Advertisement

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

  • Tatiana Minkina
  • Vishnu RajputEmail author
  • Grigory Fedorenko
  • Alexey Fedorenko
  • Saglara Mandzhieva
  • Svetlana Sushkova
  • Tatiana Morin
  • Jun Yao
Original Paper

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.

Keywords

Anatomy Barley (Hordeum sativum distichum) Cellular ultrastructure Copper Toxicity 

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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
  10. Evseev, A. V., & Krasovskaya, T. M. (2017). Toxic metals in soils of the Russian North. Journal of Geochemical Exploration, 174, 128–131.CrossRefGoogle Scholar
  11. 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
  12. 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.CrossRefGoogle Scholar
  13. Halliwell, B., & Gutteridge, J. M. (1984). Oxygen toxicity, oxygen radicals, transition metals and disease. Biochemical Journal, 219, 1–14.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Kopittke, P. M., & Menzies, N. W. (2006). Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant and Soil, 279, 287–296.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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
  22. 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
  23. Kuznetsov, V. V., & Dmitrieva, G. A. (2005). Plant physiology (pp. 248–249). Moscow: Publishing house “Higher school”. (in Russian).Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Marscner, H. (1995). Mineral nutrition of higher plants. London: Academic.Google Scholar
  28. 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
  29. Methodological Guidelines. (1992). Methodological guidelines on the determination of heavy metals in agricultural soils and crops. Moscow: TsINAO. (in Russian).Google Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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
  32. 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
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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
  39. Ouzounidou, G., Eleftheriou, E., & Karataglis, S. (1992). Ecophysiological and ultrastructural effects of copper in Thlaspi ochroleucum (Cruciferae). Canadian Journal of Botany, 70, 947–957.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Prasad, M. N. V. (1999). Heavy metal stress in plants. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.Google Scholar
  55. 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.CrossRefGoogle Scholar
  56. Sommer, A. L. (1931). Copper as an essential for plant growth. Plant Physiology, 6, 339–345.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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
  60. 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
  61. 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.CrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Southern Federal UniversityRostov-on-DonRussia
  2. 2.Southern Scientific Center of Russian Academy of SciencesRostov-on-DonRussia
  3. 3.Environmental Sciences Analytical CenterBrooklyn CollegeBrooklynUSA
  4. 4.China University of GeosciencesBeijingChina

Personalised recommendations