Skip to main content
Log in

Genotoxic and morpho-physiological responses of ZnO macro- and nano-forms in plants

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

Abstract

In the current study, two plants, viz., Pisum sativum L. and Hordeum vulgare L., were exposed to nano- and macro-dispersed ZnO at 1, 10, and 30 times of maximal permissible concentration (MPC). The main objective of the study is to depict and compare the genotoxicity in terms of chromosomal anomalies, cytotoxicity (i.e., mitotic index), and phytotoxicity (viz., germination, morphometry, maximal quantum yield, and chlorophyll fluorescence imaging) of macro- and nano-forms of ZnO along with their accumulation and translocation. In the case of genotoxic and cytotoxic responses, the maximal effect was observed at 30 MPC, regardless of the macro- or nano-forms of ZnO. The phytotoxic observations revealed that the treatment with macro- and nano-forms of ZnO significantly affected the germination rate, germination energy, and length of roots and shoots of H. vulgare in a dose-dependent manner. The factor toxicity index of treated soil demonstrated that toxicity soared as concentrations increased and that at 30 MPC, toxicity was average and high in macro- and nano-dispersed ZnO, respectively. Furthermore, the photosynthetic parameters were observed to be negatively affected in both treatments, but the maximal effect was observed in the case of nano-dispersed form. It was noted that the mobility of nano-dispersed ZnO in the soil was higher than macro-dispersed. The increased mobility of nano-dispersed ZnO might have boosted their accumulation and translocation that subsequently led to the oxidative stress due to the accelerated production of reactive oxygen species, thus strengthen toxicity implications in plants.

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

Similar content being viewed by others

Data availability

Associated data are submitted as supplementary materials.

References

  • Abdelsalam, N. R., Abdel-Megeed, A., Ghareeb, R. Y., Ali, H. M., Salem, M. Z., Akrami, M., & Desoky, E. S. M. (2021). Genotoxicity assessment of amino zinc nanoparticles in wheat (Triticum aestivum L.) as cytogenetical perspective. Saudi Journal of Biological Sciences., 29(4), 2306.

    Article  Google Scholar 

  • Ali, S., Rizwan, M., Noureen, S., Anwar, S., Ali, B., Naveed, M., & 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. Environmental Science and Pollution Research, 26(11), 11288–11299.

    Article  CAS  Google Scholar 

  • Alov I. A. Patologiya mitoza // Vestnik AN SSSR. (1965) № 11.—S. 58–66. [In Russian].

  • Baker, N. R., & Rosenqvist, E. (2004). Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. Journal of Experimental Botany, 55(403), 1607–1621. https://doi.org/10.1093/JXB/ERH196

    Article  CAS  Google Scholar 

  • Barabasz-Krasny, B., MoŻDŻEŃ, K., SoŁTys-Lelek, A., & Turisová, I. (2020). The role of light in the adaptation of Thymus praecox Opiz subsp. praecox for diverse habitat conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 48(3), 1194–1209.

    Article  Google Scholar 

  • Bezuglova, O. S., Gorbov, S. N., Tischenko, S. A., & Shimko, A. E. (2018). Use of brown coal as a detoxifier of soils contaminated with heavy metals. Journal of Geochemical Exploration, 184, 232–238. https://doi.org/10.1016/J.GEXPLO.2016.11.004

    Article  CAS  Google Scholar 

  • Chaplygin, V., Mandzhieva, S., Minkina, T., Sushkova, S., Kizilkaya, R., Gülser, C., & Chernikova, N. (2021). Sustainability of agricultural and wild cereals to aerotechnogenic exposure. Environmental Geochemistry and Health, 43(4), 1427–1439.

    Article  CAS  Google Scholar 

  • Debnath, P., Mondal, A., Hajra, A., Das, C., & Mondal, N. K. (2018). Cytogenetic effects of silver and gold nanoparticles on Allium cepa roots. Journal of Genetic Engineering and Biotechnology, 16(2), 519–526.

    Article  Google Scholar 

  • Dimkpa, C. O., Singh, U., Bindraban, P. S., Elmer, W. H., Gardea-Torresdey, J. L., & White, J. C. (2019). Zinc oxide nanoparticles alleviate drought-induced alterations in sorghum performance, nutrient acquisition, and grain fortification. Science of the Total Environment, 688, 926–934.

    Article  CAS  Google Scholar 

  • Dubrovsky, J. G., & Contreras-Burciaga, L. (1998). A squash preparation method for root meristem field studies. Biotechnic & Histochemistry: Official Publication of the Biological Stain Commission, 73(2), 92–96. https://doi.org/10.3109/10520299809140512

    Article  CAS  Google Scholar 

  • Egbuna, C., Parmar, V. K., Jeevanandam, J., Ezzat, S. M., Patrick-Iwuanyanwu, K. C., Adetunji, C. O., Khan, J., Onyeike, E. N., Uche, C. Z., Akram, M., Ibrahim, M. S., el Mahdy, N. M., Awuchi, C. G., Saravanan, K., Tijjani, H., Odoh, U. E., Messaoudi, M., Ifemeje, J. C., Olisah, M. C., & Ibeabuchi, C. G. (2021). Toxicity of nanoparticles in biomedical application: Nanotoxicology. Journal of Toxicology. https://doi.org/10.1155/2021/9954443

    Article  Google Scholar 

  • García-Gómez, C., García, S., Obrador, A. F., González, D., Babín, M., & Fernández, M. D. (2018). Effects of aged ZnO NPs and soil type on Zn availability, accumulation and toxicity to pea and beet in a greenhouse experiment. Ecotoxicology and Environmental Safety, 160, 222–230.

    Article  Google Scholar 

  • Grif, V. G., & Machs, E. M. (1994). Rhythms of mitotic activity and cell cycles in plant meristems. Cytology, 36(11), 1069–1080.

    Google Scholar 

  • Guidelines, M. (1992). Methodological guidelines on the determination of heavy metals in agricultural soils and crops. TsINAO. (in Russian).

    Google Scholar 

  • Ji, Y., Xie, X., & Wang, G. (2018). Effects of the heavy metal cadmium on photosynthetic activity and the xanthophyll cycle in Phaeodactylum tricornutum. Journal of Oceanology and Limnology, 36(6), 2194–2201.

    Article  CAS  Google Scholar 

  • Kalaji, H. M., Schansker, G., Brestic, M., Filippo, B., Calatayud, A., Ferroni, L., Goltsev, V., Guidi, L., Jajoo, A., Li, P., Losciale, P., Mishra, V. K., Amarendra, M. N., Nebauer, S. G., Pancaldi, S., Penella, C., Pollastrini, M., Suresh, K., & Zivcak, M. (2017). Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Reserch, 132, 13–66. https://doi.org/10.1007/s11120-016-0318-y

    Article  CAS  Google Scholar 

  • Khan, M., Khan, M. S. A., Borah, K. K., Goswami, Y., Hakeem, K. R., & Chakrabartty, I. (2021). The potential exposure and hazards of metal-based nanoparticles on plants and environment, with special emphasis on ZnO NPs, TiO2 NPs, and AgNPs: A review. Environmental Advances, 6, 100128. https://doi.org/10.1016/J.ENVADV.2021.100128

    Article  CAS  Google Scholar 

  • Kolesnikov, S. I., Varduny, T. V., Lysenko, V. S., Kapralova, O. A., Chokheli, V. A., Sereda, M. M., Dmitriev, P. A., & Varduny, V. M. (2018). Effect of nano- and crystalline metal oxides on growth. gene- and cytotoxicity of plants in vitro and ex vitro. Turczaninowia, 21(4), 207–214.

    Article  Google Scholar 

  • Kolesnikov, S., Minnikova, T., Kazeev, K., Akimenko, Y., & Evstegneeva, N. (2022). Assessment of the ecotoxicity of pollution by potentially toxic elements by biological indicators of haplic chernozem of Southern Russia (Rostov region). Water, Air, & Soil Pollution, 233(1), 1–18.

    Article  Google Scholar 

  • Kumari, A., & Kaur, R. (2018). Evaluation of benzyl-butyl phthalate induced germination and early growth vulnerability to barley seedlings (Hordeum vulgare L.). Indian Journal of Ecology, 45(1), 174–177.

    Google Scholar 

  • Kumari, A., Arora, S., & Kaur, R. (2020). Comparative cytotoxic and genotoxic potential of benzyl-butyl phthalate and di-n-butyl phthalate using Allium cepa assay. Energy, Ecology and Environment. https://doi.org/10.1007/s40974-020-00186-y

    Article  Google Scholar 

  • Leme, D. M., & Marin-Morales, M. A. (2009). Allium cepa test in environmental monitoring: A review on its application. Mutation Research/reviews in Mutation Research, 682(1), 71–81. https://doi.org/10.1016/J.MRREV.2009.06.002

    Article  CAS  Google Scholar 

  • Lichtenthaler, H. K., & Babani, F. (2004) Light adaptation and senescence of the photosynthetic apparatus Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity In: Chlorophyll a fluorescence. Springer, (pp 713–736)

  • Lovecká, P., Macůrková, A., Záruba, K., Hubáček, T., Siegel, J., & Valentová, O. (2021). Genomic damage induced in Nicotiana tabacum L. plants by colloidal solution with silver and gold nanoparticles. Plants, 10(6), 1260. https://doi.org/10.3390/PLANTS10061260

    Article  Google Scholar 

  • Lysenko, V. S., Varduny, T. V., Kosenko, P. O., Kosenko, Y. V., Chugueva, O. I., Semin, L. V., & Guskova, O. S. (2014). Video registration as a method for studying kinetic parameters of chlorophyll fluorescence in Ficus benjamina leaves. Russian Journal of Plant Physiology, 61(3), 419–425.

    Article  CAS  Google Scholar 

  • Lysenko, V., Guo, Y., & Chugueva, O. (2016). Cyclic Electron Transport around photosystem II: Mechanisms and methods of study. American Journal of Plant Physiology, 12(1), 1–9. https://doi.org/10.3923/AJPP.2017.1.9

    Article  Google Scholar 

  • Lysenko, V., Lazár, D., & Varduny, T. (2018). A method of a bicolor fast-Fourier pulse-amplitude modulation chlorophyll fluorometry. Photosynthetica, 56(4), 1447–1452.

    Article  CAS  Google Scholar 

  • Ma, X., & Yan, J. (2018). Plant uptake and accumulation of engineered metallic nanoparticles from lab to field conditions. Current Opinion in Environmental Science & Health, 6, 16–20.

    Article  Google Scholar 

  • Makarova, V. N., & Krasnitsky, A. A. (2020). Bioindication of soil based on differences in parameters of development of the indicator species in soils of sifferent territories of Vladivostok. In IOP Conference Series: Earth and Environmental Science (Vol. 459, No. 4, p. 042013). IOP Publishing.

  • Manuja, A., Kumar, B., Kumar, R., Chhabra, D., Ghosh, M., Manuja, M., Brar, B., Pal, Y., Tripathi, B. N., & Prasad, M. (2021). Metal/metal oxide nanoparticles: Toxicity concerns associated with their physical state and remediation for biomedical applications. Toxicology Reports, 8, 1970–1978. https://doi.org/10.1016/J.TOXREP.2021.11.020

    Article  CAS  Google Scholar 

  • Matras, E., Gorczyca, A., Pociecha, E., Przemieniecki, S. W., & Oćwieja, M. (2022). Phytotoxicity of silver nanoparticles with different surface properties on monocots and dicots model plants. Journal of Soil Science and Plant Nutrition, 1, 1–18. https://doi.org/10.1007/S42729-022-00760-9/FIGURES/7

    Article  Google Scholar 

  • Minkina, T. M., Mandzhieva, S. S., Burachevskaya, M. V., Bauer, T. V., & Sushkova, S. N. (2018). Method of determining loosely bound compounds of heavy metals in the soil. MethodsX, 5, 217–226. https://doi.org/10.1016/j.mex.2018.02.007

    Article  Google Scholar 

  • Minkina, T. M., Fedorenko, G. M., Nevidomskaya, D. G., Pol’shina, T. N., Fedorenko, A. G., Chaplygin, V. A., & Hassan, T. M. (2021). Bioindication of soil pollution in the delta of the Don River and the coast of the Taganrog Bay with heavy metals based on anatomical, morphological and biogeochemical studies of macrophyte (Typha australis Schum & Thonn). Environmental Geochemistry and Health, 43(4), 1563–1581.

    Article  CAS  Google Scholar 

  • Murali, M., Anandan, S., Ansari, M. A., Alzohairy, M. A., Alomary, M. N., Asiri, S. M. M., & Amruthesh, K. N. (2021). Genotoxic and cytotoxic properties of zinc oxide nanoparticles phyto-fabricated from the obscure morning glory plant Ipomoea obscura (L.) Ker Gawl. Molecules, 26(4), 891.

    Article  CAS  Google Scholar 

  • SanPiN 1.2.3685–21 Hygienic standards and requirements for ensuring the safety and (or) harmlessness of environmental factors for humans; Code: SanPiN 1.2.3685–21, Valid from March 1 2021. (in Russian)

  • Papageorgiou, G. C., & Govindjee. (2011). Photosystem II fluorescence: Slow changes–scaling from the past. Journal of Photochemistry and Photobiology B: Biology, 104(1–2), 258–270.

  • Potapova, T., & Gorbsky, G. J. (2017). The consequences of chromosome segregation errors in mitosis and meiosis. Biology. https://doi.org/10.3390/BIOLOGY6010012

    Article  Google Scholar 

  • Pullagurala, V. L. R., Adisa, I. O., Rawat, S., Kim, B., Barrios, A. C., Medina-Velo, I. A., & Gardea-Torresdey, J. L. (2018). Finding the conditions for the beneficial use of ZnO nanoparticles towards plants-A review. Environmental Pollution, 241, 1175–1181.

    Article  Google Scholar 

  • Rajput, V., Minkina, T., Fedorenko, A., Sushkova, S., Mandzhieva, S., Lysenko, V., Duplii, N., Fedorenko, G., Dvadnenko, K., & Ghazaryan, K. (2018). 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., Upadhyay, S. K., Kumari, A., Ranjan, A., Mandzhieva, S., Sushkova, S., Singh, R. K., & Verma, K. K. (2022). Nanotechnology in the restoration of polluted soil. Nanomaterials, 12(5), 769. https://doi.org/10.3390/NANO12050769

    Article  CAS  Google Scholar 

  • Ray, P. C., Yu, H., & Fu, P. P. (2009). Toxicity and environmental risks of nanomaterials: Challenges and future needs. Journal of Environmental Science and Health Part C, 27(1), 1–35. https://doi.org/10.1080/10590500802708267

    Article  CAS  Google Scholar 

  • Reihlen, A., Ruut, J., Engewald, P., Fammler, H., & Moukhametshina, E. (2010). The Russian system of chemicals management: Current understanding. Baltic Environmental Forum Group.

    Google Scholar 

  • Salehi, H., De Diego, N., Rad, A. C., Benjamin, J. J., Trevisan, M., & Lucini, L. (2021). Exogenous application of ZnO nanoparticles and ZnSO4 distinctly influence the metabolic response in Phaseolus vulgaris L. Science of the Total Environment, 778, 146331.

    Article  CAS  Google Scholar 

  • Sheteiwy, M. S., Dong, Q., An, J., Song, W., Guan, Y., He, F., & Hu, J. (2017). Regulation of ZnO nanoparticles-induced physiological and molecular changes by seed priming with humic acid in Oryza sativa seedlings. Plant Growth Regulation, 83(1), 27–41.

    Article  CAS  Google Scholar 

  • Soares, E. V., & Soares, H. M. V. M. (2021). Harmful effects of metal(loid) oxide nanoparticles. Applied Microbiology and Biotechnology, 105(4), 1379–1394. https://doi.org/10.1007/S00253-021-11124-1

    Article  CAS  Google Scholar 

  • Suganya, A., Saravanan, A., & Manivannan, N. (2020). Role of zinc nutrition for increasing zinc availability, uptake, yield, and quality of maize (Zea mays L.) grains: An overview. Communications in Soil Science and Plant Analysis, 51(15), 2001–2021.

    Article  CAS  Google Scholar 

  • Thounaojam, T. C., Meetei, T. T., Devi, Y. B., Panda, S. K., & Upadhyaya, H. (2021). Zinc oxide nanoparticles (ZnO-NPs): A promising nanoparticle in renovating plant science. Acta Physiologiae Plantarum, 43(10), 1–21.

    Article  Google Scholar 

  • Thwala, M., Klaine, S., & Musee, N. (2021). Exposure media and nanoparticle size influence on the fate, bioaccumulation, and toxicity of silver nanoparticles to higher plant salvinia minima. Molecules, 26(8), 2305. https://doi.org/10.3390/MOLECULES26082305

    Article  CAS  Google Scholar 

  • Verma, S., & Srivastava, A. (2018). Cyto-genotoxic consequences of carbendazim treatment monitored by cytogenetical analysis using allium root tip bioassay. Environmental Monitoring and Assessment, 190(4), 1–10.

    Article  CAS  Google Scholar 

  • Wakeel, A., Xu, M., & Gan, Y. (2020). Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. International Journal of Molecular Sciences, 21(3), 728. https://doi.org/10.3390/IJMS21030728

    Article  CAS  Google Scholar 

  • Xu, H., Lau, Y.-M., Yin, X.-H., Xu, Y.-M., & Lau, A. T. Y. (2022). Nanoparticles: Excellent materials yet dangerous when they become airborne. Toxics, 10(2), 50. https://doi.org/10.3390/TOXICS10020050

    Article  Google Scholar 

  • Yang, X., Pan, H., Wang, P., & Zhao, F. J. (2017). Particle-specific toxicity and bioavailability of cerium oxide (CeO2) nanoparticles to Arabidopsis thaliana. Journal of Hazardous Materials, 322, 292–300.

    Article  CAS  Google Scholar 

  • Youssef, M. S., & Elamawi, R. M. (2020). Evaluation of phytotoxicity, cytotoxicity, and genotoxicity of ZnO nanoparticles in Vicia faba. Environmental Science and Pollution Research, 27(16), 18972–18984.

    Article  CAS  Google Scholar 

  • Zafar, H., Ali, A., Ali, J. S., Haq, I. U., & Zia, M. (2016). Effect of ZnO nanoparticles on Brassica nigra seedlings and stem explants: Growth dynamics and antioxidative response. Frontiers in Plant Science, 7, 535.

    Article  Google Scholar 

  • Zhu, J., Zou, Z., Shen, Y., Li, J., Shi, S., Han, S., & Zhan, X. (2019). Increased ZnO nanoparticle toxicity to wheat upon co-exposure to phenanthrene. Environmental Pollution, 247, 108–117.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The study was supported by the grant from the Russian Science Foundation (project No. 21-77-20089) at the Southern Federal University.

Funding

The study was supported by the grant from the Russian Science Foundation (project No. 21-77-20089) at the Southern Federal University.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization and Methodology were contributed by SSM and TMM; experiment performing was contributed by VAC, VL, AK, MM, and AB; writing—original draft was contributed by AK; writing—review and editing was contributed by AK, VDR, SSM, VAS, SS, and TMM; All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Arpna Kumari.

Ethics declarations

Conflict of interest

All the authors declare that there are no conflicts of interest whatsoever.

Human and animal rights

Presented work does not involve animal subjects.

Consent to participate and consent to publish

All authors were actively involved in this work and given.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumari, A., Chokheli, V.A., Lysenko, V.S. et al. Genotoxic and morpho-physiological responses of ZnO macro- and nano-forms in plants. Environ Geochem Health 45, 9345–9357 (2023). https://doi.org/10.1007/s10653-022-01428-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-022-01428-0

Keywords

Navigation