Production and Function of Reactive Nitrogen Species (RNS) and Status in Stress Conditions
Year 2020,
Issue: 18, 435 - 444, 15.04.2020
İlkay Yavaş
,
Volkan Mehmet Çınar
,
Aydın Ünay
Abstract
It is known that Reactive Nitrogen Species (RNS) play a role as a signaling molecule under biotic and abiotic stress conditions in plants, but its presence causes oxidative damage. Chloroplasts, mitochondria, peroxisomes, endoplasmic reticulum and plasma membranes are cell organelles in which RNS occur. It has been shown that nitrate reductase enzyme is the most important enzyme responsible for nitric oxide (NO) production in cytoplasm. NO interacts with many enzymes, substrates and hormones and plays a role in the regulation of physiological events. In this respect, production, physiological effects and inactivation of RNS are important in defining many physiological events.
References
- Adams, L., Franco, M. C., & Estevez, A. G. (2015). Reactive nitrogen species in cellular signaling. Experimental biology and medicine, 240(6), 711-717.
Astier, J., Jeandroz, S., & Wendehenne, D. (2018). Nitric oxide synthase in plants: The surprise from algae. Plant science: an international journal of experimental plant biology, 268, 64.
- Basu, S., Azarova, N. A., Font, M. D., King, S. B., Hogg, N., Gladwin, M. T., & Kim-Shapiro, D. B. (2008). Nitrite reductase activity of cytochrome c. Journal of Biological Chemistry, 283(47), 32590-32597.
- Beligni, M. V., Fath, A., Bethke, P. C., Lamattina, L., & Jones, R. L. (2002). Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant physiology, 129(4), 1642-1650.
- Botrel, A., Magné, C., & Kaiser, W. M. (1996). Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant physiology and biochemistry (Paris), 34(5), 645-652.
- De Michele, R., Vurro, E., Rigo, C., Costa, A., Elviri, L., Di Valentin, M., ... & Schiavo, F. L. (2009). Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiology, 150(1), 217-228.
- Del Río, L. A. (2015). ROS and RNS in plant physiology: an overview. Journal of Experimental Botany, 66(10), 2827-2837.
- Delledonne, M., Xia, Y., Dixon, R. A., & Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394(6693), 585-588.
- Desikan, R., Griffiths, R., Hancock, J., & Neill, S. (2002). A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 99(25), 16314-16318.
- Durner, J., Wendehenne, D., & Klessig, D. F. (1998). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences, 95(17), 10328-10333.
- Fewson, C. A., & Nicholas, D. J. D. (1960). Utilization of nitric oxide by micro-organisms and higher plants. Nature, 188, 794-6.
- Foresi, N., Correa-Aragunde, N., Parisi, G., Caló, G., Salerno, G., & Lamattina, L. (2010). Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. The Plant Cell, 22(11), 3816-3830.
- Gupta, K. J., & Rolletschek, H. (2013). Plant respiratory metabolism: a special focus on the physiology of beetroot (Beta vulgaris L.) mitochondria. In Red Beet Biotechnology (pp. 91-104). Springer, Boston, MA.
- Gupta, K. J., & Igamberdiev, A. U. (2015). Compartmentalization of reactive oxygen species and nitric oxide production in plant cells: an overview. In Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants (pp. 1-14). Springer, Cham.
- Gupta, K. J., Stoimenova, M., & Kaiser, W. M. (2005). In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. Journal of Experimental Botany, 56(420), 2601-2609.
- Gupta, K. J., & Kaiser, W. M. (2010). Production and scavenging of nitric oxide by barley root mitochondria. Plant and Cell Physiology, 51(4), 576-584.
- Gupta, K. J., & Igamberdiev, A. U. (2016). Reactive nitrogen species in mitochondria and their implications in plant energy status and hypoxic stress tolerance. Frontiers in Plant Science, 7, 369.
- Gupta, K. J., Kumari, A., Florez-Sarasa, I., Fernie, A. R., & Igamberdiev, A. U. (2018). Interaction of nitric oxide with the components of the plant mitochondrial electron transport chain. Journal of experimental botany, 69(14), 3413-3424.
- Hancock, J. T., & Neill, S. J. (2019). Nitric Oxide: Its generation and interactions with other reactive signaling compounds. Plants, 8(2), 41.
- Hebelstrup, K. H., & Møller, I. M. (2015). Mitochondrial signaling in plants under hypoxia: use of reactive oxygen species (ROS) and reactive nitrogen species (RNS). In Reactive oxygen and nitrogen species signaling and communication in plants (pp. 63-77). Springer, Cham.
- Horchani, F., Prévot, M., Boscari, A., Evangelisti, E., Meilhoc, E., Bruand, C., & Brouquisse, R. (2011). Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiology, 155(2), 1023-1036.
- Jasid, S., Simontacchi, M., Bartoli, C. G., & Puntarulo, S. (2006). Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiology, 142(3), 1246-1255.
- Jeandroz, S., Wipf, D., Stuehr, D. J., Lamattina, L., Melkonian, M., Tian, Z., & Wendehenne, D. (2016). Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci. Signal., 9(417), re2-re2.
- Kapoor, D., Singh, S., Kumar, V., Romero, R., Prasad, R., & Singh, J. (2019). Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene, 19, 100182.
- Kim, Y., Mun, B. G., Khan, A. L., Waqas, M., Kim, H. H., Shahzad, R., & Lee, I. J. (2018). Regulation of reactive oxygen and nitrogen species by salicylic acid in rice plants under salinity stress conditions. Plos one, 13(3).
- Lazalt, A. M., Beligni, M. V., & Lamattina, L. (1997). Nitric oxide preserves the level of chlorophyll in potato leaves infected by Phytophthora infestans. European Journal of Plant Pathology, 103(7), 643-651.
- Leshem, Y. Y., & Haramaty, E. (1996). Plant aging: the emission of NO and ethylene and effect of NO-releasing compounds on growth of pea (Pisum sativum) foliage. J Plant Physiol, 148(3-4), 258-263.
- Lindermayr, C., & Durner, J. (2009). S-Nitrosylation in plants: pattern and function. Journal of Proteomics, 73(1), 1-9.
- Luis, A., & Río, D. (Eds.). (2013). Peroxisomes and their key role in cellular signaling and metabolism. Springer Netherlands.
- Malerba, M., & Cerana, R. (2015). Reactive oxygen and nitrogen species in defense/stress responses activated by chitosan in sycamore cultured cells. International journal of molecular sciences, 16(2), 3019-3034.
- Mayer, D., Mithöfer, A., Glawischnig, E., Georgii, E., Ghirardo, A., Kanawati, B., & Gaupels, F. (2018). Short-term exposure to nitrogen dioxide provides basal pathogen resistance. Plant physiology, 178(1), 468-487.
- Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., & Blake, D. R. (1998). Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS letters, 427(2), 225-228.
- Noritake, T., Kawakita, K., & Doke, N. (1996). Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant and Cell Physiology, 37(1), 113-116.
- Ohta, S. (2015). Molecular hydrogen as a novel antioxidant: overview of the advantages of hydrogen for medical applications. In Methods in enzymology (Vol. 555, pp. 289-317). Academic Press.
- Ortega-Galisteo, A. P., Rodríguez-Serrano, M., Pazmiño, D. M., Gupta, D. K., Sandalio, L. M., & Romero-Puertas, M. C. (2012). S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of experimental botany, 63(5), 2089-2103.
- Palmer, R. M., Ferrige, A. G., & Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature, 327(6122), 524-526.
- Planchet, E., Jagadis Gupta, K., Sonoda, M., & Kaiser, W. M. (2005). Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. The Plant Journal, 41(5), 732-743.
- Procházková, D., Wilhelmová, N., & Pavlík, M. (2015). Reactive nitrogen species and nitric oxide. In Nitric Oxide Action in Abiotic Stress Responses in Plants (pp. 3-19). Springer, Cham.
- Rockel, P., Strube, F., Rockel, A., Wildt, J., & Kaiser, W. M. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of experimental botany, 53(366), 103-110.
- Saddhe, A. A., Malvankar, M. R., Karle, S. B., & Kumar, K. (2019). Reactive nitrogen species: paradigms of cellular signaling and regulation of salt stress in plants. Environmental and Experimental Botany, 161, 86-97.
- Schertl, P., & Braun, H. P. (2014). Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science, 5, 163.
- Tielens, A. G., Rotte, C., van Hellemond, J. J., & Martin, W. (2002). Mitochondria as we don't know them. Trends in biochemical sciences, 27(11), 564-572.
- Tischner, R., Planchet, E., & Kaiser, W. M. (2004). Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS letters, 576(1-2), 151-155.
- Turkan, I. (2018). ROS and RNS: key signalling molecules in plants. Journal of experimental botany, 69(14), 3313-3315.
- Wang, Y., Loake, G. J., & Chu, C. (2013). Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Frontiers in Plant Science, 4, 314.
- Wilson, H. R., Veal, D., Whiteman, M., & Hancock, J. T. (2017). Hydrogen gas and its role in cell signalling. CAB Rev., 12: 1-3.
- Zheng, C., Jiang, D., Liu, F., Dai, T., Liu, W., Jing, Q., & Cao, W. (2009). Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environmental and Experimental Botany, 67(1), 222-227.
- Zhu, Y., Liao, W., Wang, M., Niu, L., Xu, Q., & Jin, X. (2016). Nitric oxide is required for hydrogen gas-induced adventitious root formation in cucumber. Journal of plant physiology, 195, 50-58.
- Zhu, Y., Liao, W., Niu, L., Wang, M., & Ma, Z. (2016). Nitric oxide is involved in hydrogen gas-induced cell cycle activation during adventitious root formation in cucumber. BMC plant biology, 16(1), 146.
Reaktif Azot Türlerinin (RNS) Üretimi, Fonksiyonu ve Stres Koşullarındaki Durumu
Year 2020,
Issue: 18, 435 - 444, 15.04.2020
İlkay Yavaş
,
Volkan Mehmet Çınar
,
Aydın Ünay
Abstract
Bitkilerde Reaktif Azot Türlerinin (RNS) biyotik ve abiyotik stres koşullarında sinyal molekülü olarak rol oynadığı, buna karşın varlığının oksidatif hasara yol açtığı bilinmektedir. Kloroplast, mitokondri, peroksizom, endoplazmik retikulum ve plazma memranları RNS’lerin ortaya çıktığı hücre organelleridir. Sitoplazmada nitrat redükdaz enziminin nitrik oksit (NO) üretiminden sorumlu en önemli enzim olduğu ortaya konulmuştur. NO birçok enzim, substrat ve hormonlar ile etkileşime girerek fizyolojik olayların düzenlenmesinde rol oynamaktadır. Bitki metabolizmasında aşırı konsantrasyonlarda üretildiğinde ise reaktif oksijen türlerinde olduğu gibi birçok enzim tarafından etkisiz forma dönüştürülmektedir. Bu yönden RNS’lerin üretimi, fizyolojik etkileri ve etkisizleştirilmeleri birçok fizyolojik olayı tanımlamada önemlidir.
References
- Adams, L., Franco, M. C., & Estevez, A. G. (2015). Reactive nitrogen species in cellular signaling. Experimental biology and medicine, 240(6), 711-717.
Astier, J., Jeandroz, S., & Wendehenne, D. (2018). Nitric oxide synthase in plants: The surprise from algae. Plant science: an international journal of experimental plant biology, 268, 64.
- Basu, S., Azarova, N. A., Font, M. D., King, S. B., Hogg, N., Gladwin, M. T., & Kim-Shapiro, D. B. (2008). Nitrite reductase activity of cytochrome c. Journal of Biological Chemistry, 283(47), 32590-32597.
- Beligni, M. V., Fath, A., Bethke, P. C., Lamattina, L., & Jones, R. L. (2002). Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant physiology, 129(4), 1642-1650.
- Botrel, A., Magné, C., & Kaiser, W. M. (1996). Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant physiology and biochemistry (Paris), 34(5), 645-652.
- De Michele, R., Vurro, E., Rigo, C., Costa, A., Elviri, L., Di Valentin, M., ... & Schiavo, F. L. (2009). Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiology, 150(1), 217-228.
- Del Río, L. A. (2015). ROS and RNS in plant physiology: an overview. Journal of Experimental Botany, 66(10), 2827-2837.
- Delledonne, M., Xia, Y., Dixon, R. A., & Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature, 394(6693), 585-588.
- Desikan, R., Griffiths, R., Hancock, J., & Neill, S. (2002). A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 99(25), 16314-16318.
- Durner, J., Wendehenne, D., & Klessig, D. F. (1998). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences, 95(17), 10328-10333.
- Fewson, C. A., & Nicholas, D. J. D. (1960). Utilization of nitric oxide by micro-organisms and higher plants. Nature, 188, 794-6.
- Foresi, N., Correa-Aragunde, N., Parisi, G., Caló, G., Salerno, G., & Lamattina, L. (2010). Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. The Plant Cell, 22(11), 3816-3830.
- Gupta, K. J., & Rolletschek, H. (2013). Plant respiratory metabolism: a special focus on the physiology of beetroot (Beta vulgaris L.) mitochondria. In Red Beet Biotechnology (pp. 91-104). Springer, Boston, MA.
- Gupta, K. J., & Igamberdiev, A. U. (2015). Compartmentalization of reactive oxygen species and nitric oxide production in plant cells: an overview. In Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants (pp. 1-14). Springer, Cham.
- Gupta, K. J., Stoimenova, M., & Kaiser, W. M. (2005). In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. Journal of Experimental Botany, 56(420), 2601-2609.
- Gupta, K. J., & Kaiser, W. M. (2010). Production and scavenging of nitric oxide by barley root mitochondria. Plant and Cell Physiology, 51(4), 576-584.
- Gupta, K. J., & Igamberdiev, A. U. (2016). Reactive nitrogen species in mitochondria and their implications in plant energy status and hypoxic stress tolerance. Frontiers in Plant Science, 7, 369.
- Gupta, K. J., Kumari, A., Florez-Sarasa, I., Fernie, A. R., & Igamberdiev, A. U. (2018). Interaction of nitric oxide with the components of the plant mitochondrial electron transport chain. Journal of experimental botany, 69(14), 3413-3424.
- Hancock, J. T., & Neill, S. J. (2019). Nitric Oxide: Its generation and interactions with other reactive signaling compounds. Plants, 8(2), 41.
- Hebelstrup, K. H., & Møller, I. M. (2015). Mitochondrial signaling in plants under hypoxia: use of reactive oxygen species (ROS) and reactive nitrogen species (RNS). In Reactive oxygen and nitrogen species signaling and communication in plants (pp. 63-77). Springer, Cham.
- Horchani, F., Prévot, M., Boscari, A., Evangelisti, E., Meilhoc, E., Bruand, C., & Brouquisse, R. (2011). Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiology, 155(2), 1023-1036.
- Jasid, S., Simontacchi, M., Bartoli, C. G., & Puntarulo, S. (2006). Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiology, 142(3), 1246-1255.
- Jeandroz, S., Wipf, D., Stuehr, D. J., Lamattina, L., Melkonian, M., Tian, Z., & Wendehenne, D. (2016). Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci. Signal., 9(417), re2-re2.
- Kapoor, D., Singh, S., Kumar, V., Romero, R., Prasad, R., & Singh, J. (2019). Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene, 19, 100182.
- Kim, Y., Mun, B. G., Khan, A. L., Waqas, M., Kim, H. H., Shahzad, R., & Lee, I. J. (2018). Regulation of reactive oxygen and nitrogen species by salicylic acid in rice plants under salinity stress conditions. Plos one, 13(3).
- Lazalt, A. M., Beligni, M. V., & Lamattina, L. (1997). Nitric oxide preserves the level of chlorophyll in potato leaves infected by Phytophthora infestans. European Journal of Plant Pathology, 103(7), 643-651.
- Leshem, Y. Y., & Haramaty, E. (1996). Plant aging: the emission of NO and ethylene and effect of NO-releasing compounds on growth of pea (Pisum sativum) foliage. J Plant Physiol, 148(3-4), 258-263.
- Lindermayr, C., & Durner, J. (2009). S-Nitrosylation in plants: pattern and function. Journal of Proteomics, 73(1), 1-9.
- Luis, A., & Río, D. (Eds.). (2013). Peroxisomes and their key role in cellular signaling and metabolism. Springer Netherlands.
- Malerba, M., & Cerana, R. (2015). Reactive oxygen and nitrogen species in defense/stress responses activated by chitosan in sycamore cultured cells. International journal of molecular sciences, 16(2), 3019-3034.
- Mayer, D., Mithöfer, A., Glawischnig, E., Georgii, E., Ghirardo, A., Kanawati, B., & Gaupels, F. (2018). Short-term exposure to nitrogen dioxide provides basal pathogen resistance. Plant physiology, 178(1), 468-487.
- Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., & Blake, D. R. (1998). Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS letters, 427(2), 225-228.
- Noritake, T., Kawakita, K., & Doke, N. (1996). Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant and Cell Physiology, 37(1), 113-116.
- Ohta, S. (2015). Molecular hydrogen as a novel antioxidant: overview of the advantages of hydrogen for medical applications. In Methods in enzymology (Vol. 555, pp. 289-317). Academic Press.
- Ortega-Galisteo, A. P., Rodríguez-Serrano, M., Pazmiño, D. M., Gupta, D. K., Sandalio, L. M., & Romero-Puertas, M. C. (2012). S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of experimental botany, 63(5), 2089-2103.
- Palmer, R. M., Ferrige, A. G., & Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature, 327(6122), 524-526.
- Planchet, E., Jagadis Gupta, K., Sonoda, M., & Kaiser, W. M. (2005). Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. The Plant Journal, 41(5), 732-743.
- Procházková, D., Wilhelmová, N., & Pavlík, M. (2015). Reactive nitrogen species and nitric oxide. In Nitric Oxide Action in Abiotic Stress Responses in Plants (pp. 3-19). Springer, Cham.
- Rockel, P., Strube, F., Rockel, A., Wildt, J., & Kaiser, W. M. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of experimental botany, 53(366), 103-110.
- Saddhe, A. A., Malvankar, M. R., Karle, S. B., & Kumar, K. (2019). Reactive nitrogen species: paradigms of cellular signaling and regulation of salt stress in plants. Environmental and Experimental Botany, 161, 86-97.
- Schertl, P., & Braun, H. P. (2014). Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science, 5, 163.
- Tielens, A. G., Rotte, C., van Hellemond, J. J., & Martin, W. (2002). Mitochondria as we don't know them. Trends in biochemical sciences, 27(11), 564-572.
- Tischner, R., Planchet, E., & Kaiser, W. M. (2004). Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS letters, 576(1-2), 151-155.
- Turkan, I. (2018). ROS and RNS: key signalling molecules in plants. Journal of experimental botany, 69(14), 3313-3315.
- Wang, Y., Loake, G. J., & Chu, C. (2013). Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Frontiers in Plant Science, 4, 314.
- Wilson, H. R., Veal, D., Whiteman, M., & Hancock, J. T. (2017). Hydrogen gas and its role in cell signalling. CAB Rev., 12: 1-3.
- Zheng, C., Jiang, D., Liu, F., Dai, T., Liu, W., Jing, Q., & Cao, W. (2009). Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environmental and Experimental Botany, 67(1), 222-227.
- Zhu, Y., Liao, W., Wang, M., Niu, L., Xu, Q., & Jin, X. (2016). Nitric oxide is required for hydrogen gas-induced adventitious root formation in cucumber. Journal of plant physiology, 195, 50-58.
- Zhu, Y., Liao, W., Niu, L., Wang, M., & Ma, Z. (2016). Nitric oxide is involved in hydrogen gas-induced cell cycle activation during adventitious root formation in cucumber. BMC plant biology, 16(1), 146.