Chelated forms of trace elements improve antioxidant properties and nodulation potential of soybean-Bradyrhizobium symbiosis under insufficient water conditions
Keywords:
Glycine max; nodule bacteria; ascorbate peroxidase; superoxide dismutase; water potential; water stress.
Abstract
The development of new nanotechnological approaches and the appearance of preparations with low concentrations of microelements can serve as a basis for promising solutions aimed at increasing stress-protective properties and tolerance to the adverse factors effects. The aim of the study is to show the effectiveness of seed inoculation with nodule bacteria modified by chelate forms of trace elements germanium, ferrum and molybdenum to stimulate antioxidant properties and improve the functioning of the Glycine max (L.) Merr. – Bradyrhizobium symbiosis in insufficient water supply conditions. For this, the symbiotic systems of soybean with active virulent Bradyrhizobium japonicum B1-20 were used with the addition of chelated forms of ferrum, germanium and molybdenum in a dilution of 1:1000 to the culture medium. The chelator was citric acid. At the phenological stages during active nitrogen fixation by soybeans, two models of plant watering regimes were created ̶ optimal at the level of 60% of the full field capacity and insufficient/water stress at the level of 30% of the full field capacity. Microbiological, physiological, and biochemical methods of plant testing were used. It was found that the addition of rhizobia, chelated forms of germanium or ferrum to the culture medium, induces an increase in the antioxidant properties of plants by activating the key enzymatic complexes of superoxide dismutase and ascorbate peroxidase in soybean nodules and leaves under water stress. The use of chelated forms of ferrum or germanium led to the stimulation of the Bradyrhizobium nodulation potential, which was accompanied by the optimization of the water status and growth processes of soybean plants in insufficient moisture supply conditions. It was shown that inoculation with rhizobia containing chelated forms of molybdenum induced soybean plants sensitive to water deficit, as evidenced by an unstable reaction of enzyme activity, decrease or increase, in nodules and leaves. It inhibits nodulation processes on soybean roots and at the same time disrupts the water status of plants with insufficient water supply. It was concluded that the addition of chelated forms of germanium or ferrum to the rhizobia culture medium is a promising solution for stimulating the protective antioxidant properties of soybeans, which helps to optimize the physiological state of plants under insufficient water conditions.References
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Kots, S. Y., Rybachenko, L. I., Khrapova, A. V., Kukol, K. P., Rybachenko, O. R., & Khomenko, Y. O. (2022). Composition of pigment complex in leaves of soybean plants, inoculated by Bradyrhizobium japonicum, subject to metal nanocarboxylates and various-levels of water supply. Biosystems Diversity, 30(1), 80–87.
Kots, S. Y., Rybachenko, L. I., Mamenko, T. P., Kukol, K. P., Pukhtaievych, P. P., & Rybachenko, O. R. (2021). Influence of metal nanocarboxylates and different water supply on efficiency of soybean-rhizobial symbiotic systems. Regulatory Mechanisms in Biosystems, 12(3), 383–390.
Laxa, M., Liebthal, M., Telman, W., Chibani, K., & Dietz, K.-J. (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants, 8(4), 94.
Liu, C., Zhou, H., & Zhou, J. (2021). The applications of nanotechnology in crop production. Molecules, 26(23), 7070.
Mamenko, T. P. (2019). Reaktsiia symbiotychnoho aparatu soi na vtraty vmistu vody u lystkakh i koreniakh, indukovani tryvaloiu diieiu posukhy [The reaction of soybean symbiotic apparatus to losses of water content in leaves and roots, induced by continuous action of drought]. Ecology and Noospherology, 30(1), 44–49 (in Ukrainian).
Mamenko, Т. P. (2021). Regulation of legume-rhizobial symbiosis: Molecular genetic aspects and participation of reactive oxygen species. Cytology and Genetics, 55(5), 447–459.
Morgun, V. V., Kots, S. Y., Mamenko, T. P., Rybachenko, L. I., & Pukhtaievych, P. P. (2021). Regulation of superoxide dismutase activity in soybean plants by inoculating seeds with rhizobia containing nanoparticles of metal carboxylates under conditions of different water supply. Biosystems Diversity, 29(1), 33–38.
Naeem, M., Gill, S. S., Aftab, T., & Tuteja, N. (2024). Editorial: Crop improvement and plant resilience to abiotic stresses. Plant Science, 339, 111958.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxidase is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867–880.
Patra, J. K., & Baek, K.-H. (2017). Antibacterial activity and synergistic antibacterial potential of biosynthesized silver nanoparticles against foodborne pathogenic bacteria along with its anticandidal and antioxidant effects. Frontiers in Microbiology, 8, 167.
Pradhan, S., Patra, P., Das, S., Chandra, S., Mitra, S., Dey, K. K., Akbar, S., Palit, P., & Goswami, A. (2013). Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: A detailed molecular, biochemical, and biophysical study. Environmental Science and Technology, 47(22), 13122–13131.
Prasad, R., Bhattacharyya, A., & Nguyen, Q. D. (2017). Nanotechnology in sustainable agriculture: Recent developments, challenges, and perspectives. Frontiers in Microbiology, 8, 161–171.
Rahimi, D., Kartoolinejad, D., Nourmohammadi, K., & Naghdi, R. (2016). Increasing drought resistance of Alnus subcordata C. A. Mey. seeds using a nano priming technique with multi-walled carbon nanotubes. Journal of Forest Science, 62(6), 269–278.
Schogolev, A. S., & Raievska, I. M. (2021). Role of nitrogen deficiency on growth and development near isogenic by E genes lines of soybean co-inoculated with nitrogen-fixing bacteria. Regulatory Mechanisms in Biosystems, 12(2), 326–334.
Shang, Y., Hasan, M. K., Ahammed, G. J., Li, M., Yin, H., & Zhou, J. (2019). Applications of nanotechnology in plant growth and crop protection: A review. Molecules, 24(14), 2558.
Solanki, P., Bhargava, A., Chhipa, H., Jain, N., & Panwar, J. (2015). Nano-fertilizers and their smart delivery system. In: Rai, M., Ribeiro, C., Mattoso, L., & Duran, N. (Eds.). Nanotechnologies in food and agriculture. Springer International Publishing, Cham. Pp. 81–101.
Taran, N., Batsmanova, L., Kovalenko, M., & Okanenko, A. (2016). Impact of metal nanoform colloidal solution on the adaptive potential of plants. Nanoscale Research Letter, 11, 89.
Wu, J., Wang, X., Wang, Q., Lou, Z., Li, S., Zhu, Y., Qin, L., & Wei, H. (2019). Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes (II). Chemical Society Reviews, 48(4), 1004–1076.
Xie, X., He, Z., Chen, N., Tang, Z., Wang, Q., & Cai, Y. (2019). The roles of environmental factors in regulation of oxidative stress in plant. BioMed Research International, 2019, 9732325.
Xue, Q., Zhu, Z., Musick, J. T., Stewart, B. A., & Dusek, D. A. (2006). Physiological mechanisms contributing to the increased water-use efficiency in winter wheat under deficit irrigation. Journal of Plant Physiology, 162(2), 154–164.
Alscher, R. G., Erturk, N., & Heath, L. S. (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany, 53(372), 1331–1341.
An, C., Sun, C., Li, N., Huang, B., Jiang, J., Shen, Y., Wang, C., Zhao, X., Cui, B., Wang, C., Li, X., Zhan, S., Gao, F., Zeng, Z., Cui, H., & Wang, Y. (2022). Nanomaterials and nanotechnology for the delivery of agrochemicals: Strategies towards sustainable agriculture. Journal of Nanobiotechnology, 20, 11.
Bradford, M. A. (1976). A rapid and sensitive method for the quantization of the microgram quantities of protein utilizing: The principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.
Chhipa, H., & Joshi, P. (2016). Nanofertilisers, nanopesticides and nanosensors in agriculture. In: Ranjan, S., Dasgupta, N., & Lichtfouse, E. (Eds.). Nanoscience in food and agriculture. Springer International Publishing, Cham. Vol. 20. Pp. 247–282.
Dimkpa, C. O., Bindraban, P. S., Fugice, J., Agyin-Birikoran, S., Singh, U., & Hellum, D. (2017). Composite micronutrient nanoparticles and salts decrease drought stress in soybean. Agronomy for Sustainable Development, 37, 5.
Du, W., Tan, W., Peralta-Videa, J. R., Gardea-Torresdey, J. L., Ji, R., Yin, Y., & Guo, H. (2017). Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiology and Biochemistry, 110, 210–225.
Gaonkar, V., & Rosentrater, K. (2019). Soybean. In: Pan, Z., Zhang, R., & Zicari, S. (Eds.). Integrated processing technologies for food and agricultural by-products. Academic Press. Pp. 73–104.
Hasanuzzaman, M., Borhannuddin Bhuyan, M. H. M., Anee, T. I., Parvin, K., Nahar, K., Mahmud, J. A., & Fujita, M. (2019). Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants, 8(9), 384.
Hasanuzzaman, M., Borhannuddin Bhuyan, M. H. M., Zulfiqar, F., Raza, A., Mohsin, S. M., Mahmud, J. A., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants, 9(8), 681.
Hlushach, D. V., & Avksentieva, O. O. (2024). Influence of Bradyrhizobium japonicum on the growth parameters and formation of the assimilation apparatus in E-gene isogenic lines of soybean. Regulatory Mechanisms in Biosystems, 15(1), 131–141.
Javaid, M., Naeem-Ullah, U., Khan, W. S., Saeed, S., Qayyum, M. A., & Khan, M. A. (2020). Role of nanotechnology in crop protection and production: A review. Journal of Innovative Sciences, 6(2), 221–227.
Kaplunenko, V. G., & Kosinov, M. V. (2009). Nadchystyi vodnyi rozchyn nanokarboksylatu metalu [Ultrapure aqueous solution of metal nanocarboxylate]. Patent UA 39397 (in Ukrainian).
Khot, L. R., Sankaran, S., Maja, J. M., Ehsani, R., & Schuster, E. W. (2012). Applications of nanomaterials in agricultural production and crop protection: A review. Crop Protection, 35, 64–70.
Kole, C., Kole, P., Randunu, K. M., Choudhary, P., Podila, R., Ke, P. C., Rao, A. M., & Marcus, R. K. (2013). Nanobiotechnology can boost crop production and quality: First evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). Biotechnology, 13, 37.
Kosinov, M. V., & Kaplunenko, V. H. (2008). Sposib otrymannia ekolohichno chystykh nanochastynok elektroprovidnykh materialiv “elektroimpulsna abliatsiia” [Method of producing ecologically clean nanoparticles of electro-conductive materials “electric impulse ablation”]. Patent UA 37412 (in Ukrainian).
Kots, S. Y., & Vorobei, N. A. (2018). Shtam bakterii Bradyrhizobium japonicum B-7538 dlia oderzhannia bakterialnoho dobryva pid soiu [Bacterial strain Bradyrhizobium japonicum B-7538 for bacterial fertilizer under soybean]. Patent UA 126060 (in Ukrainian).
Kots, S. Y., Morgun, V. V., Patyka, V. P., Datsenko, V. K., Krugova, O. D., Kyrychenko, O. V., Melnykova, N. M., & Mykhalkiv, L. M. (2010). Biologicheskaya fiksaciya azota: Bobovo-rizobialnyj simbioz [Biological fixation of nitrogen: Legume-rhizobium symbiosis]. Logos, Kyiv (in Russian).
Kots, S. Y., Rybachenko, L. I., Khrapova, A. V., Kukol, K. P., Rybachenko, O. R., & Khomenko, Y. O. (2022). Composition of pigment complex in leaves of soybean plants, inoculated by Bradyrhizobium japonicum, subject to metal nanocarboxylates and various-levels of water supply. Biosystems Diversity, 30(1), 80–87.
Kots, S. Y., Rybachenko, L. I., Mamenko, T. P., Kukol, K. P., Pukhtaievych, P. P., & Rybachenko, O. R. (2021). Influence of metal nanocarboxylates and different water supply on efficiency of soybean-rhizobial symbiotic systems. Regulatory Mechanisms in Biosystems, 12(3), 383–390.
Laxa, M., Liebthal, M., Telman, W., Chibani, K., & Dietz, K.-J. (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants, 8(4), 94.
Liu, C., Zhou, H., & Zhou, J. (2021). The applications of nanotechnology in crop production. Molecules, 26(23), 7070.
Mamenko, T. P. (2019). Reaktsiia symbiotychnoho aparatu soi na vtraty vmistu vody u lystkakh i koreniakh, indukovani tryvaloiu diieiu posukhy [The reaction of soybean symbiotic apparatus to losses of water content in leaves and roots, induced by continuous action of drought]. Ecology and Noospherology, 30(1), 44–49 (in Ukrainian).
Mamenko, Т. P. (2021). Regulation of legume-rhizobial symbiosis: Molecular genetic aspects and participation of reactive oxygen species. Cytology and Genetics, 55(5), 447–459.
Morgun, V. V., Kots, S. Y., Mamenko, T. P., Rybachenko, L. I., & Pukhtaievych, P. P. (2021). Regulation of superoxide dismutase activity in soybean plants by inoculating seeds with rhizobia containing nanoparticles of metal carboxylates under conditions of different water supply. Biosystems Diversity, 29(1), 33–38.
Naeem, M., Gill, S. S., Aftab, T., & Tuteja, N. (2024). Editorial: Crop improvement and plant resilience to abiotic stresses. Plant Science, 339, 111958.
Nakano, Y., & Asada, K. (1981). Hydrogen peroxidase is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867–880.
Patra, J. K., & Baek, K.-H. (2017). Antibacterial activity and synergistic antibacterial potential of biosynthesized silver nanoparticles against foodborne pathogenic bacteria along with its anticandidal and antioxidant effects. Frontiers in Microbiology, 8, 167.
Pradhan, S., Patra, P., Das, S., Chandra, S., Mitra, S., Dey, K. K., Akbar, S., Palit, P., & Goswami, A. (2013). Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: A detailed molecular, biochemical, and biophysical study. Environmental Science and Technology, 47(22), 13122–13131.
Prasad, R., Bhattacharyya, A., & Nguyen, Q. D. (2017). Nanotechnology in sustainable agriculture: Recent developments, challenges, and perspectives. Frontiers in Microbiology, 8, 161–171.
Rahimi, D., Kartoolinejad, D., Nourmohammadi, K., & Naghdi, R. (2016). Increasing drought resistance of Alnus subcordata C. A. Mey. seeds using a nano priming technique with multi-walled carbon nanotubes. Journal of Forest Science, 62(6), 269–278.
Schogolev, A. S., & Raievska, I. M. (2021). Role of nitrogen deficiency on growth and development near isogenic by E genes lines of soybean co-inoculated with nitrogen-fixing bacteria. Regulatory Mechanisms in Biosystems, 12(2), 326–334.
Shang, Y., Hasan, M. K., Ahammed, G. J., Li, M., Yin, H., & Zhou, J. (2019). Applications of nanotechnology in plant growth and crop protection: A review. Molecules, 24(14), 2558.
Solanki, P., Bhargava, A., Chhipa, H., Jain, N., & Panwar, J. (2015). Nano-fertilizers and their smart delivery system. In: Rai, M., Ribeiro, C., Mattoso, L., & Duran, N. (Eds.). Nanotechnologies in food and agriculture. Springer International Publishing, Cham. Pp. 81–101.
Taran, N., Batsmanova, L., Kovalenko, M., & Okanenko, A. (2016). Impact of metal nanoform colloidal solution on the adaptive potential of plants. Nanoscale Research Letter, 11, 89.
Wu, J., Wang, X., Wang, Q., Lou, Z., Li, S., Zhu, Y., Qin, L., & Wei, H. (2019). Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes (II). Chemical Society Reviews, 48(4), 1004–1076.
Xie, X., He, Z., Chen, N., Tang, Z., Wang, Q., & Cai, Y. (2019). The roles of environmental factors in regulation of oxidative stress in plant. BioMed Research International, 2019, 9732325.
Xue, Q., Zhu, Z., Musick, J. T., Stewart, B. A., & Dusek, D. A. (2006). Physiological mechanisms contributing to the increased water-use efficiency in winter wheat under deficit irrigation. Journal of Plant Physiology, 162(2), 154–164.
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2024-05-26
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