Effect of aluminium on redox-homeostasis of common buckwheat (Fagopyrum esculentum)
AbstractCommon buckwheat is a significant culture in Ukraine, whose importance for food security has increased in recent decades. An important biological feature of buckwheat is the ability of the crop to grow on poor and especially acidic soils. Common buckwheat was sown in Ukraine on the area of 125,000 ha in 2020, mainly in the central part of the country and in the soil-climatic zone Polesie in the north of the country. At the same time, the area under buckwheat cultivation has been steadily decreasing in the last decade, which is due to the low profitability of cultivation on mainly acidic soils. The research was conducted in the field conditions during 2012–2018 in Kiev region, as well as in laboratory conditions. ICP analysis and biochemical methods were used. Yield of buckwheat on light soils of low fertility depends largely on the level of acidity of the soil. On acidic sod-podzolic soils with loam substrate, the aluminum content of the layer is 20–40 cm higher, compared to a layer of 0–20 cm. This is probably one of the reasons why, when the concentration of aluminum in the soil profile is increased, the root system is located mainly in the upper layer of soil with a lower content of aluminum. In this case, the study of the mechanisms of resistance to the action of aluminum on acidic soils is an important component of the cost-effectiveness of crop production in the region. In acidic soils with pH < 5.0, phytotoxic aluminum (Al3+) rapidly inhibits root growth and afterwards negatively affects water and nutrient uptake in plants. Acquiring phytotoxic capacities, in this connection Al ions affect a wide range of cellular and molecular processes, with a consequent reduction in plant growth. In most plant species, reactive oxygen species (ROS) production can also be induced by Al toxicity leading to oxidative damage of biomolecules and biological membranes. We have detected an accumulation of Al ions in leaf tissues of treatment plants after 10 days of exposure. Tissues of F. esculentum roots contained 155.4% of control level of Al and tissues of F. esculentum leaves – 186.2% of control level of Al ions. Significant intensification of O2•– generation in roots and leaf tissues as a reaction to Al addition to nutrient solution was detected. Increase in antioxidant enzymes activities and non fixed products of lipids peroxidation was characterized as a biochemical defense reaction of F. esculentum over the 10 days of exposure to Al (50 μM). Thus, the results show that the action of 50 μM of Al ions activated antioxidant enzymes – SOD and CAT and decreased oxidative processes, thus promotes pro/antioxidant balance of common buckwheat. These mechanisms of redox homeostasis can be triggers of morphological changes in buckwheat plants, which lead to increased crop resistance when growing on acidic soils with high aluminum content. Thus, the resistance of culture to acid soils may be associated with the possibility of increased accumulation of aluminum in the plant’s tissues, as well as in changes in redox homeostasis with subsequent morphological changes, and primarily the formation of the root system in the top layer of soil with a reduced content of aluminum.
Asztemborska, M., Steborowski, R., Kowalska, J., & Bystrjewska-Piotrowska, G. (2015). Accumulation of aluminium by plants exposed to nano- and microsized particles of Al2O3. International Journal of Environmental Research, 9(1), 109–116.
Borgo, L., Rabêlo, F. H., Carvalho, G., Ramires, T. G., Righetto, A. J., Piotto, F. A., Boaretto, L. F., & Azevedo, R. A. (2020). Antioxidant performance and aluminum accumulation in two genotypes of Solanum lycopersicum in response to low pH and aluminum availability and under their combined stress. Scientia Horticulturae, 259, e108813.
Daspute, A. A., Sadhukhan, A., Tokizawa, M., Kobayashi, Y., Panda, S. K., & Koyama, H. (2017). Transcriptional regulation of aluminum-tolerance genes in higher plants: Clarifying the underlying molecular mechanisms. Frontiers in Plant Science, 8, 1358.
Ferdinando, M., Brunetti, C., Fini, A., & Tattini, M. (2012). Flavonoids as antioxidants in plants under abiotic stresses. In: Ahmad, P., Prasad, M. N. V. (Eds.). Abiotic stress responses in plants: Metabolism, productivity and sustainability. Springer, New York. Pp. 159–179.
Haling, R. E., Simpson, R. J., Culvenor, R. A., Lambers, H., & Richardson, A. E. (2011). Effect of soil acidity, soil strength and macropores on root growth and morphology of perennial grass species differing in acid-soil resistance. Plant, Cell and Environment, 34(3), 444–456.
Huang, W., Oo, T. L., He, H., Wang, A. Q., Zhan, J., Li, C. Z., Wei, S. Q., & He, L. F. (2014). Aluminum induces rapidly mitochondria-dependent programmed cell death in Al-sensitive peanut root tips. Botanical Studies, 55(1), 67.
Kumar, G. N. M., & Knowles, N. R. (1993). Changes in lipid peroxidation and lipolitic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed-tubers. Plant Physiology, 102, 115–124.
Salazar-Chavarría, V., Sánchez-Nieto, S., & Cruz-Ortega, R. (2020). Fagopyrum esculentum at early stages copes with aluminum toxicity by increasing ABA levels and antioxidant system. Plant Physiology and Biochemistry, 152, 170–176.
Smirnov, O. E., & Taran, N. Y. (2013). Fitotoksychni efekty alyuminiyu ta mekhanizmy alyumorezystentnosti vyshchykh roslyn [Phytotoxic effects of aluminium and aluminium resistance mechanisms of higher plants]. Plant Physiology and Genetics, 45(4), 281–289 (in Ukrainian).
Tamas, L., Huttova, J., & Mistrık, I. (2002). Effect of aluminium on peroxidase activity in roots of Al-sensitive and Al-resistant barley cultivars. Rostlinna Vyroba, 48(2), 76–79.
Taran, N., Batsmanova, L., Kosyk, O., Smirnov, O., Kovalenko, M., Honchar, L., & Okanenko, O. (2016). Colloidal nanomolybdenum influence upon the antioxidative reaction of chickpea plants (Cicer arietinum L.). Nanoscale Research Letters, 11, 476.
Vardar, F., & Ünal, M. (2007). Aluminum toxicity and resistance in higher plants. Advances in Molecular Biology, 1, 1–12.
Yamamoto, Y., Kobayashi, Y., Devi, S. R., Rikiishi, S., & Matsumoto, H. (2002). Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiology, 128, 63–72.
Zhang, L., Xiao, S., Li, W., Feng, W., Li, J., Wu, Z., Gao, X., Liu, F., & Shao, M. (2011). Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. Journal of Experimental Botany, 62(12), 4229–4238.