Regulation of superoxide dismutase activity in soybean plants by inoculating seeds with rhizobia containing nanoparticles of metal carboxylates under conditions of different water supply
AbstractSoybean is one of the most profitable advanced crops in agricultural production in Ukraine and the world as a whole. Therefore, studies of means of regulation and increase in the adaptive capacity of soybeans in symbiosis with nodule bacteria under the action of unfavourable environmental factors are relevant and should be aimed at the use of complex bacterial compositions involving modern nanotechnological approaches. Nanocarboxylates of ferrum, molybdenum and germanium metals were used as components of rhizobia inoculation suspension for soybean seed treatment to study the effectiveness of their complex effect on the regulation of the activity of the key antioxidant enzyme superoxide dismutase in plants under drought. Various symbiotic systems were used, which included soybean plants and inoculation suspensions based on the active, virulent Tn5-mutant Bradyrhizobium japonicum B1-20 by adding nanoparticles of ferrum, germanium and molybdenum carboxylates to the culture medium in a ratio of 1: 1000. Citric acid was the chelator. A model drought lasting 14 days was created during the period of active fixation of atmospheric molecular nitrogen by root nodules of soybeans in the budding and flowering stages, by means of controlled watering of plants to 30% of the total moisture content. In the stage of bean formation, watering of plants was resumed to the optimal level – 60% of the total moisture content. The control was soybean plants, the seeds of which were inoculated with a suspension of rhizobia without the addition of chelated metals. The following research methods were used in the work – microbiological, physiological and biochemical. According to the results, it was found that when nanoparticles of carboxylates of ferrum, molybdenum and germanium were added to the inoculation suspension of rhizobia, there was an increase in superoxide dismutase activity in root nodules and a decrease in soybean leaves under optimal water supply conditions of plants. This indicates the initial changes in the activity of the antioxidant enzyme in these symbiotic systems, induced by the influence of chelated metals in combination with the rhizobia of the active Tn5-mutant B. japonicum B1-20. Prolonged drought induced an increase in the overall level of superoxide dismutase activity in soybean nodules and leaves, compared to plants grown under optimal watering conditions. The symbiotic system formed by soybeans and B. japonicum with molybdenum carboxylate nanoparticles was the most sensitive to long-term drought exposure, compared to two other soybean-rhizobial symbioses using ferrum and germanium nanocarboxylates. This was manifested in the unstable reaction of the enzyme to the action of drought – suppression or intensification of the level of its activity in the root nodules and leaves of soybeans inoculated with rhizobia containing molybdenum carboxylate nanoparticles. In symbiotic systems with the participation of germanium and ferrum nanocarboxylates, slight changes were revealed in superoxide dismutase activity in root nodules and leaves of plants during drought and restoration of enzyme activity to the level of plants with optimal watering after water stress. It is concluded that the addition to the culture medium of rhizobia Tn5-mutant B1-20 of nanocarboxylates of germanium or ferrum is an effective means of regulating the activity of the antioxidant enzyme superoxide dismutase in soybean root nodules and leaves, which can contribute to an increase in the protective properties and adaptation of plants to the action of dehydration.
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.
Asensio, A. C., Gil-Monreal, M., Pires, L., Gogorcen, Y., Aparicio-Tejo, P. M., & Moran, J. F. (2012). Two Fe-superoxide dismutase families respond differently to stress and senescence in legumes. Journal of Plant Physiology, 169(13), 1253–1260.
Asensio, A. C., Marino, D., James, E. K., Ariz, I., Arrese-Igor, C., Aparicio-Tejo, P. M., Arredondo-Peter, R., & Moran, J. F. (2011). Expression and localization of a Rhizobium-derived cambialistic superoxide dismutase in pea (Pisum sativum) nodules subjected to oxidative stress. Molecular Plant-Microbe Interactions, 24(10), 1247–1257.
Becana, M., Matamoros, M. A., Udvardi, M., & Dalton, D. A. (2010). Recent insights into antioxidant defenses of legume root nodules. New Phytologist, 188(4), 960–976.
Benedito, V. A., Torres-Jerez, I., Murray, J. D., Andirankaja, A., Allen, S., Kakar, K., Wandrey, M., Verdier, J., Zuber, H., & Ott, T. (2008). A gene expression atlas of the model legume Medicago truncatula. Plant Journal, 55, 504–513.
Bradford, M. A. (1976). Rapid and sensitive method for the quantization of the microgram quantities of protein utilizing: The principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
de Deus, K. E., Lanna, A. C., Abreu, F. R. M., Silveira, R. D. D., Pereira, W. J., Brondani, C., & Vianello, R. P. (2015). Molecular and biochemical characterization of superoxide dismutase (SOD) in upland rice under drought. Australian Journal of Crop Science, 9(8), 744–753.
Du, W, Gardea-Torresdey, J. L., Ji, R., Yin, Y., Zhu, J., Peralta-Videa, J. R., & Guo, H. (2015). Physiological and biochemical changes imposed by CeO2 nanoparticles on wheat: A life cycle field study. Environtal Science Technology, 49(19), 11884–11893.
Foyer, C. H., & Noctor, G. (2005). Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell, 17(7), 1866–1875.
Furlan, A. L., Bianucci, E., Tordable, M. C., Castro, S., & Dietz, K. J. (2014). Antioxidant enzyme activities and gene expression patterns in peanut nodules during a drought and rehydration cycle. Functional Plant Biology, 41(7), 704–713.
Gogorcena, Y., Iturbe-Ormaetxe, I., Escuredo, P. R., & Becana, M. (1995). Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiology, 108(2), 753–759.
Gutiérrez-Martínez, P. B., Torres-Morán, M. I., Romero-Puertas, M. C., Casas-Solís, J., Zarazúa-Villaseñor, P., Sandoval-Pinto, E., & Ramírez-Hernández, B. C. (2020). Assessment of antioxidant enzymes in leaves and roots of Phaseolus vulgaris plants under cadmium stress. Biotecnia, 22(2), 110–118.
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), 1–50.
Ivanova, K. A., & Cygankov, V. E. (2017). Antioksidantnaya sistema zashchity v simbioticheskih kluben’kah bobovyh rastenij [Antioxidant defense system in symbiotic nodules of legumes]. Selskokhozyajstvennaya Biologiya, 52(5), 878–894 (in Russian).
Jaspers, P., & Kangasjärvi, J. (2010). Reactive oxygen species in abiotic stress signaling. Plant Physiology, 138(4), 405–413.
Jebara, S., Jebara, M., Limam, F., & Aouani, M. E. (2005). Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. Plant Physiology, 162, 929–936.
Kaplunenko, V. G., & Kosinov, M. V. (2009). Nadchystyi vodnyi rozchyn nanokarboksylatu metalu [Ultrapure aqueous solution of metal nanocarboxylate]. Patent 39397UA. Publ. 25.02.2009. Bul. 4 (in Ukrainian).
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(1), 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 37412UA. Publ. 25.11.2008. Bul. 22 (in Ukrainian).
Kots, S. Y., Rybachenko, L. I., Pukhtaievych, P. P., & Mokrytskyi, K. A. (2019). Formuvannia ta funktsionuvannia symbiotychnykh system soia – Bradyrhizobium japonicum za vplyvu kompleksiv nanochastynok karboksylativ mikroelementiv [Formation and functioning of symbiotic systems of soybean – Bradyrhizobium japonicum under the influence of complexes of nanoparticles of carboxylates of microelements]. Silskohospodarska Mikrobiolohiia, 29, 12–20 (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 126060 UA. Publ. 11.06.2018. Bul. 11 (in Ukrainian).
Kunert, K. J., Vorster, B. J., Fenta, B. A., Kibido, T., Dionisio, G., & Foyer, C. H. (2016). Drought stress responses in soybean roots and nodules. Frontiers Plant Science, 7, 1015.
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), 1–31.
Mamenko, T. P., Khomenko, Y. O., & Kots, S. I. (2018). Aktyvnist superoksyddysmutazy ta enzymiv askorbat-hlutationovoho tsyklu u symbiotychnykh systemakh Glycine max – Bradyrhizobium japonicum za dii posukhy [Activity of superoxide dismutase and ascorbate-glutathione cycle enzymes in symbiotic systems Glycine max – Bradyrhizobium japonicum under drought]. Mikrobiolohichnyi Zhurnal, 80(3), 77–88 (in Ukrainian).
Matamoros, M. A., Dalton, D. A., Ramos, J., Clemente, M. R., Rubio, M. C., & Becana, M. (2003). Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiology, 133(2), 499–509.
Mhamdi, A., & Van Breusegem, F. (2018). Reactive oxygen species in plant development. Development, 145(15), 1–12.
Moran, J. F., James, E. K., Rubio, M. C., Sarath, G., Klucas, R. V., & Becana, M. (2003). Functional characterization and expression of a cytosolic iron-superoxide dismutase from cowpea root nodules. Plant Physiology, 133(2), 773–782.
Palma, F., López-Gómez, M., Tejera, N. A., & Lluch, C. (2013). Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Science, 208, 75–82.
Pauly, N., Pucciariello, C., Mandon, K., Innocenti, G., Jamet, A., Baudouin, E., Hérouart, D., Frendo, P., & Puppo, A. (2006). Reactive oxygen and nitrogen species and glutathione: Key players in the legume-Rhizobium symbiosis. Journal of Experimental Botany, 57(8), 1769–1776.
Porcel, R., Barea, J. M., & Ruiz-Lozano, J. M. (2003). Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytologist, 157(1), 135–143.
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. Environtal Science Technology, 47(22), 13122–13131.
Raychauhuri, S. S., & Deng, X. W. (2000). The role of superxide dismutase in combating oxidative stress in higher plants. The Botanical Review, 66(1), 89–98.
Rubio, M. C., Becana, M., Sato, S., James, E. K., Tabata, S., & Spaink, H. P. (2007). Characterization of genomic clones and expression analysis of the three types of superoxide dismutases during nodule development in Lotus japonicus. Molecular Plant-Microbe Interactions, 20(3), 262–275.
Rubio, M. C., James, E. K., Clemente, M. R., Bucciarelli, B., Fedorova, M., Vance, C. P., & Becana, M. (2004). Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Molecular Plant-Microbe Interactions, 17(12), 1294–1305.
Santos, R., Hérouart, D., Puppo, A., & Touati, D. (2000). Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Molecular Microbiology, 38(4), 750–759.
Sarker, U., & Oba, S. (2018). Catalase, superoxide dismutase and ascorbate-glutathione cycle enzymes confer drought tolerance of Amaranthus tricolor. Scientific Reports, 8(1), 1–12.
Suzuki, N., Koussevitzky, S., Mittler, R., & Miller, G. (2012). ROS and redox signaling in the response of plants to abiotic stress. Plant, Cell and Environment, 35(2), 259–270.
Talukdar, D., & Talukdar, T. (2013). Superoxide-dismutase deficient mutants in common beans (Phaseolus vulgaris L.): Genetic control, differential expressions of isozymes, and sensitivity to arsenic. Biomed Research International, 372, 782450.
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), 1–6.
Tejera, N. A., Campos, R., Sanjuán, J., & Lluch, C. (2004). Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. Plant Physiology, 161(3), 329–338.
Tyagi, S., Sharma, S., Taneja, M., Shumayla, Kumar, R., Sembi, J. K., & Upadhyay, S. K. (2017). Superoxide dismutases in bread wheat (Triticum aestivum L.): Comprehensive characterization and expression analysis during development and, biotic and abiotic stresses. Agri Gene, 6, 1–13.
Tyagi, S., Shumayla, Madhu, Singh, K., & Upadhyay, S. K. (2021). Molecular characterization revealed the role of catalases under abiotic and arsenic stress in bread wheat (Triticum aestivum L.). Journal of Hazardous Materials, 403, 123585.
Udvardi, M. K., & Poole, P. S. (2013). Transport and metabolism in legume-Rhizobia symbioses. Annual Review of Plant Biology, 64(1), 781–808.
Wisniewski, J. P., Rathbun, E. A., Knox, J. P., & Brewin, N. J. (2000). Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: Implications for pea nodule initiation by Rhizobium leguminosarum. Molecular Plant-Microbe Interactions, 13(4), 413–420.
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.