Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper
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.
KeywordsAnatomy Barley (Hordeum sativum distichum) Cellular ultrastructure Copper Toxicity
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.
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Conflict of interest
The authors declare that they have no conflict of interest.
- 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.CrossRefGoogle 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
- 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
- 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.Google Scholar
- Methodological Guidelines. (1992). Methodological guidelines on the determination of heavy metals in agricultural soils and crops. Moscow: TsINAO. (in Russian).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.CrossRefGoogle 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
- 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.CrossRefGoogle 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
- 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