Skip to main content
Log in

Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper

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

Abstract

Effects of Cu toxicity from contaminated soil were analysed in spring barley (Hordeum sativum distichum), a widely cultivated species in South Russia. In this study, H. sativum was planted outdoors in one of the most fertile soils—Haplic Chernozem spiked with high concentration of Cu and examined between the boot and head emergence phase of growth. Copper toxicity was observed to cause slow ontogenetic development of plants, changing their morphometric parameters (shape, size, colour). To the best of our knowledge, the ultrastructural changes in roots, stems and leaves of H. sativum induced by excess Cu were fully characterized for the first time using transmission electron microscopy. The plant roots were the most effected, showing degradation of the epidermis, reduced number of parenchyma cells, as well as a significant decrease in the diameter of the stele and a disruption and modification to its cell structure. The comparative analysis of the ultrastructure of control plants and plants exposed to the toxic effects of Cu has made it possible to reveal significant disruption of the integrity of the cell wall and cytoplasmic membranes in the root with deposition of electron-dense material. The changes in the ultrastructure of the main cytoplasmic organelles—endoplasmic reticulum, mitochondria, chloroplasts and peroxisomes—in the stem and leaves were found. The cellular Cu deposition, anatomical and ultrastructural modifications could mainly account for the primary impact points of metal toxicity. Therefore, this work extends the available knowledge of the mechanisms of the Cu effect tolerance of barley.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Ali, N. A., Ater, M., Sunahara, G. I., & Robidoux, P. Y. (2004). Phytotoxicity and bioaccumulation of copper and chromium using barley (Hordeum vulgare L.) in spiked artificial and natural forest soils. Ecotoxicology and Environmental Safety,57, 363–374.

    CAS  Google Scholar 

  • Arduini, I., Godbold, D. L., & Onnis, A. (1995). Influence of copper on root growth and morphology of Pinus pinea L. and Pinus pinaster Ait. seedlings. Tree Physiology,15, 411–415.

    CAS  Google Scholar 

  • Arendt, E. K., & Zannini, E. (2013). Cereal grains for the food and beverage industries, Barley: A volume in woodhead publishing series in food science, technology and nutrition, (pp. 155–200). https://doi.org/10.1533/9780857098924.155.

    Book  Google Scholar 

  • Baker, D. E., & Senef, J. P. (1995). Copper. In B. J. Alloy (Ed.), Heavy metals in soils (pp. 179–205). London: Blackie Academic and Professional.

    Google Scholar 

  • Boyd, R., Barnes, S. J., De Caritat, P., Chekushin, V. A., Melezhik, V. A., Reimann, C., et al. (2009). Emissions from the copper–nickel industry on the Kola Peninsula and at Noril’sk, Russia. Atmospheric Environment,43, 1474–1480.

    CAS  Google Scholar 

  • Brun, L. A., Maillet, J., Richarte, J., Herrmann, P., & Remy, J. C. (1998). Relationships between extractable copper, soil properties and copper uptake by wild plants in vineyard soils. Environmental Pollution,102, 151–161.

    CAS  Google Scholar 

  • Brune, A., Urbach, W., & Dietz, K. (1995). Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: A comparison of Cd-, Mo-, Ni- and Zn-stress. New Phytologist,129, 403–409.

    CAS  Google Scholar 

  • Chibber, S., Ansari, S. A., & Satar, R. (2013). New vision to CuO, ZnO, and TiO2 nanoparticles: Their outcome and effects. Journal of Nanoparticle Research,15, 1–13.

    Google Scholar 

  • de Freitas, T. A., França, M. G., de Almeida, A. A., de Oliveira, S. J., de Jesus, R. M., Souza, V. L., et al. (2015). Morphology, ultrastructure and mineral uptake is affected by copper toxicity in young plants of Inga subnuda subs. luschnathiana (Benth.) T.D. Penn. Environmental Science and Pollution Research,22, 15479–15494.

    Google Scholar 

  • Evseev, A. V., & Krasovskaya, T. M. (2017). Toxic metals in soils of the Russian North. Journal of Geochemical Exploration,174, 128–131.

    CAS  Google Scholar 

  • Fedorenko, G. M., Fedorenko, A. G., Minkina, T. M., Mandzhieva, S. S., Rajput, V. D., Usatov, A. V., et al. (2018). Method for hydrophytic plant sample preparation for light and electron microscopy (studies on Phragmites australis Cav.). MethodsX,5, 1213–1220.

    Google Scholar 

  • Guo, G., Yuan, T., Wang, W., Li, D., Cheng, J., Gao, Y., et al. (2011). Bioavailability, mobility, and toxicity of Cu in soils around the Dexing Cu mine in China. Environmental Geochemistry and Health,33, 217–224.

    CAS  Google Scholar 

  • Halliwell, B., & Gutteridge, J. M. (1984). Oxygen toxicity, oxygen radicals, transition metals and disease. Biochemical Journal,219, 1–14.

    CAS  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, 259–266.

    Google Scholar 

  • Hou, W., Chen, X., Song, G., Wang, Q., & Chang, C. C. (2007). Effects of copper and cadmium on heavy metal polluted waterbody restoration by duckweed (Lemna minor). Plant Physiology and Biochemistry,45, 62–69.

    CAS  Google Scholar 

  • Jarvi, S., Gollan, P. J., & Aro, E. M. (2013). Understanding the roles of the thylakoid lumen in photosynthesis regulation. Frontiers in Plant Science,4, 434.

    Google Scholar 

  • Kennedy, C. D., & Gonsalves, F. A. N. (1989). The action of divalent Zn, Cd, Hg, Cu, and Pb ions on the ATPase activity of a plasma membrane fraction isolated from roots of Zea mays. Plant and Soil,117, 167–175.

    CAS  Google Scholar 

  • Kessler, F., & Vidi, P. A. (2007). Plastoglobule lipid bodies: Their functions in chloroplasts and their potential for applications. Advances in Biochemical Engineering/Biotechnology,107, 153–172.

    CAS  Google Scholar 

  • Kopittke, P. M., & Menzies, N. W. (2006). Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant and Soil,279, 287–296.

    CAS  Google Scholar 

  • Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F. (2006). World map of the Köppen–Geiger climate classification updated. Meteorologische Zeitschrift,15(3), 259–263.

    Google Scholar 

  • Krämer, U., & Clemens, S. (2006). Functions and homeostasis of zinc, copper, and nickel in plants. In M. J. Tamás & E. Martinoia (Eds.), Molecular biology of metal homeostasis and detoxification (pp. 215–271). Berlin, Heidelberg: Springer.

    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 

  • Kuznetsov, V. V., & Dmitrieva, G. A. (2005). Plant physiology (pp. 248–249). Moscow: Publishing house “Higher school”. (in Russian).

    Google Scholar 

  • Lee, J. S., Chon, H. T., & Kim, K. W. (2005). Human risk assessment of As, Cd, Cu and Zn in the abandoned metal mine site. Environmental Geochemistry and Health,27, 185–191.

    CAS  Google Scholar 

  • Long, J., Tan, D., Deng, S., & Lei, M. (2018). Uptake and accumulation of potentially toxic elements in colonized plant species around the world’s largest antimony mine area, China. Environmental Geochemistry and Health,40, 2383–2394.

    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.

    CAS  Google Scholar 

  • Marscner, H. (1995). Mineral nutrition of higher plants. London: Academic.

    Google Scholar 

  • McVay, I. R., Maher, W. A., Krikowa, F., & Ubrhien, R. (2018). 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. https://doi.org/10.1007/s10653-018-0215-8.

    Article  Google Scholar 

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

    Google Scholar 

  • Michaud, A. M., Bravin, M. N., Galleguillos, M., & Hinsinger, P. (2007). Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils. Plant and Soil,298, 99–111.

    CAS  Google Scholar 

  • Minkina, T., Fedorenko, G., Nevidomskaya, D., Fedorenko, A., Chaplygin, V., & Mandzhieva, S. (2018). Morphological and anatomical changes of Phragmites australis Cav. due to the uptake and accumulation of heavy metals from polluted soils. Science of the Total Environment,636, 392–401.

    CAS  Google Scholar 

  • Minkina, T. M., Linnik, V. G., Nevidomskaya, D. G., Bauer, T. V., Mandzhieva, S. S., & Khoroshavin, V. Y. (2017). Forms of Cu (II), Zn (II), and Pb (II) compounds in technogenically transformed soils adjacent to the Karabashmed copper smelter. Journal of Soils and Sediments,6, 2229–2230.

    Google Scholar 

  • Minkina, T. M., Motusova, G. V., Mandzhieva, S. S., & Nazarenko, O. G. (2012). Ecological resistance of the soil-plant system to contamination by heavy metals. Journal of Geochemical Exploration,123, 33–40.

    CAS  Google Scholar 

  • Minkina, T. M., Motuzova, G. V., Nazarenko, O. G., Kryshchenko, V. S., & Mandzhieva, S. S. (2008). Forms of heavy metal compounds in soils of the steppe zone. Eurasian Journal of Soil Science,41, 708–716.

    Google Scholar 

  • Nevidomskaya, D. G., Sushkova, S. N., Sherstnev, A. K., & Zamulina, I. V. (2017). Content and distribution of heavy metals in herbaceous plants under the effect of industrial aerosol emissions. Journal of Geochemical Exploration,174, 113–120.

    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.

    CAS  Google Scholar 

  • Oorts, K., Bronckaers, H., & Smolders, E. (2009). Discrepancy of the microbial response to elevated copper between freshly spiked and long-term contaminated soils. Environmental Toxicology and Chemistry,25, 845–853.

    Google Scholar 

  • Otabbong, E., Sadovnikova, L., Lakimenko, O., Nilsson, I., & Persson, J. (1997). Sewage sludge: Soil conditioner and nutrient source II. Availability of Cu, Zn, Pb and Cd to barley in a pot experiment. Acta Agriculturae Scandinavica, Section B—Soil and Plant Science,47, 65–70.

    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.

    CAS  Google Scholar 

  • Paton, G. I., Viventsova, E., Kumpene, J., Wilson, M. J., Weitz, H. J., & Dawson, J. J. (2006). An ecotoxicity assessment of contaminated forest soils from the Kola Peninsula. Science of the Total Environment,355, 106–117.

    CAS  Google Scholar 

  • Peng, C., Duan, D., Xu, C., Chen, Y., Sun, L., Zhang, H., et al. (2015). Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environmental Pollution,197, 99–107.

    CAS  Google Scholar 

  • Peng, H. Y., Yang, X. E., & Tian, S. K. (2005). Accumulation and ultrastructural distribution of copper in Elsholtzia splendens. Journal of Zhejiang University Science B,6, 311–318.

    Google Scholar 

  • Pérez-Harguindeguy, N., Díaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P., et al. (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany,61, 167–234.

    Google Scholar 

  • Poschenrieder, C., Bech, J., Llugany, M., Pace, A., Fenes, E., & Barceló, J. (2001). Copper in plant species in a copper gradient in Catalonia (North East Spain) and their potential for Phytoremediation. Plant and Soil,230, 247–256.

    CAS  Google Scholar 

  • Prasad, M. N. V. (1999). Heavy metal stress in plants. Berlin, Heidelberg: Springer.

    Google Scholar 

  • Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C., & O’Halloran, T. V. (1999). Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase. Science,284, 805–808.

    CAS  Google Scholar 

  • Rajput, V., Minkina, T., Fedorenko, A., Sushkova, S., Mandzhieva, S., Lysenko, V., et al. (2018a). Toxicity of copper oxide nanoparticles on spring barley (Hordeum sativum distichum). Science of the Total Environment,645, 1103–1113.

    CAS  Google Scholar 

  • Rajput, V. D., Minkina, T., Sushkova, S., Tsitsuashvili, V., Mandzhieva, S., Gorovtsov, A., et al. (2018b). Effect of nanoparticles on crops and soil microbial communities. Journal of Soils and Sediments,18(6), 2179–2187.

    CAS  Google Scholar 

  • Rajput, V. D., Minkina, T., Suskova, S., Mandzhieva, S., Tsitsuashvili, V., Chapligin, V., et al. (2018c). Effect of copper nanoparticles (CuO NPs) on crop plants a mini review. BioNanoScience,8, 36–42.

    Google Scholar 

  • Rajput, V. D., Minkina, T. M., Behal, A., Sushkova, S. N., Mandzhieva, S., Singh, R., et al. (2018d). Effects of zinc-oxide nanoparticles on soil, plants, animals and soil organisms: A review. Environmental Nanotechnology, Monitoring and Management,9, 76–84.

    Google Scholar 

  • Rottet, S., Besagni, C., & Kessler, F. (2015). The role of plastoglobules in thylakoid lipid remodeling during plant development. Biochimica et Biophysica Acta,1847, 889–899.

    CAS  Google Scholar 

  • Ruyters, S., Salaets, P., Oorts, K., & Smolders, E. (2013). Copper toxicity in soils under established vineyards in Europe: A survey. Science of the Total Environment,443, 470–477.

    CAS  Google Scholar 

  • Seneviratne, M., Rajakaruna, N., Rizwan, M., Madawala, H., Ok, Y. S., & Vithanage, M. (2017). Heavy metal-induced oxidative stress on seed germination and seedling development: A critical review. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-017-0005-8.

    Article  Google Scholar 

  • Smolders, E., Buekers, J., Oliver, I., & McLaughlin, M. J. (2009). Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environmental Toxicology and Chemistry,23, 2633–2640.

    Google Scholar 

  • Sommer, A. L. (1931). Copper as an essential for plant growth. Plant Physiology,6, 339–345.

    CAS  Google Scholar 

  • Taylor, G. J., & Foy, C. D. (1985). Differential uptake and toxicity of ionic and chelated copper in Triticum aestivum. Canadian Journal of Botany,63, 1271–1275.

    CAS  Google Scholar 

  • Upadhyay, R. K., & Panda, S. K. (2009). Copper-induced growth inhibition, oxidative stress and ultrastructural alterations in freshly grown water lettuce (Pistia stratiotes L.). Comptes Rendus Biologies,332, 623–632.

    CAS  Google Scholar 

  • US-EPA. (1993). Standards for the use or disposal of sewage sludge; final rules (40 CFR Parts 257, 403 and 503). Federal Register,58, 9248–9415.

    Google Scholar 

  • Verkleij, J. A. C., & Schat, H. (1990). Mechanisms of metal tolerance in higher plants. In A. J. Shaw (Ed.), Heavy metal tolerance in plants: Evolutionary aspects (pp. 179–193). Boca Raton: CRC Press.

    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.

    Google Scholar 

  • Wang, X., Ma, R., Cui, D., Cao, Q., Shan, Z., & Jiao, Z. (2017). Physio-biochemical and molecular mechanism underlying the enhanced heavy metal tolerance in highland barley seedlings pre-treated with low-dose gamma irradiation. Scientific Reports,7, 4233.

    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.

    CAS  Google Scholar 

  • Žaltauskaitė, J., & Šliumpaitė, I. (2013). Evaluation of toxic effects and bioaccumulation of cadmium and copper in spring barley (Hordeum vulgare L.). Environmental Research, Engineering and Management,64, 51–58.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the Ministry of Education and Science of Russia, Project No. 5.948.2017/PCh and Russian Academy of Sciences, Project No. AAAA-A19-119011190176-7.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vishnu Rajput.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Minkina, T., Rajput, V., Fedorenko, G. et al. Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper. Environ Geochem Health 42, 45–58 (2020). https://doi.org/10.1007/s10653-019-00269-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-019-00269-8

Keywords

Profiles

  1. Vishnu Rajput