Key role of phenol enzymes metabolism in the legume-rhizobial symbiosis under different water supply regimes
Keywords:
Glycine max (L.) Merr.; Bradyrhizobium japonicum; polyphenol oxidases; guaiacol peroxidase; phenylalanine ammonia lyase; symbiotic system; strain.
Abstract
The legume-rhizobium interaction induces formation of specific reactions that take metabolism in the host plant up to a new functional level, increasing its tolerance to unfavourable cultivation conditions. Our objective was to study the participation of key enzymes – phenylalanine ammonia lyase, guaiacol peroxidase, and polyphenol oxidases – in the phenol-metabolism processes and synthesis of a broad spectrum of secondary metabolites in soybean plants that have established symbiotic interactions with rhizobia of varying effectiveness during optimal and insufficient water supplies. In our studies, we used symbiotic systems of soybean and rhizobia (Bradyrhizobium japonicum) that varied in efficiency and virulence. In the period of active nitrogen fixation by soybean, from the third-true-leaf stage until budding, we created different water-supply regimes for the plants, including optimal watering at the level of 60% of full field capacity (control) and insufficient, at the level of 30% (drought). When the soybean was flowering, we recovered the optimal level of water supply (resumed watering). In the studies, we employed microbiological, biochemical, and physiological approaches. We determined the specificity of how key enzymes of the phenol metabolism such as phenylalanine ammonia lyase, polyphenol oxidase and guaiacol peroxidase in the nodules, roots, and leaves of the soybean reacted to different levels of water supply, depending on the functional efficiency of the symbiotic system involving strains of B. japonicum, varying in effectiveness and virulence. In the effective soybean-rhizobium symbiosis, there occurred insignificant changes in the activity of phenol-metabolism enzymes in the nodules, roots, and leaves during drought and after action of the stress. This evidence is that in symbiosis with effective rhizobia B1-20, soybean could realize its own defensive systems that regulate optimal functioning of phenol metabolism in dehydration conditions. In the low-effective 107 and ineffective 604k symbiotic systems of soybean, there was observed unstable dynamics of the activity of enzymes in leaves and roots, manifested in intensification or inhibition of their activity levels during drought or post-stress period. This indicates malfunctioning of the processes associated with phenol metabolism in the soybean plants. We concluded that tolerance of legume-rhizobium symbiosis to water deprivation depends on mutual involvements of the both symbiotic partners – host plant and rhizobia, their ability to fully realize the defensive systems for activation of the key enzymatic complexes taking part in regulation of phenol metabolism in plants.References
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Alunni, S., Cipiciani, A., Fioroni, G., & Ottavi, L. (2003). Mechanisms of inhibition of phenylalanine ammonia-lyase by phenol inhibitors and phenol/glycine synergistic inhibitors. Archives of Biochemistry and Biophysics, 412(2), 170–175.
Araji, S., Grammer, T. A., & Gertzen, R. (2014). Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiolоgy, 164(3), 1191–1203.
Bradford, M. (1976). A rapid and sensitive method for the quantitation of the microgram quantities of protein utilizing: the principle of protein – dye binding. Analytical Biochemistry, 72, 248–254.
Cerezini, P., Riar, M. K., & Sinclair, T. R. (2016). Transpiration and nitrogen fixation recovery capacity in soybean following drought stress. Journal of Crop Improvement, 30, 562–571.
Chen, H., & Vierling, R. A. (2000). Molecular cloning and characterization of soybean peroxidase gene families. Plant Science, 150(2), 129–137.
Chon, S.-U. (2013). Total polyphenols and bioactivity of seeds and sprouts in several legumes. Current Pharmaceutical Desing, 19(34), 6112–6124.
Cosme, P., Rodríguez, A. B., Espino, J., & Garrido, M. (2020). Plant phenolics: Bioavailability as a key determinant of their potential health-promoting applications. Antioxidants, 9(12), 1263.
Damiani, I., Pauly, N., Puppo, A., Brouquisse, R., & Boscar, A. (2016). Reactive oxygen species and nitric oxide control early steps of the legume – Rhizobium symbiotic. Frontiers in Plant Science, 7, 454.
Dicko, M. H., Gruppen, H., Traore, A. S., Voragen, A. G. J., & Berkel, W. J. H. (2006). Phenolic compounds and related enzymes as determinants of sorghum for food use. Biotechnology and Molecular Biology Review, 1(1), 21–38.
Egley, G. H., Paul, R. N., Vaughn, K. C., & Duke, S. O. (1983). Role of peroxidase in the development of water impermeable seed coats in Sida sprinosa L. Planta, 157(1), 224–232.
Fan, L., Shi, G., Yang, J., Liu, G., Niu, Z., Ye, W., Wu, S., Wang, L., & Guan, Q. A. (2022). Protective role of phenylalanine ammonia-lyase from Astragalus membranaceus against saline-alkali stress. International Journal of Molecular Sciences, 23(24), 15686.
Gaonkar, V., & Rosentrater, K. (2019). Soybean. In: Pan, Z., Zhang, R., Zicari, S. (Eds.). Integrated processing technologies for food and agricultural by-products. Elsevier Inc. Pp. 73–104.
Gho, Y. S., Kim, S. J., & Jung, K. H. (2019). Phenylalanine ammonia-lyase family is closely associated with response to phosphate deficiency in rice. Genes and Genomics, 42(1), 67–76.
Gourion, B., Berrabah, F., Ratet, P., & Stacey, G. (2015). Rhizobium-legume symbioses: The crucial role of plant immunity. Trends Plant Science, 20(3), 186–194.
Hawkins, J., & Oresnik, I. (2021). The Rhizobium-legume symbiosis: Co-opting successful stress management. Front Plant Sciences, 12, 796045.
Jun, S. Y., Sattler, S. A., Cortez, G. S., Vermerris, W., Sattler, S. E., & Kang, C. H. (2018). Biochemical and structural analysis of substrate specificity of a phenylalanine ammonia-lyase. Plant Physiology, 176(2), 1452–1468.
Keet, J.-H., Ellis, A. G., Hui, C., & Le Roux, J. J. (2017). Legume-Rhizobium symbiotic promiscuity and effectiveness do not affect plant invasiveness. South African Journal of Botany, 109, 341.
Khatun, M., Sarkar, S., Era, F., Islam, A., Anwar, M., Fahad, S., Datta, R., & Islam, A. (2021). A drought stress in grain legumes: Effects, tolerance mechanisms and management. Agronomy, 11(12), 2374.
Kots, S. Y., & Hryschuk, O. O. (2019). Fitohormonal’na rehuliatsija bobovo-ryzobial’noho symbiozu [Phytohormonal regulation of legume-rhizobial symbiosis]. Fyzyolohyia Rastenyi y Henetyka, 51(1), 1–27 (in Ukrainian).
Kots, S. Y., Morgun, V. V., & Patykа, V. F. (2010). Biologicheskaya fiksacija azota: Bobovo-rizobialnyj symbioz [Biological fixation of nitrogen: Legume-rhizobium symbiosis]. Logos, Kyiv (in Ukrainian).
Kuvalekar, A., Redkar, A., Gandhe, K., & Harsulkar, A. (2011). Peroxidase and polyphenol oxidase activities in compatible host–pathogen interaction in Jasminum officinale and Uromyces hobsoni: Insights into susceptibility of host. New Zealand Journal of Botany, 49(3), 351–359.
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.
Mamenko, Т. (2021). Regulation of legume-rhizobial symbiosis: Molecular genetic aspects and participation of reactive oxygen species. Cytology and Genetics, 55(5), 447–459.
Mamenko, Т. P., Kots, S. Y., Mykhalkiv, L. M., & Homenko, Y. A. (2021). Phenylalanine ammonia-lyase enzyme activity in the symbiotic system Glycine max – Bradyrhizobium japonicum by seed inoculation different in activity and virulation strain and treatment with fungicides. Mikrobiologichnyi Zhurnal, 83(4), 63–73.
McCormick, S. (2018). Rhizobial strain‐dependent restriction of nitrogen fixation in a legume‐Rhizobium symbiosis. The Plant Journal, 93(1), 3–4.
Minibayeva, F., Beckett, R. P., & Kranner, I. (2015). Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry, 112, 122–129.
Mittler, R. (2017). ROS are good. Trends Plant Science, 22(1), 11–19.
Mrázová, A., Belay, S. A., Eliášová, A., Perez-Delgado, C., Kaducová, M., Betti, M., Vega, J. M., & Paľove-Balang, P. (2017). Expression, activity of phenylalanine-ammonia-lyase and accumulation of phenolic compounds in Lotus japonicus under salt stress. Biologia, 72(1), 36–42.
Nogales, S. (2021). Polyphenoloxidase (PPO): Effect, current determination and inhibition treatments in fresh-cut produce. Applied Science, 11(17), 7813.
Nyzhnyk, T., Pukhtaievych, P., & Kots, S. (2022). The intensity of drought-induced oxidative processes in soybeans depends on symbiosis with Bradyrhizobium strains. Journal of Central European Agriculture, 23(2), 318–326.
Omiadze, N. T., Mchedlishvili, N. I., & Abutidze, M. O. (2018). Phenoloxidases of perennial plants: Hydroxylase activity, isolation and physiological role. Annals of Agrarian Science, 16(2), 196–200.
Panadare, D., & Rathod, V. K. (2018). Extraction and purification of polyphenol oxidase: A review. Biocatalysis and Agricultural Biotechnolog, 14, 431–437.
Pandey, V. P., Awasthi, M., Singh, S., Tiwari, S., & Dwivedi, U. N. (2017). A сomprehensive review on function and application of plant peroxidases. Biochemistry and Analytical Biochemistry, 6, 308.
Pradhan, D., Sinclair, T., & Alijani, K. (2018). Nitrogen fixation establishment during initial growth of grain legume species. Journal of Crop Improvement, 32(1), 50–58.
Raza, A., Razzaq, A., Mehmood, S., Zou, X., Zhang, X., Lv, Y., & Xu, J. (2019). Impact of climate change on crops adaptation and strategies to tackle its outcome: A review. Plants, 8(2), 34.
Rosa, E. (2017). Enhancing legume growing through sustainable cropping for protein supply. Science of Food and Agriculture, 97(13), 4271–4272.
Ryu, H., Cho, H., Choi, D., & Hwang, I. (2012). Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Molecules and Cells, 34(2), 117–126.
Shigeto, J., & Tsutsumi, Y. (2016). Diverse functions and reactions of class III peroxidases. New Phytologist, 209, 1395–1402.
Singh, N., & Yadav, S. S. (2022). A review on health benefits of phenolics derived from dietary spices. Current Research in Food Science, 5, 1508–1523.
Sousa, W., Soratto, P., Peixoto, D., Campos, T. S., da Silva, M. B., Vaz Souza, A. G., Teixeira, I. R., & Gitari, H. I. (2022). Effects of Rhizobium inoculum compared with mineral nitrogen fertilizer on nodulation and seed yield of common bean. A meta-analysis. Agronomy for Sustainable Development, 42(2), 52.
Taranto, F., Pasqualone, A., Mangini, G., Tripodi, P., Miazzi, M. M., Pavan, S., & Montemurro, C. (2017). Polyphenol oxidases in crops: Biochemical, physiological and genetic aspects. International Journal of Molecular Science, 18(2), 377.
Tomás‐Barberán, F. A., & Espín, J. C. (2001). Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. Journal of the Science of Food and Agriculture, 81, 853–876.
Tonelli, M. L., Figueredo, M. S., Rodríguez, J., Fabra, A., & Ibañez, F. (2020). Induced systemic resistance-like responses elicited by rhizobia. Plant and Soil, 448(4), 1–14.
Wang, Q., Liu, J., & Zhu, H. (2018). Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Frontiers of Plant Science, 9, 313.
Xu, J., Wang, W., & Zhao, Y. (2021). Phenolic compounds in whole grain sorghum and their health benefits. Foods, 10(8), 1921.
Yu, S.-I., Kim, H., Yun, D.-J., Suh, M. C., & Lee, B.-H. (2018). Post-translational and transcriptional regulation of phenylpropanoid biosynthesis pathway by Kelch repeat F-box protein SAGL1. Plant Molecular Biology, 99, 135–148.
Alunni, S., Cipiciani, A., Fioroni, G., & Ottavi, L. (2003). Mechanisms of inhibition of phenylalanine ammonia-lyase by phenol inhibitors and phenol/glycine synergistic inhibitors. Archives of Biochemistry and Biophysics, 412(2), 170–175.
Araji, S., Grammer, T. A., & Gertzen, R. (2014). Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiolоgy, 164(3), 1191–1203.
Bradford, M. (1976). A rapid and sensitive method for the quantitation of the microgram quantities of protein utilizing: the principle of protein – dye binding. Analytical Biochemistry, 72, 248–254.
Cerezini, P., Riar, M. K., & Sinclair, T. R. (2016). Transpiration and nitrogen fixation recovery capacity in soybean following drought stress. Journal of Crop Improvement, 30, 562–571.
Chen, H., & Vierling, R. A. (2000). Molecular cloning and characterization of soybean peroxidase gene families. Plant Science, 150(2), 129–137.
Chon, S.-U. (2013). Total polyphenols and bioactivity of seeds and sprouts in several legumes. Current Pharmaceutical Desing, 19(34), 6112–6124.
Cosme, P., Rodríguez, A. B., Espino, J., & Garrido, M. (2020). Plant phenolics: Bioavailability as a key determinant of their potential health-promoting applications. Antioxidants, 9(12), 1263.
Damiani, I., Pauly, N., Puppo, A., Brouquisse, R., & Boscar, A. (2016). Reactive oxygen species and nitric oxide control early steps of the legume – Rhizobium symbiotic. Frontiers in Plant Science, 7, 454.
Dicko, M. H., Gruppen, H., Traore, A. S., Voragen, A. G. J., & Berkel, W. J. H. (2006). Phenolic compounds and related enzymes as determinants of sorghum for food use. Biotechnology and Molecular Biology Review, 1(1), 21–38.
Egley, G. H., Paul, R. N., Vaughn, K. C., & Duke, S. O. (1983). Role of peroxidase in the development of water impermeable seed coats in Sida sprinosa L. Planta, 157(1), 224–232.
Fan, L., Shi, G., Yang, J., Liu, G., Niu, Z., Ye, W., Wu, S., Wang, L., & Guan, Q. A. (2022). Protective role of phenylalanine ammonia-lyase from Astragalus membranaceus against saline-alkali stress. International Journal of Molecular Sciences, 23(24), 15686.
Gaonkar, V., & Rosentrater, K. (2019). Soybean. In: Pan, Z., Zhang, R., Zicari, S. (Eds.). Integrated processing technologies for food and agricultural by-products. Elsevier Inc. Pp. 73–104.
Gho, Y. S., Kim, S. J., & Jung, K. H. (2019). Phenylalanine ammonia-lyase family is closely associated with response to phosphate deficiency in rice. Genes and Genomics, 42(1), 67–76.
Gourion, B., Berrabah, F., Ratet, P., & Stacey, G. (2015). Rhizobium-legume symbioses: The crucial role of plant immunity. Trends Plant Science, 20(3), 186–194.
Hawkins, J., & Oresnik, I. (2021). The Rhizobium-legume symbiosis: Co-opting successful stress management. Front Plant Sciences, 12, 796045.
Jun, S. Y., Sattler, S. A., Cortez, G. S., Vermerris, W., Sattler, S. E., & Kang, C. H. (2018). Biochemical and structural analysis of substrate specificity of a phenylalanine ammonia-lyase. Plant Physiology, 176(2), 1452–1468.
Keet, J.-H., Ellis, A. G., Hui, C., & Le Roux, J. J. (2017). Legume-Rhizobium symbiotic promiscuity and effectiveness do not affect plant invasiveness. South African Journal of Botany, 109, 341.
Khatun, M., Sarkar, S., Era, F., Islam, A., Anwar, M., Fahad, S., Datta, R., & Islam, A. (2021). A drought stress in grain legumes: Effects, tolerance mechanisms and management. Agronomy, 11(12), 2374.
Kots, S. Y., & Hryschuk, O. O. (2019). Fitohormonal’na rehuliatsija bobovo-ryzobial’noho symbiozu [Phytohormonal regulation of legume-rhizobial symbiosis]. Fyzyolohyia Rastenyi y Henetyka, 51(1), 1–27 (in Ukrainian).
Kots, S. Y., Morgun, V. V., & Patykа, V. F. (2010). Biologicheskaya fiksacija azota: Bobovo-rizobialnyj symbioz [Biological fixation of nitrogen: Legume-rhizobium symbiosis]. Logos, Kyiv (in Ukrainian).
Kuvalekar, A., Redkar, A., Gandhe, K., & Harsulkar, A. (2011). Peroxidase and polyphenol oxidase activities in compatible host–pathogen interaction in Jasminum officinale and Uromyces hobsoni: Insights into susceptibility of host. New Zealand Journal of Botany, 49(3), 351–359.
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.
Mamenko, Т. (2021). Regulation of legume-rhizobial symbiosis: Molecular genetic aspects and participation of reactive oxygen species. Cytology and Genetics, 55(5), 447–459.
Mamenko, Т. P., Kots, S. Y., Mykhalkiv, L. M., & Homenko, Y. A. (2021). Phenylalanine ammonia-lyase enzyme activity in the symbiotic system Glycine max – Bradyrhizobium japonicum by seed inoculation different in activity and virulation strain and treatment with fungicides. Mikrobiologichnyi Zhurnal, 83(4), 63–73.
McCormick, S. (2018). Rhizobial strain‐dependent restriction of nitrogen fixation in a legume‐Rhizobium symbiosis. The Plant Journal, 93(1), 3–4.
Minibayeva, F., Beckett, R. P., & Kranner, I. (2015). Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry, 112, 122–129.
Mittler, R. (2017). ROS are good. Trends Plant Science, 22(1), 11–19.
Mrázová, A., Belay, S. A., Eliášová, A., Perez-Delgado, C., Kaducová, M., Betti, M., Vega, J. M., & Paľove-Balang, P. (2017). Expression, activity of phenylalanine-ammonia-lyase and accumulation of phenolic compounds in Lotus japonicus under salt stress. Biologia, 72(1), 36–42.
Nogales, S. (2021). Polyphenoloxidase (PPO): Effect, current determination and inhibition treatments in fresh-cut produce. Applied Science, 11(17), 7813.
Nyzhnyk, T., Pukhtaievych, P., & Kots, S. (2022). The intensity of drought-induced oxidative processes in soybeans depends on symbiosis with Bradyrhizobium strains. Journal of Central European Agriculture, 23(2), 318–326.
Omiadze, N. T., Mchedlishvili, N. I., & Abutidze, M. O. (2018). Phenoloxidases of perennial plants: Hydroxylase activity, isolation and physiological role. Annals of Agrarian Science, 16(2), 196–200.
Panadare, D., & Rathod, V. K. (2018). Extraction and purification of polyphenol oxidase: A review. Biocatalysis and Agricultural Biotechnolog, 14, 431–437.
Pandey, V. P., Awasthi, M., Singh, S., Tiwari, S., & Dwivedi, U. N. (2017). A сomprehensive review on function and application of plant peroxidases. Biochemistry and Analytical Biochemistry, 6, 308.
Pradhan, D., Sinclair, T., & Alijani, K. (2018). Nitrogen fixation establishment during initial growth of grain legume species. Journal of Crop Improvement, 32(1), 50–58.
Raza, A., Razzaq, A., Mehmood, S., Zou, X., Zhang, X., Lv, Y., & Xu, J. (2019). Impact of climate change on crops adaptation and strategies to tackle its outcome: A review. Plants, 8(2), 34.
Rosa, E. (2017). Enhancing legume growing through sustainable cropping for protein supply. Science of Food and Agriculture, 97(13), 4271–4272.
Ryu, H., Cho, H., Choi, D., & Hwang, I. (2012). Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Molecules and Cells, 34(2), 117–126.
Shigeto, J., & Tsutsumi, Y. (2016). Diverse functions and reactions of class III peroxidases. New Phytologist, 209, 1395–1402.
Singh, N., & Yadav, S. S. (2022). A review on health benefits of phenolics derived from dietary spices. Current Research in Food Science, 5, 1508–1523.
Sousa, W., Soratto, P., Peixoto, D., Campos, T. S., da Silva, M. B., Vaz Souza, A. G., Teixeira, I. R., & Gitari, H. I. (2022). Effects of Rhizobium inoculum compared with mineral nitrogen fertilizer on nodulation and seed yield of common bean. A meta-analysis. Agronomy for Sustainable Development, 42(2), 52.
Taranto, F., Pasqualone, A., Mangini, G., Tripodi, P., Miazzi, M. M., Pavan, S., & Montemurro, C. (2017). Polyphenol oxidases in crops: Biochemical, physiological and genetic aspects. International Journal of Molecular Science, 18(2), 377.
Tomás‐Barberán, F. A., & Espín, J. C. (2001). Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. Journal of the Science of Food and Agriculture, 81, 853–876.
Tonelli, M. L., Figueredo, M. S., Rodríguez, J., Fabra, A., & Ibañez, F. (2020). Induced systemic resistance-like responses elicited by rhizobia. Plant and Soil, 448(4), 1–14.
Wang, Q., Liu, J., & Zhu, H. (2018). Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Frontiers of Plant Science, 9, 313.
Xu, J., Wang, W., & Zhao, Y. (2021). Phenolic compounds in whole grain sorghum and their health benefits. Foods, 10(8), 1921.
Yu, S.-I., Kim, H., Yun, D.-J., Suh, M. C., & Lee, B.-H. (2018). Post-translational and transcriptional regulation of phenylpropanoid biosynthesis pathway by Kelch repeat F-box protein SAGL1. Plant Molecular Biology, 99, 135–148.
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2023-07-26
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