Wu, T., Song, C., & Chi, Y. (2019). iTRAQ-based proteomic analysis to identify molecular mechanisms of the selenium deficiency response in the Przewalski’s gazelle. Journal of Proteomics. https://doi.org/10.1016/j.jprot.2019.103389
Solymosi, K., & Bertrand, M. (2012). Soil metals, chloroplasts, and secure crop production: A review. Agronomy for Sustainable Development. https://doi.org/10.1007/s13593-011-0019-z
Song, C., Gan, S., He, J., & Shen, X. (2020a). Effects of nano-zinc on immune function in qianbei-pockmarked goats. Biological Trace Element Research. https://doi.org/10.1007/s12011-020-02182-z
Song, C. J., Gan, S., & Shen, X. (2020c). Effects of nano-copper poisoning on immune and antioxidant function in the wumeng semi-fine wool sheep. Biological Trace Element Research, 198(2), 515–520. https://doi.org/10.1007/s12011-020-02085-z
Song, C., Jiang, Q., & Shen, X. (2020b). Responses of przewalski’s gazelle (Procapra przewalskii) to zinc nutrition in physical habitat. Biological Trace Element Research. https://doi.org/10.1007/s12011-020-02137-4
Trujillo-Reyes, J., Majumdar, S., Botez, C. E., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2014). Exposure studies of core-shell Fe/Fe3O4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: Are they a potential physiological and nutritional hazard? Journal of Hazardous Materials, 267, 255–263. https://doi.org/10.1016/j.jhazmat.2013.11.067
Venkatachalam, P., Jayaraj, M., Manikandan, R., Geetha, N., Rene, E. R., Sharma, N. C., & Sahi, S. V. (2017). Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: A physiochemical analysis. Plant Physiology and Biochemistry, 110, 59–69. https://doi.org/10.1016/j.plaphy.2016.08.022
Wang, Z., Wang, S., & Peijnenburg, W. J. G. M. (2016). Prediction of joint algal toxicity of nano-CeO2/nano-TiO2 and florfenicol: Independent action surpasses concentration addition. Chemosphere, 156, 8–13. https://doi.org/10.1016/j.chemosphere.2016.04.072
White, J. C., & Gardea-Torresdey, J. (2018). Achieving food security through the very small. Nature Nanotechnology, 13(8), 627–629. https://doi.org/10.1038/s41565-018-0223-y
Wu, T., Song, M., & Shen, X. (2020). Seasonal dynamics of copper deficiency in wumeng semi-fine wool sheep. Biological Trace Element Research, 197(2), 487–494. https://doi.org/10.1007/s12011-019-02018-5
Yahyaoui, A., Bouarroudj, T., & Houssem, K. (2017). Metabolic capacities of three strains of pseudomonas aeruginosa to biodegrade crude oil 1hassaine amina and bordjiba ouahiba advances in environmental biology view project mohammed-réda Djebar. https://www.researchgate.net/publication/323586692. Accessed from 23 May 2021.
Zazpe, I., Sánchez-Taínta, A., Santiago, S., De La Fuente-Arrillaga, C., Bes-Rastrollo, M., Martínez, J. A., & Martínez-González, M. Á. (2014). Association between dietary carbohydrate intake quality and micronutrient intake adequacy in a Mediterranean cohort: The SUN (Seguimiento Universidad de Navarra) project. British Journal of Nutrition, 111(11), 2000–2009. https://doi.org/10.1017/S0007114513004364
Zhao, L., Lu, L., Wang, A., Zhang, H., Huang, M., Wu, H., et al. (2020). Nano-biotechnology in agriculture: Use of nanomaterials to promote plant growth and stress tolerance. Journal of Agricultural and Food Chemistry, 68(7), 1935–1947. https://doi.org/10.1021/acs.jafc.9b06615
Acknowledgements
This work was supported by the Tunisian Ministry of High Education and Research, and the Dry Land and Oases Cropping Laboratory in Arid Land Institute of Medenine (IRA). We acknowledge the help and support of Mr Mustapha Neji, Mr Mohamed Bahka, the technicians at ISBAM, for purchasing materials and chemicals.
Funding
Tunisian Ministry of High Education and Research.
Author information
Authors and Affiliations
Contributions
IK contributed to conceptualization and writing—original draft preparation; IK, ST, BL, TB, MM were involved in methodology; IK and ST performed formal analysis and investigation; IK, ST and AC done writing—review and editing; MD, ML and AC contributed to funding acquisition; MD, ML, TB, MM and AC done resources; IK, ML, MD and AC supervised the study.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Data availability
Declared, data transparency.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Karmous, I., Tlahig, S., Loumerem, M. et al. Assessment of the risks of copper- and zinc oxide-based nanoparticles used in Vigna radiata L. culture on food quality, human nutrition and health. Environ Geochem Health 44, 4045–4061 (2022). https://doi.org/10.1007/s10653-021-01162-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-021-01162-z