Skip to main content

Advertisement

Log in

The toxic effect of CuO of different dispersion degrees on the structure and ultrastructure of spring barley cells (Hordeum sativum distichum)

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Nowadays, nanotechnology is one of the most dynamically developing and most promising technologies. However, the safety issues of using metal nanoparticles, their environmental impact on soil and plants are poorly understood. These studies are especially important in terms of copper-based nanomaterials because they are widely used in agriculture. Concerning that, it is important to study the mechanism behind the mode of CuO nanoparticles action at the ultrastructural intracellular level. It is established that the contamination with CuO has had a negative influence on the development of spring barley. A greater toxic effect has been exerted by the introduction of CuO nanoparticles as compared to the macrodispersed form. A comparative analysis of the toxic effects of copper oxides and nano-oxides on plants has shown changes in the tissue and intracellular levels in the barley roots. However, qualitative changes in plant leaves have not practically been observed. In general, conclusions can be made that copper oxide in nano-dispersed form penetrates better from the soil into the plant and can accumulate in large quantities in it.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anjum, N. A., Gill, S. S., Duarte, A. C., et al. (2013). Silver nanoparticles in soil–plant systems. Journal of Nanoparticle Research, 15, 1–26. https://doi.org/10.1007/s11051-013-1896-7.

    Article  Google Scholar 

  • Arendt, E. K., & Zannini, E. (2013). Cereal grains for the food and beverage industries (p. 512). Amsterdam: Woodhead Publishing Limited.

    Book  Google Scholar 

  • Assadian, E., Zarei, M. H., Gilani, A. G., et al. (2017). Toxicity of copper oxide (CuO) nanoparticles on human blood lymphocytes. Biological Trace Element Research, 184(2), 350–357. https://doi.org/10.1007/s12011-019-01678-7.

    Article  CAS  Google Scholar 

  • Bauer, T., Pinskii, D., Minkina, T., Nevidomskaya, D., Mandzhieva, S., Burachevskaya, M., et al. (2018). Time effect on the stabilization of technogenic copper compounds in solid phases of Haplic Chernozem. Science of the Total Environment, 626, 1100–1107.

    Article  CAS  Google Scholar 

  • Conway, J. R., Hanna, S. K., Lenihan, H. S., & Keller, A. A. (2014). Effects and implications of trophic transfer and accumulation of CeO2 nanoparticles in a marine mussel. Environmental Science and Technology, 48, 1517–1524. https://doi.org/10.1021/es404549u.

    Article  CAS  Google Scholar 

  • Costa, D. M. V. J., & Sharma, P. K. (2016). Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica, 54, 110. https://doi.org/10.1007/s11099-015-0167-5.

    Article  CAS  Google Scholar 

  • Darlington, T. K., Neigh, A. M., Spencer, M. T., Nguyen, O. T., & Oldenburg, S. J. (2009). Nanoparticle characteristics affecting environmental fate and transport through soil. Environmental Toxicology and Chemistry, 28(6), 1191–1199.

    Article  CAS  Google Scholar 

  • Dmitrakov, L. M., & Dmitrakova, L. К. (2006). Lead translocation in oat plants. Agrochemistry, 2, 71–77. (in Russian).

    Google Scholar 

  • Du, W., Tan, W., Yin, Y., Ji, R., Peralta-Videa, J. R., Guo, H., et al. (2018). Differential effects of copper nanoparticles/microparticles in agronomic and physiological parameters of oregano (Origanum vulgare). Science of the Total Environment, 618, 306–312.

    Article  CAS  Google Scholar 

  • Fedorenko, G. M., Fedorenko, A. G., Minkina, T. M., et al. (2018). Method for hydrophytic plant sample preparation for light and electron microscopy (studies on Phragmites australis Cav.). MethodsX, 5, 1213–1220. https://doi.org/10.1016/j.mex.2018.09.009.

    Article  Google Scholar 

  • Festa, R. A., & Thiele, D. J. (2011). Copper: an essential metal in biology. Current Biology, 21, 877–883. https://doi.org/10.1016/j.cub.2011.09.040.

    Article  CAS  Google Scholar 

  • Gabbay, J., Borkow, G., Mishal, J., Magen, E., Zatcoff, R., & Shemer-Avni, Y. (2006). Copper oxide impregnated textiles with potent biocidal activities. Journal of Industrial Textiles, 35, 323–335. https://doi.org/10.1177/1528083706060785.

    Article  CAS  Google Scholar 

  • Gomes, T., Pinheiro, J. P., Cancio, I., et al. (2011). Effects of copper nanoparticles exposure in the mussel Mytilus galloprovincialis. Environmental Science and Technology, 45, 9356–9362. https://doi.org/10.1021/es200955s.

    Article  CAS  Google Scholar 

  • Griffitt, R. J., Hyndman, K., Denslow, N. D., & Barber, D. S. (2009). Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicological Sciences, 107(2), 404–415. https://doi.org/10.1093/toxsci/kfn256.

    Article  CAS  Google Scholar 

  • Gunawan, C., Teoh, W. Y., Marquis, C. P., & Amal, R. (2011). Cytotoxic origin of copper (II) oxide nanoparticles: comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano, 5, 7214–7225. https://doi.org/10.1021/nn2020248.

    Article  CAS  Google Scholar 

  • Guzman, K. A., Finnegan, M. P., & Banfield, J. F. (2006). Influence of surface potential on aggregation and transport of titania nanoparticles. Environmental Science and Technology, 40(24), 7688–7693.

    Article  Google Scholar 

  • Hänsch, R., & Mendel, R. R. (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology, 12(3), 259–266. https://doi.org/10.1016/j.pbi.2009.05.006.

    Article  CAS  Google Scholar 

  • Hartwig, A. (2013). Metal interaction with redox regulation: an integrating concept in metal carcinogenesis? Free Radical Biology and Medicine, 55, 63–72. https://doi.org/10.1016/j.freeradbiomed.2012.11.009.

    Article  CAS  Google Scholar 

  • Hou, J., Wang, X., Hayat, T., & Wang, X. (2017). Ecotoxicological effects and mechanism of CuO nanoparticles to individual organisms. Environmental Pollution, 221, 209–217.

    Article  CAS  Google Scholar 

  • Hu, W., Culloty, S., Darmody, G., et al. (2014). Toxicity of copper oxide nanoparticles in the blue mussel, Mytilus edulis: A redox proteomic investigation. Chemosphere, 108, 289–299. https://doi.org/10.1016/j.chemosphere.2014.01.054.

    Article  CAS  Google Scholar 

  • Ivask, A., Bondarenko, O., Jepihhina, N., & Kahru, A. (2010). Profiling of the reactive oxygen species related eco-toxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Analytical and Bioanalytical Chemistry, 398, 701–716. https://doi.org/10.1007/s00216-010-3962-7.

    Article  CAS  Google Scholar 

  • Julich, D., & Gäth, S. (2014). Sorption behavior of copper nanoparticles in soils compared to copper ions. Geoderma, 235–236, 127–132. https://doi.org/10.1016/j.geoderma.2014.07.003.

    Article  CAS  Google Scholar 

  • Kahru, A., & Ivask, A. (2013). Mapping the dawn of nanoecotoxicological research. Accounts of Chemical Research, 46(3), 823–833. https://doi.org/10.1021/ar3000212.

    Article  CAS  Google Scholar 

  • Keller, A., McFerran, S., Lazareva, A., et al. (2013). Global life cycle releases of engineered nanomaterials. Journal of Nanoparticle Research, 15, 1692. https://doi.org/10.1007/s11051-013-1692-4.

    Article  Google Scholar 

  • Krzesłowska, M., Lenartowska, M., Samardakiewicz, S., Bilski, H., & Woźny, A. (2010). Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable-a remobilization can occur. Current Opinion in Plant Biology, 158, 325–338.

    Google Scholar 

  • Kulizhsky, S., Loyko, S., & Lim, A. (2013). Pedotransfer capacity of nickel and platinum nanoparticles in Albeluvisols Haplic in the South-East of the Western Siberia. Eurasian J. Soil Sci., 2(2), 90–96.

    Google Scholar 

  • Kvesitadze, G. I., Khatisashvili, G. A., Sadunishvili, T. A., & Evstigeneeva, Z. G. (2005). Metabolism of anthropogenic toxicants in higher plants (p. 199). Moscow: Publishing House Science. (in Russian).

    Google Scholar 

  • Lecoanet, H. F., Bottero, J.-Y., & Wiesner, M. R. (2004). Laboratory assessment of the mobility of nanomaterials in porous media. Environmental Science and Technology, 38(19), 5164–5169.

    Article  CAS  Google Scholar 

  • Ma, X., Geiser-Lee, J., Deng, Y., & Kolmakov, A. (2010). Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Science of the Total Environment, 408(16), 3053–3061. https://doi.org/10.1016/j.scitotenv.2010.03.031.

    Article  CAS  Google Scholar 

  • MacFarlane, G. R., & Burchett, M. D. (2000). Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquatic Botany, 68, 45–59.

    Article  CAS  Google Scholar 

  • McVay, I. R., Maher, W. A., Krikowa, F., & Ubrhien, R. (2019). Metal concentrations in waters, sediments and biota of the far south-east coast of New South Wales, Australia, with an emphasis on Sn, Cu and Zn used as marine antifoulant agents. Environmental Geochemistry and Health, 41, 1351–1367.

    Article  CAS  Google Scholar 

  • Minkina, T. M., Fedorov, Y. A., Nevidomskaya, D. G., Pol’shina, T. N., Mandzhieva, S. S., & Chaplygin, V. A. (2017). Heavy metals in soils and plants of the don river estuary and the Taganrog Bay coast. Eurasian Soil Science, 50(9), 1033–1047. https://doi.org/10.1134/S1064229317070067.

    Article  CAS  Google Scholar 

  • Minkina, T., Rajput, V., Fedorenko, G., Fedorenko, A., Mandzhieva, S., Sushkova, S., et al. (2019). Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-019-00269-8.

    Article  Google Scholar 

  • Morgalev, Yu N, Khoch, N. S., Morgaleva, T. G., et al. (2010). Biological testing of nanomaterials: on the possibility of nanoparticles translocation into food networks. Russian Nanotechnologies, 5, 131–135. https://doi.org/10.1134/S1995078010110157.

    Article  Google Scholar 

  • Musante, C., & White, J. C. (2012). Toxicity of silver and copper to Cucurbita pepo: Differential effects of nano and bulk-size particles. Environmental Toxicology, 27, 510–517.

    Article  CAS  Google Scholar 

  • Navratilova, J., Praetorius, A., Gondikas, A., Fabienke, W., von der Kammer, F., & Hofmann, T. (2015). Detection of engineered copper nanoparticles in soil using single particle ICP-MS. International Journal of Environmental Research and Public Health, 12(12), 15756–15768. https://doi.org/10.3390/ijerph121215020.

    Article  CAS  Google Scholar 

  • Nishizono, H., Ichikawa, H., Suziki, S., & Ishii, F. (1987). The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant and Soil, 101, 15–20.

    Article  CAS  Google Scholar 

  • Oberdörster, G., Stone, V., & Donaldson, K. (2007). Toxicology of nanoparticles: A historical perspective. Nanotoxicology, 1, 2–25. https://doi.org/10.1080/17435390701314761.

    Article  CAS  Google Scholar 

  • Ouzounidou, G., Eleftheriou, E., & Karataglis, S. (1992). Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). Canadian Journal of Botany, 70, 947–957.

    Article  CAS  Google Scholar 

  • Panou-Filotheou, H., Bosabalidis, A. M., & Karataglis, S. (2001). Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Annals of Botany, 88, 207–214. https://doi.org/10.1006/anbo.2001.1441.

    Article  CAS  Google Scholar 

  • Peng, C., Duan, D. C., Xu, C., et al. (2015). Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environmental Pollution, 197, 99–107. https://doi.org/10.1016/j.envpol.2014.12.008.

    Article  CAS  Google Scholar 

  • Perevolotskaya, T. V., & Anisimov, V. S. (2018). Conceptual and mathematical statement of the process of heavy metals migration in the system soil–agricultural plant. Biogeosystem Technique, 5(1), 110–128. https://doi.org/10.13187/bgt.2018.1.110.

    Article  Google Scholar 

  • Phenrat, T., Kim, H.-J., Fagerlund, F., Illangasekare, T., Tilton, R. D., & Lowry, G. V. (2009). Particle size distribution, concentration, and magnetic attraction affect transport of polymer-modified Fe0 nanoparticles in sand columns. Environmental Science and Technology, 43(13), 5079–5085.

    Article  CAS  Google Scholar 

  • Rajput, V., Minkina, T., Ahmed, B., Sushkova, S., Singh, R., Soldatov, M., et al. (2020). Interaction of copper-based nanoparticles to soil, terrestrial, and aquatic systems: Critical review of the state of the science and future perspectives. Reviews of Environmental Contamination and Toxicology, 252, 51–96. https://doi.org/10.1007/398_2019_34.

    Article  CAS  Google Scholar 

  • Rajput, V., Minkina, T., Sushkova, S., Behal, A., Maksimov, A., Blicharska, E., et al. (2019). ZnO and CuO nanoparticles: A threat to soil organisms, plants, and human health. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-019-00317-3.

    Article  Google Scholar 

  • Rajput, V., Minkina, T. M., Fedorenko, A. G., et al. (2018a). Toxicity of copper oxide nanoparticles on spring barley (Hordeum sativum distichum). Science of the Total Environment, 645, 1103–1113. https://doi.org/10.1016/j.scitotenv.2018.07.211.

    Article  CAS  Google Scholar 

  • Rajput, V. D., Minkina, T., Suskova, S., et al. (2018b). Effects of copper nanoparticles (CuO NPs) on crop plants: A mini review. BioNanoSci, 8, 36–42. https://doi.org/10.1007/s12668-017-0466-3.

    Article  Google Scholar 

  • Rico, C. M., Majumdar, S., Duarte-Gardea, M., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. Journal of Agriculture and Food Chemistry, 59, 3485–3498. https://doi.org/10.1021/jf104517j.

    Article  CAS  Google Scholar 

  • Shaw, A. K., & Hossain, Z. (2013). Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere, 93, 906–915. https://doi.org/10.1016/j.chemosphere.2013.05.044.

    Article  CAS  Google Scholar 

  • Tutayuk, V. H. (1972). Anatomy and morphology of plants. Textbook for agricultural universities (p. 336). Moscow: Higher School Publishing House. (in Russian).

    Google Scholar 

  • Usatov, A. V., Fedorenko, G. M., Shcherbakova, L. B., & Mashkina, E. V. (2004). Ultrastructure of chloroplasts in mustard Brassica juncea as an index of salt tolerance. Tsitologiya, 46, 1035–1042.

    CAS  Google Scholar 

  • Vesk, P. A., Nockolds, C. E., & Allaway, W. G. (1999). Metal localization in water hyacinth roots from an urban wetland. Plant, Cell and Environment, 22, 149–158.

    Article  Google Scholar 

  • Xiong, T., Dumat, C., Dappe, V., Vezin, H., Schreck, E., Shahid, M., et al. (2017). Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environmental Science and Technology, 51, 5242–5251.

    Article  CAS  Google Scholar 

  • Ytterberg, A. J., Peltier, J. B., & van Wijk, K. J. (2006). Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiology, 140, 984–997.

    Article  CAS  Google Scholar 

  • Zhang, N., He, X. D., Gao, Y. B., Li, Y. H., Wang, H. T., Ma, D., et al. (2010). Pedogenic carbonate and soil dehydrogenase activity in response to soil organic matter in Artemisia ordosica community. Pedosphere, 20, 229–235. https://doi.org/10.1016/s1002-0160(10)60010-0.

    Article  CAS  Google Scholar 

  • Zuverza-Mena, N., Medina-Velo, I. A., Barrios, A. C., Tan, W., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2015). Copper nanoparticles/compounds impact agronomic and physiological parameters in cilantro (Coriandrum sativum). Environmental Science: Processes & Impacts, 17, 1783–1793. https://doi.org/10.1039/c5em00329f.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Russian Scientific Foundation, No. 19-74-10046. Analytical work was carried out on the equipment of Centers for collective use of Southern Federal University “Modern microscopy” and “High Technology.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tatiana M. Minkina.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fedorenko, A.G., Minkina, T.M., Chernikova, N.P. et al. The toxic effect of CuO of different dispersion degrees on the structure and ultrastructure of spring barley cells (Hordeum sativum distichum). Environ Geochem Health 43, 1673–1687 (2021). https://doi.org/10.1007/s10653-020-00530-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-020-00530-5

Keywords

Navigation