Peculiarities of soybean-rhizobial systems subject to different levels of water supply fol-lowing treatment with succinic acid and epibrassinolide
Keywords:
drought; symbiotic nitrogen-fixation; cytokinins; zeatin; zeatin riboside; photosynthetic pigments
Abstract
All around the world, one of the leading – according to area of cultivated fields – oleic crops is soybean, which has a high demand for moisture. Given the significance of this crop and negative impact of drought on its yield, integrated research of the influence of insufficient water supply on the intensity of physiological-biochemical processes in those plants is necessary for identifying and understanding the drought-tolerance mechanisms of soybean, as well as symbiotic systems created with its participation, and also for search for ways to adapt it to this stressor. Therefore, our objective was determining the specifics of formation and functioning of the symbiotic systems of soybean and Bradyrhizobium japonicum, following treatment with succinic acid (0.01 g/L) and 24-epibrassinolide (0.00001 g/L), subject to different levels of watering. Our studies revealed that pre-sowing treatment of the seeds with a solution of 24-epibrassinolide with their subsequent inoculation with B. japonicum Т21-2 resulted in the most pronounced stimulation of formation and functioning of the symbiotic systems of soybean in the optimal growing conditions. At the same time, during water shortage, the intensity of nitrogen fixation was the highest in the plants grown from seeds that had been successively treated with the acid and the inoculant. We confirmed that water deficit led to significant increase in the overall content of phytohormones of cytokinin nature in the soybean root nodules, depending on the way the seeds were treated. However, the largest pool of cytokinins was seen in the plants that had been treated with succinic acid against the background of both optimal and insufficient water supply. Treatment of the seeds with 24-epibrassinolide caused significant excess of content of zeatin riboside over the content of zeatin during the flowering stage, whereas in the stage of pods formation it led to an opposite effect – excess of zeatin over zeatin riboside. Fourteen days-long water deficit decreased the content of chlorophylls in the leaves and grain productivity of the plants of all variants of the experiment. The use of growth regulators managed to alleviate the negative impact of stress and protect the pigment complex from ruination. Treatment of the seeds with solutions of succinic acid and 24-epibrassinolide provided the growth of soybean grain productivity regardless on water-supply level. The most efficient was 24-epibrassinolide. Therefore, use of 24-epibrassinolide for pre-sowing treatment of the soybean seeds provided formation of effective symbiotic systems with high nitrogen-fixing activity and caused a number of specific changes in the pattern of accumulation of free and complex forms of cytokinins in the root nodules of those plants. At the same time, the treatment provided the highest concentration of photosynthesis pigments in the soybean leaves, and as a result produced the greatest increase in grain productivity of plants of all the variants, regardless of levels of water supply. In turn, use of succinic acid produced the highest level of nitrogen-fixing activity in the case of the lowest number of root nodules in the conditions of insufficient water supply, and also caused significant accumulation of cytokinins in the nodules, compared with other studied variants against the background of both optimal and insufficient water supply. Therefore, it did result in increase in soybean grain productivity, but this was lower than in the plants treated with 24-epibrassinolide.References
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Bergersen, F. J., & Turner, G. L. (1967). Nitrogen fixation by the fraction of breis of soybean root nodules. Biochimica et Biophysica Acta, 141(3), 507–515.
Collier, R., & Tegeder, M. (2012). Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. The Plant Journal, 72, 355–367.
Croft, H., & Chen, J. M. (2017). Leaf pigment content. Reference Module in Earth Systems and Environmental Sciences, 3, 117–142.
Daryanto, S., Wang, L., & Jacinthe, P. A. (2015). Global synthesis of drought effects on food legume production. PloS One, 10(6), e0127401.
Eleiwa, M. E., Bafeel, S. O., & Ibrahim, S. A. (2011). Influence of brassinosteroids on wheat plant (Triticum aestivum L.) production under salinity stress conditions I-growth parameters and photosynthetic pigments. Australian Journal of Basic and Applied Sciences, 5(5), 58–65.
Ferguson, B. J., & Mathesius, U. (2003). Signaling interactions during nodule development. Journal of Plant Growth Regulation, 22(1), 47–72.
Finan, T. М., Wood, J. M., & Jordan, D. C. (1981). Succinate transport in Rhizobium leguminosarum. Journal of Bacteriology, 148(1), 193–202.
Frederick, J. R., Camp, C. R., & Bauer, P. J. (2001). Drought-stress effects on branch and mainstem seed yield and yield components of determinate soybean. Crop Science, 41(3), 759–763.
Gamas, P., Brault, M., Jardinaud, M. F., & Frugier, F. (2017). Cytokinins in symbiotic nodulation: When, where, what for? Trends in Plant Science, 22(9), 792–802.
Gaspar, Т., Kevers, С., Penel, С., Greppin, Н., Reid, D. M., & Thorpe, T. A. (1996). Plant hormones and plant growth regulators in plant tissue culture. In Vitro Cellular and Developmental Biology – Plant, 32, 272–289.
Ghassemi-Golezani, K., & Lotfi, R. (2012). Response of soybean cultivars to water stress at reproductive stages. International Journal of Plant, Animal and Environmental Sciences, 2, 198–202.
Gil-Quintana, E., Larrainzar, E., Seminario, A., Díaz-Leal, J. L., Alamillo, J. M., Pineda, M., Arrese-Igor, C., Wienkoop, S., & González, E. M. (2013). Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean. Journal of Experimental Botany, 64(8), 2171–2182.
Gruznova, K. A., Bashmakov, D. I., Miliauskienė, J., Vaštakaitė, V., Duchovskis, P., & Lukatkin, A. S. (2018). The effect of a growth regulator Ribav-Extra on winter wheat seedlings exposed to heavy metals. Zemdirbyste-Agriculture, 105(3), 227–234.
Hardy, R. W. F., Holsten, R. D., Jackson, E. K., & Burns, R. C. (1968). The acethylene – ethylene assay for N2 fixation: Laboratory and field evaluation. Plant Physiology, 43, 1185–1207.
Hayat, S., Hasan, S. A., Yusuf, M., Hayat, Q., & Ahmad, A. (2010). Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata. Environmental and Experimental Botany, 69, 105–112.
Heckmann, A. B., Sandal, N., Bek, A. S., Madsen, L. H., Jurkiewicz, A., Nielsen, M. W., Tirichine, L., & Stougaard, J. (2011). Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Molecular Plant-Microbe Interactions, 24(11), 1385–1395.
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Islam, M. S., Muhyidiyn, I., Islam, M. R., Hasan, M. K., Hafeez, A. S. M. G., Hosen, M. M., Saneoka, H., Ueda, A., Liu, L., Naz, M., Barutçular, C., Lone, J., Raza, M. A., Chowdhury, M. K., Sabagh, A. E., & Erman, M. (2022). Soybean and sustainable agriculture for food security. In: Ohyama, T. (Ed.). Soybean – recent advances in research and application. IntechOpen.
Janeczko, A., Gullner, G., Skoczowski, A., Dubert, F., & Barna, B. (2007). Effects of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biologia Plantarum, 51, 355–358.
Jingnan, Z., Hang, Y., Qi, Y., Xijun, J., Lian, C., Mingyao, W., Mengxue, W., Chunyuan, R., & Yuxian, Z. (2021). Physiological and UPLC-MS/MS widely targeted metabolites mechanisms of alleviation of drought stress-induced soybean growth inhibition by melatonin. Industrial Crops and Products, 163, 113323.
Kangasjärvi, S., Neukermans, J., Li, S., Eva-Mari Aro, E.-V., & Noctor, G. (2012). Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany, 63(4), 1619–1636.
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Kots, S. Y., Vorobey, N. A., Kyrychenko, O. V., Melnykova, N. N., Mykhalkiv, L. M., & Pukhtayevych, P. P. (2016). Mikrobiolohichni preparaty dlia sil’s’koho hospodarstva [Microbiological preparations for agriculture]. Logos, Kyiv (in Ukrainian).
Krishna, P., Prasad, B. D., & Rahman, T. (2017). Brassinosteroid аction in рlant аbiotic stress tolerance. Methods in Molecular Biology, 1564, 193–202.
Kumari, A., & Hemantaranjan, A. (2018). Morpho-physiological attributes of Wheat (Triticum aestivum L.) genotypes as influenced by brassinosteroids under heat stress. Journal of Pharmacognosy and Phytochemistry, 7(6), 2111–2115.
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 in Plant Science, 7, 1015.
Larrainzar, E., Molenaar, J. A., Wienkoop, S., Gil-Quintana, E., Alibert, B., Limami, A. M., Arrese-Igor, C., & González, E. M. (2014). Drought stress provokes the down-regulation of methionine and ethylene biosynthesis pathways in Medicago truncatula roots and nodules. Plant, Cell and Environment, 37, 2051–2063.
Lieshchova, M. A., Bilan, M. V., Bohomaz, A. A., Tishkina, N. M., & Brygadyren-ko, V. V. (2020). Effect of succinic acid on the organism of mice and their intestinal microbiota against the background of excessive fat consumption. Regulatory Mechanisms in Biosystems, 11(2), 153–161.
Liu, H., Zhang, C., Yang, J., Yu, N., & Wang, E. (2018). Hormone modulation of legume-rhizobial symbiosis. Journal of Integrative Plant Biology, 60(8), 632–648.
Mahmood, T., Khalid, S., Abdullah, M., Ahmed, Z., Shah, M. K. N., Ghafoor, A., & Du, X. (2020). Insights into drought stress signaling in plants and the molecular genetic basis of cotton drought tolerance. Cells, 9(1), 105.
Mak, M., Babla, M., Xu, S.-C., O’carrigan, A., Liu, X.-H., Gong, Y.-M., Holford, P., & Chen, Z.-H. (2014). Leaf mesophyll K+, H+ and Ca2+ fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean. Environmental and Experimental Botany, 98, 1–12.
Manavalan, L. P., Guttikonda, S. K., Tran, L.-S. P., & Nguyen, H. T. (2009). Physiological and molecular approaches to improve drought resistance in soybean. Plant and Cell Physiology, 50(7), 1260–1276.
Petrychenko, V. F., Lykhochvor, V. V., Ivaniuk, S. V., Korniichuk, O. V., Kolisnyk, S. I., Kobak, S. Y., Zadorozhnyi, V. S., Chornolata, L. P., Kulik, M. F., Obertyuk, Y. V., Voronetska, I. S., Patyka, V. P., Hnatiuk, T. T., Alekseev, O. O., Kalinichenko, A. V., Kots, S. Y., Berehovenko, S. K., & Zakharova, O. M. (2016). Soya [Soybean]. Dilo, Vinnytsia (in Ukrainian).
Rademacher, W. (2015). Plant growth regulators: Backgrounds and uses in plant production. Journal of Plant Growth Regulation, 34, 845–872.
Riyazuddin, R., Nisha, N., Singh, K., Verma, R., & Gupta, R. (2022). Involvement of dehydrin proteins in mitigating the negative effects of drought stress in plants. Plant Cell Reports, 41(3), 519–533.
Sadeghipour, O., & Abbasi, S. (2012). Soybean responses to drought and seed inoculation. World Applied Sciences Journal, 17, 55–60.
Serraj, R. (2003). Effects of drought stress on legume symbiotic nitrogen fixation: Physiological mechanisms. Indian Journal of Experimental Biology, 41(10), 1136–1141.
Serraj, R., Sinclair, T. R., & Purcell, L. C. (1999). Symbiotic N2 fixation response to drought. Journal of Experimental Botany, 50(331), 143–155.
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