Fiziol. rast. genet. 2022, vol. 54, no. 6, 498-515, doi:

The content of metabolites in soybeans roots after inoculation seeds of Bradyrhizobium japonicum and treatment with fungicide preparations

Kots S.Ya., Khrapova A.V., Karaushu O.V.

  • Institute of Plant Physiology and Genetics, National Academy of Sciences of Ukraine 31/17 Vasylkivska St., Kyiv, 03022, Ukraine

Plant organisms are constantly affected by external factors of a diverse nature, which can change the course of a number of physiological and biochemical processes, and as a result, be reflected in the growth and development of plants, as well as the realization of their genetic potential. The study of the metabolomic profile of soybean plants against the background of inoculation with rhizobia allows to determine the changes in the biological system caused by the treatment of seeds with fungicides. Therefore, the aim of the work was to analyze the total content of the main groups of low-molecular-weight compounds of soybean roots and to consider their dynamics after seed treatment with the fungicides fever, standak top and inoculation with Bradyrhizobium japonicum 634b. Microbiological, physiological, biochemical and statistical research methods were used. When analyzing the mass spectra of metabolites of soybean roots, it was established that under the action of the fungicides fever and standak top, the growth of polyatomic alcohols occurs in the stages of the primordial and two trifoliate leaves. At the same time, during the formation and active functioning of legume-rhizobial symbiosis (stage of development of two or three tripartite leaves), standak top had a more pronounced effect than fever. It was noted that fungicides during the early stages of soybean development significantly affect the accumulation of organic acids in the roots of plants, leading to a significant increase in their content during the development of the first (under the action of both fungicides) and two trifoliate leaves (under treatment with stand top), which may be due to their involvement in the formation of protective reactions of plants to stressors. A gradual increase in the percentage content of sugars during the growing season of the plants was observed in the variants where the seeds were treated with fever, with the highest content (34.12 %) in the stage of the development of three trifoliate leaves. When treated with standak top, the greatest accumulation of sugars (30.55 %) was in the stage of development of the first trifoliate leaf. We assume that the increase in the percentage of sugars in the total pool of metabolites occurred, in particular, due to the decrease in the percentage content of organic acids. It was shown that the highest content of amino acids was found in control plants and those treated with fever in the stage of the development of two tripartite leaves, which corresponds to the period of active formation of root nodules, increasing their mass and increasing the fixation of atmospheric nitrogen, creating conditions for ensuring the further effective functioning of legume-rhizobial symbiosis. In this way, we found out that the degree and character of severity of the action of fungicides depended on the stage of plant development and the nature of the protectant. The use of fever and standak top caused certain changes in the content of a number of compounds (alcohols, organic acids, sugars and amino acids) during the growing season, which can be considered as components of a complex of reactions to the action of a stress factor and adaptation processes in the plant-bacterial system.

Keywords: Glycine max (L.) Merr., Bradyrhizobium japonicum, metabolites, alcohols, sugars, amino acids, organic acids, fever, standak top

Fiziol. rast. genet.
2022, vol. 54, no. 6, 498-515

Full text and supplemented materials

Free full text: PDF  


1. Shulaev, V., Cortes, D., Miller, G. & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, No. 2, pp. 199-208.

2. Patel, M., Pandey, S., Kumar, M., Haque, M., Pal, S. & Yadav, N. (2021). Plants metabolome study: emerging tools and techniques. Plants, 10, No. 11, 2409.

3. Hong, J., Yang, L., Zhang, D. Shi, J. (2016). Plant metabolomics: an indispensable system biology tool for plant science. International Journal of Molecular Sciences, 17, No 6, 767.

4. Clarke, C.J. & Haselden, J.N. (2008). Metabolic profiling as a tool for understanding mechanisms of toxicity. Toxicologic Pathology, 36, No. 1, pp. 140-147.

5. Prisedsky, Yu.G. & Likholat, Yu.V. (2017). Adaptation of plants to anthropogenic factors. Vinnytsia: Nylan-LTD [in Ukrainian].

6. Bowne, J., Bacic, A., Tester, M. & Roessner, U. (2011). Abiotic stress and metabolomics. Annu Plant Rev, 43, pp. 61-85.

7. Obata, T. & Fernie, A. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences, 69, No. 19, pp. 3225-3243.

8. Levchik, N.Ya., Skripka, G.I., Levon, V.F., Zakrasov, O.V. & Gorbenko, N.E. (2020). Content of biochemical substances in plants Phlox paniculata L. in the conditions of the forest-steppe of Ukraine. Scientific Bulletin of NLTU of Ukraine, 30, No. 2, pp. 19-23 [in Ukrainian].

9. Sartori, F.F., Pimpinato, R.F., Tornisielo, V.L., Engroff, T.D., Jaccoud-Filho, D.S., Menten, J.O., Dorrance, A.E. & Dourado-Neto, D. (2020). Soybean seed treatment: how do fungicides translocate in plants? Pest management science, 76, No. 7, pp. 2355-2359.

10. Amaro, A.C.E., Baron, D., Ono, E.O. & Rodrigues, J.D. (2020). Physiological effects of strobilurin and carboxamides on plants: an overview. Acta Physiologiae Plantarum, 42, No. 4, pp. 212-218.

11. Singh, G. & Sahota, H.K. (2018). Impact of benzimidazole and dithiocarbamate fungicides on the photosynthetic machinery, sugar content and various antioxidative enzymes in chickpea. Plant Physiology and Biochemistry, 132, pp. 166-173.

12. Pavlishche, A.V., Kiriziy, D.A. & Kotz, S.Ya. (2017). Reaction of soybean symbiotic systems to the action of fungicides under different treatment methods. Plant physiology and genetics, 49, No. 3, pp. 237-247 [in Ukrainian].

13. Mamenko, T., Kots, S. & Patyka, V. (2021). Realization of protective and symbiotic properties of soybeans using fungicide seed treatment. Agricultural Science and Practice, 8, No. 2, pp. 24-35.

14. Mostoviak, I.I. & Kravchenko, O.V. (2019). Symbiotic apparatus of soya under the application of different types of fungicides and microbial preparation. Taurian Scientific Herald, 108, pp. 72-77.

15. Gorshkov, A.P., Tsyganova, A.V., Vorobiev, M.G. & Tsyganov V.E. (2020). The fungicide tetramethylthiuram disulfide negatively affects plant cell walls, infection thread walls, and symbiosomes in pea (Pisum sativum L.) symbiotic nodules. Plants, 9, No. 11, 1488 p.

16. Rodrigues, T.F., Bender, F.R., Sanzovo, A.W.S., Ferreira, E., Nogueira, M.A. & Hungria, M. (2020). Impact of pesticides in properties of Bradyrhizobium spp. and in the symbiotic performance with soybean. World Journal of Microbiology and Biotechnology, 36, No. 11, pp. 1-16.

17. Kots, S., Kiriziy, D., Pavlyshche, A. & Rybachenko, L. (2022). Peculiarities of formation and functioning of the soybean - Bradyrhizobium japonicum symbiotic apparatus in relation to photosynthetic activity under the influence of seed protectant. Journal of Microbiology, Biotechnology and Food Sciences, No. 6, e3128.

18. Scandiani, M.M., Luque, A.G., Razori, M.V., Casalini, L.C., Aoki, T., O'Donnell, K., Cervigni, G.D.L. & Spampinato, C.P. (2015). Metabolic profiles of soybean roots during early stages of Fusarium tucumaniae infection. Journal of Experemental Botany, 66, No. 1, pp. 391-402.

19. Biliavska, L.H. & Prysiazhniuk, O.I. (2018). A model of early-maturing soybean variety. Novitni agrotehnologii, 6, pp. 1-15 [in Ukrainian].

20. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A.R. (2006). Gas chromatography mass spectrometry - based metabolite profiling in plants. Nature protocols, 1, No. 1, pp. 387-396.

21. Dolgova, L.G. (2010). Osmotically active substances in the formation of resistance of introduced plants of the genus Chaenomeles Lindl. Issues of bioindication and ecology. Zaporozhye: ZNU, 15, pp. 127-134 [in Russian].

22. Wang, H., Zhang, Y. & Zhou, W. (2018). Mechanism and enhancement of lipid accumulation in filamentous oleaginous microalgae Tribonema minus under heterotrophic condition. Biotechnology for Biofuels and Bioproducts, 11, 328.

23. Blanch, M., Alvarez, I., Sanchez-Ballesta, M.T., Escribano, M. & Merodio, C. (2017). Trisaccharides isomers, galactinol and osmotic imbalance associated with CO2 stress in strawberries. Postharvest Biology and Technology, 131, pp. 84-91.

24. Jia, Q., Kong, D., Li, Q., Sun, S., Song, J., Zhu, Y. & Huang, J. (2019). The function of inositol phosphatases in plant tolerance to abiotic stress. International Journal of Molecular Sciences, 20, No. 16, 3999.

25. Michell, R.H. (2011). Inositol and its derivatives: Their evolution and functions. Advances in Enzyme Regulation, 51, No. 1, pp. 84-90.

26. Loskutov, I.G., Shelenga, T.V., Rodionov, A.V., Khoreva, V.I., Blinova, E.V. & Konarev, A.V. (2019). Application of metabolomic analysis in exploration of plant genetic resources. In Proceedings of the Latvian Academy of Sciences. Section B. Natural Exact and Applied Sciences, 73, No. 6, pp. 494-501.

27. Sultangazina, G.J. (2012). Physiology of plants. Teaching aid (course of lectures). Kostanay: KSU named after A. Baitursynova [in Russian].

28. Patel, T.K. & Williamson, J.D. (2016). Mannitol in plants, fungi, and plant-fungal interactions. Trends in Plant Science, 21, No. 6, pp. 486-497.

29. Kaschuk, G., Kuyper, T.W., Leffelaar, P.A., Hungria, M. & Giller, K.E. (2009). Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biology and Biochemistry, 41, No. 6, pp. 1233-1244.

30. Prudnikova, T.N. & Roslyakov, Yu.F. (1994). Propionic acid in the metabolism of living organisms. Food technology, No. 5-6, pp. 23-27 [in Russian].

31. Couto, C., Silva, L.R., Valentao, P., Velazquez, E., Peix, A. & Andrade, P. (2011). Effects induced by the nodulation with Bradyrhizobium japonicum on Glycine max (soybean) metabolism and antioxidant potential. Food Chemistry, 127, No. 4, pp. 1487-1495.

32. Qualley, A.V., Widhalm, J.R., Adebesin, F., Kish, C.M. & Dudareva, N. (2012). Completion of the core b-oxidative pathway of benzoic acid biosynthesis in plants. Proceedings of the National Academy of Sciences, 109, No. 40. pp. 16383-16388.

33. Petrichenko, V.F., Likhochvor, V.V., Ivanyuk, S.V., Korniychuk, O.V., Kolesnik, S.I., Kobak, S.Ya., Zadorozhny, V.S., Chernolata, L.P. & Zakharova, O.M. (2016). Soy. Vinnytsia: Dilo [in Ukrainian].

34. Das, A., Rushton, P.J. & Rohila, J.S. (2017). Metabolomic profiling of soybeans (Glycine max L.) reveals the importance of sugar and nitrogen metabolism under drought and heat stress. Plants, 6, No. 4, 21.

35. Gardner, K. (2018). What is glucose used for in a plant? Sciencing, 220, pp. 3-13.

36. Nielsen, T., Rung, J. & Villadsen, D. (2004). Fructose-2,6-bisphosphate: a traffic signal in plant metabolism. Trends in Plant Science, 9, No. 11, pp. 556-563.

37. Liu, L., Wang, B. & Liu, D. (2020). Transcriptomic and metabolomic analyses reveal mechanisms of adaptation to salinity in which carbon and nitrogen metabolism is altered in sugar beet roots. BMC Plant Biology, No. 20, 138.

38. Franko, O.L. & Melo, F.R. (2000). Osmoprotectors: plant response to osmotic stress. Plant physiology, 47, No. 1, pp. 152-159 [in Russian].

39. Kolupaev, Yu.E. & Trunova, T.I. (1994). Invertase activity and carbohydrate content in wheat coleoptiles under hypothermic and salt stress. Plant physiology, 41, No. 4, pp. 552-557 [in Russian].

40. Rosa, M., Prado, C., Podazza, G., Interdonato, R., Gonzalez, J.A., Hilal, M. & Prado, F.E. (2009). Soluble sugars - metabolism, sensing and abiotic stress. Plant Signal. Behav, 4, pp. 388-393.

41. Kolupaev, Yu.E. (2010). Fundamentals of plant resistance physiology: a course of lectures. Kharkiv: Miska drukarnya [in Ukrainian].

42. Polyanchikov, S.P. & Kovbel, A.I. (2021). The role of amino acids in protecting crops from stress. Agro Mage [in Ukrainian].

43. Azevedo, R.A., Lancien, M. & Lea, P.J. (2006). The aspartic acid metabolic pathway, an exciting and essential pathway in plants. Amino Acids, 30, No. 2, pp. 143-162.

44. Saradhi, P.P., Alia Arora, S. & Prasad, K.V. (1995). Proline accumulates in plants exposed to UV radiation and protects them against UV-induced peroxidation. Biochemical and biophysical research communications, 209, No. 1, pp. 1-5.

45. Zhang, M., Liu, Y., Shi, H., Guo, M., Chai, M., He, Q., Yan, M., Cao, D., Zhao, L., Cai, H., & Qin, Y. (2018). Evolutionary and expression analyses of soybean basic Leucine zipper transcription factor family. BMC Genomics, 19, 159.