GENERATION OF NITRIC OXIDE AND ITS ROLE UNDER STRESS CONDITIONS IN PLANTS
Abstract
Nitric oxide is one of reactive nitrogen species. This form of nitrogen can influence the plant organism both positively and negatively. This work provides available information on the effect of nitric oxide donors on the plant organism. At low concentrations •NO can operate as a signaling molecule with a wide range of regulatory functions. •NO is involved in the response of plants to stressful environmental factors, both biotic and abiotic nature. Specifically, •NO increases plant resistance at exposure to salt stress, heavy metal ions, pathogens, increases tolerance to sudden decrease or increase of the ambient temperature. In this work the mechanisms of nitric oxide formation in various plant organelles are described. Plant organisms also can be affected environmentally derived •NO. Nitrate reductase and NO-synthase are the enzymes involved in •NO formation. Nitric oxide is released from the peroxisomes, chloroplasts and mitochondria. Nitrite can be reduced to nitric oxide in the plant mitochondria. Inhibitors of the mitochondrial electron transport chain (ETC) also inhibit •NO production. That indicate that the electrons from mitochondrial ETC can participate in reduction of nitrite. In peroxisomes •NO is formed by the action of the enzyme NO-synthase. Also non-enzymatic reduction of nitrite in apoplast space as one of the ways of •NO formation in plants, especially in roots, was described. The increase of nitric oxide release can be observed under treatment by herbicides and nitrate fertilizers. In addition, reactive nitrogen species can be received by plants from the environment, particularly as nitric oxide. This review paper presents generalized scheme of effect of nitric oxide and its transformations in plants.
Key words: nitric oxide; transportation routes; chemical transformation.
References
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Bethke P.C., Badger M.R., Jones R.L.. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. 2004; 16: 332–341.
Corpas F.J., Barroso J.B. Peroxisomal plant nitric oxide synthase (NOS) protein is imported by peroxisomal targeting signal type 2 (PTS2) in a process that depends on the cytosolic receptor PEX7 and calmodulin.. FEBS Lett. 2014; http://dx.doi.org/10.1016/ j.febslet.2014.04.034
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Dean J.V., Harper J.E. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean.. Plant Physiol. 1988; 88: 389-395.
Desikan R., Cheung M.K., Bright J., Henson D., Hancock J.T., Neill S.J. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J. Exp. Bot. 2004; 55: 205–212.
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Garcia-Mata C., Lamattina L. Abscisic acid, nitric oxide and stomatal closure: is nitrate reductase one of the missing links. Trends Plant Sci. 2003; 8: 20–26.
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Lamattina L., García-Mata C., Graziano M., Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule.. Annu. Rev. Plant Biol. 2003; 54: 109–136.
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Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.. Cell Devel. Biol. 1994; 79: 583–593.
Malik S.I., Hussain A., Yun B.W., Spoel S.H., Loake G.J. GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci. 2011; 181: 540-544.
McDowell J.M., Dangl J.L. Signal transduction in the plant immune response. Trends in Biochemical Sciences. 2000; 25: 79–82.
Møller I.M. Plant mitochondria and oxidative stress. Electron transport, NADPH turnover and metabolism of reactive oxygen species.. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 561–591.
Overmyer K., Brosche M., Kangasjarvi J. Reactive oxygen species and hormonal control of cell death.. Trends Plant Sci. 2003; 8: 335-342.
Planchet E., Jagadis Gupta K., Sonoda M., Kaiser W.M. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport.. Plant J. 2005; 41: 732–743.
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Rapoport S. M. The reticulocyte.. Boca Raton, FL: CRC Press; 1986.
Ribeiro E.A.Jr, Cunha F.Q., Tamashiro W.M.S.C., Martins I.S. Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells.. FEBS Letters. 1999; 445: 283–286.
Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 2002; 53: 103–110.
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Stohr C., Strube F., Marx G., Ullrich W.R., Rockel P. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite.. Planta. 2001; 212: 835–841.
Stohr C., Ullrich W.R. Generation and possible roles of NO in plant roots and their apoplastic space. J. Exp. Bot. 2002; 53: 2293–2303.
Tanno M., Sueyoshi S., Miyata N., Nakagawa S. Nitric oxide generation from aromatic N-nitrosoureas at ambient temperature.. Chem. Pharm. Bulletin . 1996; 44: 1849–1852.
Tewari R.K., Prommer J., Watanabe M. Endogenous nitric oxide generation in protoplast chloroplasts.. Plant Cell Rep. 2013; 32: 31–44.
Tischner R., Planchet E., Kaiser W.M. Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana.. FEBS Letters. 2004; 576: 151–155.
Xu J, Yin H, Li Y, Liu X. Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum.. Plant Physiol. 2010; 154: 13190–1334.
Yamasaki H. Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2000; 355: 1477–1488.
Yamasaki H., Sakihama Y., Takahashi S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme.. Trends Plant Sci. 1999; 4: 128–129.
Yun B.W., Feechan A., Yin M., Saidi N.B.B., Le Bihan T., Yu M., et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. 2011; 478: 264–268.
Zhao M.G., Chen L, Zhang L.L., Zhang W.H. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 2009; 151: 755–767.
Baudhouin E. The language of nitric oxide signaling.. Plant Biol. (Stuttg). 2011; 13: 233–242.
Beligni M.V., Lamattina L. Nitric oxide in plants: the history is just beginning.. Plant. Cell Environ. 2001; 24: 267–278.
Bethke P.C., Badger M.R., Jones R.L.. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. 2004; 16: 332–341.
Corpas F.J., Barroso J.B. Peroxisomal plant nitric oxide synthase (NOS) protein is imported by peroxisomal targeting signal type 2 (PTS2) in a process that depends on the cytosolic receptor PEX7 and calmodulin.. FEBS Lett. 2014; http://dx.doi.org/10.1016/ j.febslet.2014.04.034
Corpas F.J., Barroso J.B., del Río L.A. Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells.. Trends Plant Sci. 2001; 6: 145–150.
Corpas F.J., Leterrier M., Valderrama R., Airaki M., Chaki M., Palma J.M., Barroso J.B. Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress.. Plant Sci. 2011; 181: 604–611.
Crawford N.M. Mechanisms for nitric oxide synthesis in plants.. J. Exp. Bot. 2006: 57(3): 471–478.
Dean J.V., Harper J.E. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean.. Plant Physiol. 1988; 88: 389-395.
Desikan R., Cheung M.K., Bright J., Henson D., Hancock J.T., Neill S.J. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J. Exp. Bot. 2004; 55: 205–212.
Domingos P., Prado A. M., Wong A., Gehring C., Feijo J. A. Nitric Oxide: A Multitasked signaling gas in plants.. Molecular Plant. 2015; http://dx.doi.org/10.1016/j.molp.2014.12.010
Ferrer M.A., Ros Barcelo A. Differential effects of nitric oxide on peroxidase and H2O2 production by the xylem of Zinnia elegans.. Plant Cell Environ. 1999; 22: 891-897.
Garcia-Mata C., Lamattina L. Abscisic acid, nitric oxide and stomatal closure: is nitrate reductase one of the missing links. Trends Plant Sci. 2003; 8: 20–26.
Gouvêa C.M.C.P., Souza J.F., Magalhâes A.C.N., Martins I.S. NO-releasing substances that induce growth elongation in maize root segments.. Plant Grow. Regul. 1997; 21: 183–187.
Grubišic D., Giba Z., Konjevic R. The effect of organic nitrates in phytochrome-controlled germination of Paulownia tormentosa seeds.. Photochem. Photobiol. 1992; 56: 629–632.
Grubišic D., Konjevic R. Light and nitrate interaction in phytochrome-controlled germination of Paulownia tormentosa seeds.. Planta. 1990; 181: 239-243.
Gupta K.J., Igamberdiev A.U., Manjunatha G., Segu S., Moran J.F., Neelawarne B., Bauwe H., Kaiser W.M. The emerging roles of nitric oxide (NO) in plant mitochondria.. Plant Sci. 2011; 181: 520–526.
Halliwell B., Gutteridge J.M.C. Free radicals in biology and medicine.. Oxford: Oxford Univ. Press. 3rd ed. 1999.
Halliwell B., Gutteridge J.M.C. Free radicals in biology and medicine. Oxford: Clarendon Press. 2007.
Harper J.E. Evolution of Nitrogen Oxide(s) during In Vivo Nitrate Reductase Assay of Soybean Leaves.. Plant Physiol. 1981; 68(6): 1488–1493.
Klepper L.A. Comparison between NOx evolution mechanisms of wild-type and nr1 mutant soybean leaves.. Plant Physiology. 1990; 93: 26–32.
Klepper L.A. Nitric oxide emissions from soybean leaves during in vivo nitrate reductase assays.. Plant Physiol. 1987; 85: 96–99.
Klepper L.A. Nitric-oxide (NO) and nitrogen-dioxide (NO2) emissions from herbicide-treated soybean plants.. Atmos. Environ. 1979; 13: 537–542.
Lamattina L., García-Mata C., Graziano M., Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule.. Annu. Rev. Plant Biol. 2003; 54: 109–136.
Lea U.S., Ten Hoopen F., Provan F., Kaiser W.M., Meyer C., Lillo C. Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in high nitrite excretion and NO emission from leaf and root tissue.. Planta. 2004; 219: 59–65.
Leshem Y.Y., Haramaty E. The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum L. foliage.. J. Plant Physiol. 1996; 148: 258–263.
Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.. Cell Devel. Biol. 1994; 79: 583–593.
Malik S.I., Hussain A., Yun B.W., Spoel S.H., Loake G.J. GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci. 2011; 181: 540-544.
McDowell J.M., Dangl J.L. Signal transduction in the plant immune response. Trends in Biochemical Sciences. 2000; 25: 79–82.
Møller I.M. Plant mitochondria and oxidative stress. Electron transport, NADPH turnover and metabolism of reactive oxygen species.. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 561–591.
Overmyer K., Brosche M., Kangasjarvi J. Reactive oxygen species and hormonal control of cell death.. Trends Plant Sci. 2003; 8: 335-342.
Planchet E., Jagadis Gupta K., Sonoda M., Kaiser W.M. Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport.. Plant J. 2005; 41: 732–743.
Ramamurthi A., Lewis R.S. Measurements and modelling of nitric oxide release rates for nitric oxide donors.. Chem. Res. Toxicol. 1997; 10: 408–413.
Rapoport S. M. The reticulocyte.. Boca Raton, FL: CRC Press; 1986.
Ribeiro E.A.Jr, Cunha F.Q., Tamashiro W.M.S.C., Martins I.S. Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells.. FEBS Letters. 1999; 445: 283–286.
Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 2002; 53: 103–110.
Shi H.-T., Li R.-J., Cai W., Liu W., Fu Z.-W., Lu Y.-T. In vivo role of nitric oxide in plant response to abiotic and biotic stress.. Plant Signal. Behav. 2012; 7(3): 437–439.
Stohr C., Strube F., Marx G., Ullrich W.R., Rockel P. A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite.. Planta. 2001; 212: 835–841.
Stohr C., Ullrich W.R. Generation and possible roles of NO in plant roots and their apoplastic space. J. Exp. Bot. 2002; 53: 2293–2303.
Tanno M., Sueyoshi S., Miyata N., Nakagawa S. Nitric oxide generation from aromatic N-nitrosoureas at ambient temperature.. Chem. Pharm. Bulletin . 1996; 44: 1849–1852.
Tewari R.K., Prommer J., Watanabe M. Endogenous nitric oxide generation in protoplast chloroplasts.. Plant Cell Rep. 2013; 32: 31–44.
Tischner R., Planchet E., Kaiser W.M. Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana.. FEBS Letters. 2004; 576: 151–155.
Xu J, Yin H, Li Y, Liu X. Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum.. Plant Physiol. 2010; 154: 13190–1334.
Yamasaki H. Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2000; 355: 1477–1488.
Yamasaki H., Sakihama Y., Takahashi S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme.. Trends Plant Sci. 1999; 4: 128–129.
Yun B.W., Feechan A., Yin M., Saidi N.B.B., Le Bihan T., Yu M., et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. 2011; 478: 264–268.
Zhao M.G., Chen L, Zhang L.L., Zhang W.H. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. 2009; 151: 755–767.
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2015-06-30
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BIOCHEMISTRY, BIOTECHNOLOGY, MOLECULAR GENETICS
