The intensity of ethylene release by soybean plants under the influence of fungicides in the early stages of legume-rhizobial symbiosis

Keywords: Bradyrhizobium japonicum; Glycine max; 1-aminocyclopropane-1-carboxylic acid; symbiotic system.

Abstract

The effect of pre-sowing treatment of soybean seeds with fungicides on the intensity of ethylene release, the processes of nodulation and nitrogen fixation in different symbiotic systems in the early stages of ontogenesis were investigated. The objects of the study were selected symbiotic systems formed with the participation of soybean (Glycine max (L.) Merr.) Diamond variety, strains Bradyrhizobium japonicum 634b (active, virulent) and 604k (inactive, highly virulent) and fungicides Maxim XL 035 PS (fludioxonil, 25 g/L, metalaxyl, 10 g/L), and Standak Top (fipronil, 250 g/L, thiophanate methyl, 225 g/L, piraclostrobin, 25 g/L). Before sowing, the seeds of soybean were treated with solutions of fungicides, calculated on the basis of one rate of expenditure of the active substance of each preparation indicated by the producer per ton of seed. One part of the seeds treated with fungicides was inoculated with rhizobium culture for 1 h (the titre of bacteria was 107 cells/mL). To conduct the research we used microbiological, physiological, biochemical methods, gas chromatography and spectrophotometry. It is found that, regardless of the effectiveness of soybean rhizobial symbiosis, the highest level of ethylene release by plants was observed in the stages of primordial leaf and first true leaf. This is due to the initial processes of nodulation – the laying of nodule primordia and the active formation of nodules on the roots of soybeans. The results show that with the participation of fungicides in different symbiotic systems, there are characteristic changes in phytohormone synthesis in the primordial leaf stage, when the nodule primordia are planted on the root system of plants. In particular, in the ineffective symbiotic system, the intensity of phytohormone release decreases, while in the effective symbiotic system it increases. At the same time, a decrease in the number of nodules on soybean roots inoculated with an inactive highly virulent rhizobia 604k strain due to the action of fungicides and an increase in their number in variants with co-treatment of fungicides and active virulent strain 634b into the stage of the second true leaf were revealed. It was shown that despite a decrease in the mass of root nodules, there is an increase in their nitrogen-fixing activity in an effective symbiotic system with the participation of fungicides in the stage of the second true leaf. The highest intensity of ethylene release in both symbiotic systems was recorded in the stage of the first true leaf, which decreased in the stage of the second true leaf and was independent of the nature of the action of the active substances of fungicides. The obtained data prove that the action of fungicides changes the synthesis of ethylene by soybean plants, as well as the processes of nodulation and nitrogen fixation, which depend on the efficiency of the formed soybean-rhizobial systems and their ability to realize their symbiotic potential under appropriate growing conditions.

References

Bikrol, A., Saxena, N., & Singh, K. (2005). Response of Glycine max in relation to nitrogen fixation as influenced by fungicide seed treatment. African Journal of Biotechnology, 4(7), 667–671.

Breakspear, A., Liu, C., Roy, S., Stacey, N., Rogers, C., Trick, M., Morieri, G., Mysore, K. S., Wen, J., Oldroyd, G. E. D., Downie, J. A., & Murray, J. D. (2014). The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell, 26(12), 4680–4701.

Chan, P. K., Biswas, B., & Gresshoff, P. M. (2013). Classical ethylene insensitive mutants of the Arabidopsis EIN2 orthologue lack the expected “hypernodulation” response in Lotus japonicus. Juornal of Integrative Plant Biology, 55(4), 395–408.

Tsyganova, A. V., & Tsyganov, V. E. (2015). Negativnaya gormonal’naya regulyaczyiya razvitiya simbioticheskikh klben’kov. Soobshhenie I. Etilen. Negative hormonal regulation of symbiotic nodule development. I. Ethylene Sel’skokhozyajstvennaya Biologiya, 50(3), 267–277 (in Russian).

Desbrosses, G. J., & Stougaard, J. (2011). Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host and Microbe, 10(4), 348–358.

Ferguson, B. J., Foo, E., Ross, J. J., & Reid, J. B. (2011). Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytology, 189(3), 829–842.

Fox, J. E., Gulledge, J., Engelhaupt, E., Burow, M. E., & McLachlan, J. A. (2007). Pecticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proceeding of the National Academy of Sciences USA, 104(24), 10282–10287.

Gamalero, E., & Glick, B. R. (2015). Bacterial modulation of plant ethylene levels. Plant Physiology, 169(1), 1–10.

Guan, D., Stacey, N., Liu, C., Wen, J., Mysore, K. S., Torres-Jerez, I., Vernié, T., Tadege, M., Zhou, C., Wang, Z., Udvardi, M. K., Oldroyd, G. E. D., & Murray, J. D. (2013). Rhizobial infection is associated with the development of peripheral vasculature in nodules of Medicago truncatula. Plant Physio¬logy, 162(1), 107–115.

Guerra, J. C. P., Coussens, G., De Keyser, A., De Rycke, R., De Bodt, S., Van de Velde, W., Goormachtig, S., & Holsters, M. (2010). Comparison of develop-mental and stress-induced nodule senescence in Medicago truncatula. Plant Physiology, 152(3), 1574–1584.

Guzmán, P., & Ecker, J. R. (1990). Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2(6), 513–523.

Hardy, R. W. F., Holsten, R. D., Jackson, E. K., & Burns, R. C. (1968). The acety-lene-ethylene assay for nitrogen fixation: Laboratory and field evalution. Plant Physiology, 43(8), 1185–1207.

Hayashi, T., Banba, M., Shimoda, Y., Kouchi, H., Hayashi, M., & Imaizumi-An-raku, H. (2010). A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant Journal, 63(1), 141–154.

Ju, C., Yoon, G. M., Shemansky, J. M., Lin, D. Y., Ying, Z. I., Chang, J., Garrett, W. M., Kessenbrock, M., Groth, G., Tucker, M. L., Cooper, B., Kieber, J. J., & Chang, C. (2012). CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidop¬sis. Proceding of the National Academy of Sciences, 109(47), 19486–19491.

Khatabi, B., & Schäfer, P. (2012). Ethylene in mutualistic symbioses. Plant Signaling and Behavior, 7(12), 1634–1638.

Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, K., Tabata, S., San¬dal, N., Stougaard, J., Webb, K. J., Szczyglowski, K., & Parniske, M. (2005). Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell, 17(8), 2217–2229.

Kots, S. Y., & Hryshchuk, O. O. (2019). Fitohormonalna rehuliatsiia bobovo-ry-zobialnoho symbiozu [Phytohormonal regulation of legume-rhizobial symbiosis]. Fiziologiya Rastenij i Genetika, 51(1), 3–27 (in Ukrainian).

Larrainzar, E., Riely, B. K., Kim, S. C., Carrasquilla-Garcia, N., Yu, H.-J., Hwang, H.-J., Oh, M., Kim, G. B., Surendrarao, A. K., Chasman, D., Siahpirani, A. F., Penmetsa, R. V., Lee, G.-S., Kim, N., Roy, S., Mun, J.-H., & Cook, D. R. (2015). Deep sequencing of the Medicago truncatula root transcriptome reveals a massive and early interaction between nod factor and ethylene signals. Plant Physiology, 169(1), 233–265.

Lee, K. H., & LaRue, T. A. (1992a). Exogenous ethylene inhibits nodulation of Pisum sativum L. cv. Sparkle. Plant Physioljgy, 100(3), 1759–1763.

Lee, K. H., & LaRue, T. A. (1992b). Pleiotropic effects of sym17. A mutation in Pisum sativum L. cv. Sparkle causes decreased nodulation, altered root and shoot growth, and increased ethylene production. Plant Physiology, 100(4), 1326–1333.

Ligero, F., Lluch, C., & Olivares, J. (1986). Evolution of ethylene from roots of Medicago sativa plants inoculated with Rhizobium meliloti. Journal of Plant Physiology, 125(3–4), 361–365.

Lohar, D., Stiller, J., Kam, J., Stacey, G., & Gresshoff, P. M. (2009). Ethylene insensitivity conferred by a mutated Arabidopsis ethylene receptor gene alters nodulation in transgenic Lotus japonicus. Annals of Botany, 104(2), 277–285.

Lopez-Gomez, M., Sandal, N., Stougaard, J., & Boller, T. (2012). Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. Journal of Experimental Botany, 63(1), 393–401.

Ma, W., Guinel, F. C., & Glick, B. R. (2003). Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-carboxylate deaminase promotes nodulation of pea plants. Applied and Environmental Microbiology, 69(8), 4396–4402.

Ma, W., Penrose, D. M., & Glick, B. R. (2002). Strategies used by rhizobia to lower plant ethylene levels and increase nodulation. Canadian Journal of Microbiology, 48(11), 947–954.

Mamenko, T. P., Khomenko, Y. O., & Kots, S. Y. (2019). Influence of fungicides on activities of enzymes of phenolic metabolism in the early stages of formation and functioning of soybean symbiotic apparatus. Regulatory Mechanisms in Biosystems, 10(1), 111–116 (in Ukrainian).

Miyata, K., Kawaguchi, M., & Nakagawa, T. (2013). Two distinct EIN2 genes cooperatively regulate ethylene signaling in Lotus japonicus. Plant Cell Physiology, 54(9), 1469–1477.

Murset, V., Hennecke, H., & Pessi, G. (2012). Disparate role of rhizobial ACC de-aminase in root-nodule symbioses. Symbiosis, 57(1), 43–50.

Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takahashi, K. (2011). From defense to symbiosis: Limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant Journal, 65(2), 169–180.

Nason, M. A., Farrar, J., & Bartlett, D. (2007). Strobilurin fungicides induce changes in photosynthetic gas exchange that do not improve water use efficiency of plants grown under conditions of water stress. Pest Management Science, 63(12), 1191–1200.

Nukui, N., Ezura, H., Yuhashi, K.-I., Yasuta, T., & Minamisawa, K. (2000). Ef¬fects of ethylene precursor and inhibitors for ethylene biosynthesis and perception on nodulation in Lotus japonicus and Macroptilium atropurpureum. Plant Cell Physiology, 41(7), 893–897.

Oldroyd, G. E. D., & Downie J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology, 59(1), 519–546.

Oldroyd, G. E. D., Engstrom, E. M., & Long, S. R. (2001). Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell, 13(8), 1835–1849.

Oldroyd, G. E. D., Murray, J. D., Poole, P. S., & Downie, J. A. (2011). The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Gene¬tics, 45(1), 119–144.

Peck, M. C., Fisher, R. F., & Long, S. R. (2006). Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. Journal of Bacteriology, 188(15), 5417–5427.

Penmetsa, V. P., Uribe, P., Anderson, J., Lichtenzveig, J., Gish, J.-C., Nam, Y. W., Engstrom, E., Xu, K., Sckisel, G., Pereira, M., Baek, J. M., Lopez-Meyer, M., Long, S. R., Harrison, M. J., Singh, K. B., Kiss, G. B., & Cook, D. R. (2008). The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant Journal, 55(40), 580–595.

Prayitno, J. (2010). Root and nodulation phenotypes of the ethylene-insensitive sickle mutant of Medicago truncatula. Hayati Journal of Biosciences, 17(3), 131–136.

Prayitno, J., & Mathesius, U. (2010). Differential regulation of the nodulation zone by silver ions, L-α-(2-amino-ethoxyvinyl)-glycine, and the skl mutation in Medicago truncatula. Hayati Journal of Biosciences, 17(1), 15–20.

Prayitno, J., Imin, N., Rolfe, B. G., & Mathesius, U. (2006). Identification of ethy-lene-mediated protein changes during nodulation in Medicago truncatula using proteome analysis. Journal of Proteome Research, 5(11), 3084–3095.

Prayitno, J., Rolfe, B. G., & Mathesius, U. (2006b). The ethylene-insensitive sick¬le mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiology, 142(1), 168–180.

Schmidt, J. S., Harper, J. E., Hoffman ,T. K., & Bent, A. F. (1999). Regulation of soybean nodulation independent of ethylene signaling. Plant Physiology, 119(3), 951–960.

Standish, J. R., Brenneman, T. B., & Stevenson, K. L. (2018). Dynamics of fungicide sensitivity in Venturia effusa and fungicide efficacy under field conditions. Plant Disease, 102(8), 1606–1611.

Suganuma, N., Yamauchi, H., & Yamamoto, K. (1995). Enhanced production of ethylene by soybean roots after inoculation with Bradyrhizobium japonicum. Plant Science, 111(2), 163–168.

Tamimi, S. M., & Timko, M. P. (2003). Effects of ethylene and inhibitors of ethylene synthesis and action on nodulation in common bean (Phaseolus vulgaris L.). Plant Soil, 257(1), 125–131.

Urao, T., Zamaguchi-Shinozaki, K., & Shinozaki, K. (2000). Two-component systems in plant signal transduction. Trends in Plant Science, 5(2), 67–73.

van Zeijl, A., Op den Camp, R. H. M., Deinum, E. E., Charnikhova, T., Franssen, H., Op den Camp, H. J. M., Bouwmeester, H., Kohlen, W., Bisseling, T., & Geurts, R. (2015). Rhizobium lipo-chitooligosaccharide signaling triggers accumulation of cytokinin in Medicago truncatula roots. Molecular Plant, 8(8), 1213–1226.

Wang, K. L., Li, H., & Ecker, J. R. (2002). Ethylene biosynthesis and signaling networks. The Plant Cell, 12(1), 131–151.

Weller, J. L., Foo, E. M., Hecht, V., Ridge, S., Vander Schoor, J. K., & Reid, J. B. (2015). Ethylene signaling influences light-regulated development in pea. Plant Physiology, 169(1), 115–124.

Xia, X., Ma, C., Dong, S., Xu, Y., & Gong, Z. (2017). Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants. Soil Siences and Plant Nutrition, 63(5), 470–482.

Published
2020-02-22
How to Cite
Mamenko, T. P., Kots, S. Y., & Khomenko, Y. O. (2020). The intensity of ethylene release by soybean plants under the influence of fungicides in the early stages of legume-rhizobial symbiosis . Regulatory Mechanisms in Biosystems, 11(1), 98-104. https://doi.org/10.15421/022014