Regulation of cation currents through the plasma membrane of root cells of higher plants under the influence of copper, iron and titanium oxide nanoparticles

Authors

  • Palina V. Hryvusevich Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus
  • Veranika Ya. Artsisheuskaya Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus
  • Marharyta A. Mysleika V. F. Kuprevich Institute of Experimental Botany, National Academy of Sciences of Belarus, 27 Akademichnaja Street, Minsk 220072, Belarus
  • Anatoliy I. Sokolik Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus
  • Natallia L. Pshybytko Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus
  • Ihar I. Smolich Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus
  • Vadim V. Demidchik V. F. Kuprevich Institute of Experimental Botany, National Academy of Sciences of Belarus, 27 Akademichnaja Street, Minsk 220072, Belarus

Keywords:

patch-clamp, Arabidopsis thaliana (L.) Heynh., potassium channels, calcium channels, metal oxide nanoparticles, nanofertilisers
Supporting Agencies
The work was carried out with financial support from the Belarusian Republican Foundation for Fundamental Research within the framework of project B25KI-086 as well as assignment 2.04.5 «Establishing the patterns of toxic effects of metal-containing atmospheric nanopollutants on physiological processes in higher plants» of the state programme of scientific research «Natural resources and environment» for 2021–2025 (state registration No. 20211705).

Abstract

The development and use of environmentally friendly and highly effective forms of fertilisers based on nanoparticles are important subjects in modern plant biology. In this area one of the key problems is the assessment of the impact of metal-containing nanoparticles, such as copper, iron and titanium oxides, on the functioning of membrane ion transport systems in root cells of higher plants. In the present work using the local potential clamp method (patchclamp) the effect of CuO, Fe3O4 and TiO2 nanoparticles on activities of outward-rectifying K+ channels and inward-rectifying Ca2+ channels of the plasma membrane of Arabidopsis thaliana (L.) Heynh. root cells were investigated in detail. It was demonstrated that CuO and TiO2 nanoparticles at a concentration of 300 mg/L inhibited outward K+ currents and inward Ca2+ currents across the plasma membrane, when the time exposure was up to 15 min. With an increase in the exposure time for CuO nanoparticles to 30 min, activation of K+ and Ca2+ currents was recorded, which was probably associated with redox-dependent stimulation of the cation channels. Fe3O4 nanoparticles did not cause changes in the pattern of ionic currents through the plasma membrane of root cells. There were also no effects, when using the corresponding macroparticles (bulk form; more than 1 μm) instead of nanoparticles. Fe3O4 nanoparticles, which do not have membranotropic effects, were tested as growth stimulants in special small-volume cultivation systems. It was shown that these nanoparticles, starting from their level in the medium of 300 mg/L, stimulated growth of A. thaliana. This fact indicates a high potential for their use as nanofertilisers. The obtained data reveal new patterns of the effect of nanomaterials on the ion-transport mechanisms of plant cell membranes, demonstrating significant membranotropic effects of CuO and TiO2 nanoparticles and relative inertness with respect to cell membranes of Fe3O4 nanoparticles.

Author Biographies

  • Palina V. Hryvusevich, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

    PhD (biology); associate professor at the department of plant cell biology and bioengineering, faculty of biology

  • Veranika Ya. Artsisheuskaya, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

    competitor at the department of plant cell biology and bioengineering, faculty of biology

  • Marharyta A. Mysleika, V. F. Kuprevich Institute of Experimental Botany, National Academy of Sciences of Belarus, 27 Akademichnaja Street, Minsk 220072, Belarus

    specialist at the laboratory of plant immunity and biotechnology

  • Anatoliy I. Sokolik, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

    PhD (biology), docent; associate professor at the department of plant cell biology and bioengineering, faculty of biology

  • Natallia L. Pshybytko, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

    PhD (biology), docent; leading researcher at the laboratory of cell and systems biology, department of plant cell biology and bioengineering, faculty of biology

  • Ihar I. Smolich, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

    PhD (biology), docent; leading researcher at the laboratory of cell and systems biology, department of plant cell biology and bioengineering, faculty of biology

  • Vadim V. Demidchik, V. F. Kuprevich Institute of Experimental Botany, National Academy of Sciences of Belarus, 27 Akademichnaja Street, Minsk 220072, Belarus

    doctor of science (biology), сorresponding member of the National Academy of Sciences of Belarus, full professor; chief researcher at the laboratory of plant growth and development

References

  1. Marschner H. Mineral nutrition of higher plants. London: Academic Press; 2012. 651 p.
  2. Nongbet A, Mishra AK, Mohanta YK, Mahanta S, Ray MK, Khan M, et al. Nanofertilizers: a smart and sustainable attribute to modern agriculture. Plants. 2022;11(19):2587. DOI: 10.3390/plants11192587.
  3. Sosan A, Svistunenko D, Straltsova D, Tsiurkina K, Smolich I, Lawson T, et al. Engineered silver nanoparticles are sensed at the plasma membrane and dramatically modify the physiology of Arabidopsis thaliana plants. Plant Journal. 2016;85(2):245–257. DOI: 10.1111/tpj.13105.
  4. el-Zohri M, al-Wadaani NA, Bafeel SO. Foliar sprayed green zinc oxide nanoparticles mitigate drought-induced oxidative stress in tomato. Plants. 2021;10(11):2400. DOI: 10.3390/plants10112400.
  5. Semida WM, Abdelkhalik A, Mohamed GF, Abd El-Mageed TA, Abd El-Mageed SA, Rady MM, et al. Foliar application of zinc oxide nanoparticles promotes drought stress tolerance in eggplant (Solanum melongena L.). Plants. 2021;10(2):421. DOI: 10.3390/plants10020421.
  6. Wang Q, Ebbs SD, Chen Y, Ma X. Trans-generational impact of cerium oxide nanoparticles on tomato plants. Metallomics. 2013;5:753–759. DOI: 10.1039/c3mt00033h.
  7. Margenot AJ, Rippner DA, Dumlao MR, Nezami S, Green PG, Parikh SJ, et al. Copper oxide nanoparticle effects on root growth and hydraulic conductivity of two vegetable crops. Plant Soil. 2018;431:333–345. DOI: 10.1007/s11104-018-3741-3.
  8. Asli S, Neumann PM. Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant, Cell & Environment. 2009;32(5):577–584. DOI: 10.1111/j.1365-3040.2009.01952.x.
  9. Feng Y, Kreslavski VD, Shmarev AN, Ivanov AA, Zharmukhamedov SK, Kosobryukhov A, et al. Effects of iron oxide nanoparticles (Fe3O4) on growth, photosynthesis, antioxidant activity and distribution of mineral elements in wheat (Triticum aestivum) plants. Plants. 2022;11(14):1894. DOI: 10.3390/plants11141894.
  10. Demidchik V. Characterisation of root plasma membrane Ca2+-permeable cation channels: techniques and basic concepts. In: Volkov AG. Plant electrophysiology. Berlin: Springer-Verlag; 2012. p. 339–369.
  11. Ebrahiminezhad A, Zare-Hoseinabadi A, Berenjian A, Ghasemi Y. Green synthesis and characterization of zero-valent iron nanoparticles using stinging nettle (Urtica dioica) leaf extract. Green Processing and Synthesis. 2017;6(5):469–475. DOI: 10.1515/gps-2016-0133.
  12. Palchoudhury S, Jungjohann KL, Weerasena L, Arabshahi A, Gharge U, Albattah A, et al. Enhanced legume root growth with pre-soaking in α-Fe2O3 nanoparticle fertilizer. RSC Advances. 2018;8(43):24075–24083. DOI: 10.1039/c8ra04680h.
  13. Srivastava G, Das CK, Das A, Singh SK, Roy M, Kim H, et al. Seed treatment with iron pyrite (FeS2) nanoparticles increases the production of spinach. RSC Advances. 2014;4:58495–58504. DOI: 10.1039/C4RA06861K.
  14. Li J, Chang PR, Huang J, Wang Y, Yuan H, Ren H. Physiological effects of magnetic iron oxide nanoparticles towards watermelon. Journal of Nanoscience and Nanotechnology. 2013;13(8):5561–5567. DOI: 10.1166/jnn.2013.7533.
  15. Maswada HF, Djanaguiraman M, Prasad PVV. Seed treatment with nano-iron(III) oxide enhances germination, seeding growth and salinity tolerance of sorghum. Journal of Agronomy and Crop Science. 2018;204(6):577–587. DOI: 10.1111/jac.12280.
  16. al-Amri N, Tombuloglu H, Slimani Y, Akhtar S, Barghouthi M, Almessiere M, et al. Size effect of iron(III) oxide nanomaterials on the growth, and their uptake and translocation in common wheat (Triticum aestivum L.). Ecotoxicology and Environmental Safety. 2020;194:110377. DOI: 10.1016/j.ecoenv.2020.110377.
  17. Chen G, Li J, Han H, Du R, Wang X. Physiological and molecular mechanisms of plant responses to copper stress. International Journal of Molecular Sciences. 2022;23(21):12950. DOI: 10.3390/ijms232112950.
  18. Mydy LS, Chigumba DN, Kersten RD. Plant copper metalloenzymes as prospects for new metabolism involving aromatic compounds. Frontiers in Plant Science. 2021;12:692108. DOI: 10.3389/fpls.2021.692108.
  19. Gaucin-Delgado JM, Ortiz-Campos A, Hernandez-Montiel LG, Fortis-Hernandez M, Reyes-Pérez JJ, Gonzáles-Fuentes JA, et al. CuO – NPs improve biosynthesis of bioactive compounds in lettuce. Plants. 2022;11(7):912. DOI: 10.3390/plants11070912.
  20. Abbasirad S, Ghotbi-Ravandi AA. Toxicity of copper oxide nanoparticles in barley: induction of oxidative stress, hormonal imbalance, and systemic resistances. BMC Plant Biology. 2025;25(1):187. DOI: 10.1186/s12870-025-06213-6.
  21. Lyu S, Wei X, Chen J, Wang C, Wang X, Pan D. Titanium as a beneficial element for crop production. Frontiers in Plant Science. 2017;8:597. DOI: 10.3389/fpls.2017.00597.
  22. Skiba E, Pietrzak M, Michlewska S, Gruszka J, Malejko J, Godlewska-Żyłkiewicz B, et al. Photosynthesis governed by nanoparticulate titanium dioxide. The Pisum sativum L. case study. Environmental Pollution. 2024;340(2):122735. DOI: 10.1016/j.envpol.2023.122735.
  23. Demidchik V, Tester M. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiology. 2002;128(2):379–387. DOI: 10.1104/pp.010524.
  24. Demidchik V. Mechanisms and physiological roles of K+ efflux from root cells. Journal of Plant Physiology. 2014;171(9):696–707. DOI: 10.1016/j.jplph.2014.01.015.
  25. Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I. Calcium transport across plant membranes: mechanisms and functions. New Phytologist. 2018;220:49–69. DOI: 10.1111/nph.15266.
  26. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442–446. DOI: 10.1038/nature01485.
  27. Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, et al. Arabidopsis root K+ efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science. 2010;123(9):1468–1479. DOI: 10.1242/jcs.064352.
  28. Angel BM, Batley GE, Jarolimek CV, Rogers NJ. The impact of size on the fate and toxicity of nanoparticulate silver in aquatic systems. Chemosphere. 2013;93(2):359–365. DOI: 10.1016/j.chemosphere.2013.04.096.
  29. Yusefi-Tanha E, Fallah S, Rostamnejadi A, Pokhrel LR. Root system architecture, copper uptake and tissue distribution in soybean (Glycine max (L.) Merr.) grown in copper oxide nanoparticle (CuO-NP)-amended soil and implications for human nutrition. Plants. 2020;9:1326. DOI: 10.3390/plants9101326.
  30. Liu X, Nadeem M, Rui Y. Effects of nanofertilizers on the mechanism of photosynthetic efficiency in plants: a review. Phyton – International Journal of Experimental Botany. 2024;93(12):3197–3216. DOI: 10.32604/phyton.2024.059281.
  31. Kiss T, Osipenko ON. Toxic effects of heavy metals on ionic channels. Pharmacological Reviews. 1994;46(3):245–267.
  32. Nguyen DV, Nguyen HM, Le NT, Nguyen KH, Nguyen HT, Le HM, et al. Copper nanoparticle application enhances plant growth and grain yield in maize under drought stress conditions. Journal of Plant Growth Regulation. 2022;41:364–375. DOI: 10.1007/s00344-021-10301-w.
  33. Linh TMT, Mai NC, Hoe PT, Lien LQ, Ban NK, Hien LTT, et al. Metal-based nanoparticles enhance drought tolerance in soybean. Journal of Nanomaterials. 2020;2020:1–13. DOI: 10.1155/2020/4056563.
  34. Shaw AK, Hossain Z. Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere. 2013;93(6):906–915. DOI: 10.1016/j.chemosphere.2013.05.044.
  35. Hruby MM, Cigler P, Kuzel S. Contribution to understanding the mechanism of titanum action in plants. Journal of Plant Nutrition. 2002;25(3):577–598. DOI: 10.1081/PLN-120003383.
  36. Hong F, Zhou J, Liu C, Yang F, Wu C, Zheng L, et al. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biological Trace Element Research. 2005;105(1–3):269–279. DOI: 10.1385/BTER:105:1–3:269.
  37. Djanaguiraman M, Nair R, Giraldo JP, Prasad PVV. Cerium oxide nanoparticles decrease drought-induced oxidative damage in sorghum leading to higher photosynthesis and grain yield. ACS Omega. 2018;3(10):14406–14416. DOI: 10.1021/acsomega.8b01894.
  38. Zheng L, Hong F, Lu S, Liu C. Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biological Trace Element Research. 2005;105:83–91. DOI: 10.1385/BTER:104:1:083.
  39. Lu CM, Zhang CY, Wu JQ, Tao MX. Research of the effect of nanometer on germination and growth enhancement of Glycine max and its mechanism. Soybean Science. 2002;21:168–172.
  40. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V. Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany. 2014;65:1259 –1270. DOI: 10.1093/jxb/eru004.
  41. Mazaherinia S, Astaraei A, Fotovvat A, Monshi A. Nano iron oxide particles efficiency on Fe, Mn, Zn and Cu concentrations in wheat plant. World Applied Sciences Journal. 2010;7(1):36–40.
  42. Sundaria N, Singh M, Upreti P, Chauhan RP, Jaiswal JP, Kumar A. Seed priming with iron oxide nanoparticles triggers iron acquisition and biofortification in wheat (Triticum aestivum L.) grains. Journal of Plant Growth Regulation. 2018;38:122–131. DOI: 10.1007/s00344-018-9818-7.
  43. Farooqui A, Tabassum H, Ahmad A, Mabood A, Ahmad A, Ahmad IZ. Role of nanoparticles in growth and development of plants: a review. International Journal of Pharmaceutics. 2016;7:22–37. DOI: 10.3389/fpls.2022.976179.
  44. Siddiqi KS, Rahman AU, Tajuddin T, Husen A. Biogenic fabrication of iron/iron oxide nanoparticles and their application. Nanoscale Research Letters. 2016;11(1):498. DOI: 10.1186/s11671-016-1714-0.
  45. Raza MAS, Amin J, Valipour M, Iqbal R, Aslam MU, Zulfiqar B, et al. Cu-nanoparticles enhance the sustainable growth and yield of drought-subjected wheat through physiological progress. Scientific Reports. 2024;14(1):14254. DOI: 10.1038/s41598-024-62680-1.
  46. Rashad YM, El-Sharkawy HHA, Belal BEA, Razik EAS, Galilah DA. Silica nanoparticles as a probable anti-oomycete compound against downy mildew, and yield and quality enhancer in grapevines: field evaluation, molecular, physiological, ultrastructural, and toxicity investigations. Frontiers in Plant Science. 2021;12:763365. DOI: 10.3389/fpls.2021.763365.
  47. Bakhtiari M, Moaveni P, Sani B. The effect of iron nanoparticles spraying time and concentration on wheat. Biological Forum – an International Journal. 2015;7:679–683.

Downloads

Published

2026-02-17

Issue

No. 3 (2025): Experimental Biology and Biotechnology

Section

Physiology and Сell Biology

License

Copyright (c) 2026 Experimental Biology and Biotechnology

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

The authors who are published in this journal agree to the following:

  1. The authors retain copyright on the work and provide the journal with the right of first publication of the work on condition of license Creative Commons Attribution-NonCommercial. 4.0 International (CC BY-NC 4.0).
  2. The authors retain the right to enter into certain contractual agreements relating to the non-exclusive distribution of the published version of the work (e.g. post it on the institutional repository, publication in the book), with the reference to its original publication in this journal.
  3. The authors have the right to post their work on the Internet (e.g. on the institutional store or personal website) prior to and during the review process, conducted by the journal, as this may lead to a productive discussion and a large number of references to this work. (See The Effect of Open Access.)

How to Cite

Hryvusevich, P. V., Artsisheuskaya, V. Y., Mysleika, M. A., Sokolik, A. I., Pshybytko, N. L., Smolich, I. I., & Demidchik, V. V. (2026). Regulation of cation currents through the plasma membrane of root cells of higher plants under the influence of copper, iron and titanium oxide nanoparticles. Experimental Biology and Biotechnology, 3, 4-15. https://doi.org/10.33581/2957-5060-2025-3-%p