Photosynthetica 2013, 51(4):483-489 | DOI: 10.1007/s11099-013-0053-y

Effects of exogenous nitric oxide on photosynthesis

D. Procházková1,*, D. Haisel1, N. Wilhelmová1, D. Pavlíková2, J. Száková2
1 Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Prague 6, Czech Republic
2 Department of Agroenvironmental Chemistry and Plant Nutrition, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague 6, Czech Republic

Nitric oxide (NO) is an important signalling molecule with diverse physiological functions in plants. In plant cell, it is synthesised in several metabolic ways either enzymatically or nonenzymatically. Due to its high reactivity, it could be also cytotoxic in dependence on concentration. Such effects could be also mediated by NO-derived compounds. However, the role of NO in photosynthetic apparatus arrangement and in photosynthetic performance is poorly understood as indicated by a number of studies in this field with often conflicting results. This review brings a short survey of the role of exogenous NO in photosynthesis under physiological and stressful conditions, particularly of its effect on parameters of chlorophyll fluorescence.

Additional key words: chlorophyll fluorescence; chloroplast; nitration; nitrotyrosine

Received: March 15, 2013; Accepted: June 26, 2013; Published: December 1, 2013  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Procházková, D., Haisel, D., Wilhelmová, N., Pavlíková, D., & Száková, J. (2013). Effects of exogenous nitric oxide on photosynthesis. Photosynthetica, 51(4), 483-489. doi: 10.1007/s11099-013-0053-y
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Abat, J.K., Mattoo, A.K., Dewal, R.: S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata - ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. - FEBS J. 275: 2862-2872, 2008. Go to original source...
    2. Asada, K.: The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. - Annu. Rev. Plant Physiol. Plant. Mol. Biol. 50: 601-639, 1999. Go to original source...
    3. Barroso, J.B., Corpas, F.J., Carreras, A. et al.: Localization of nitric-oxide synthase in plant peroxisomes. - J. Biol. Chem. 274: 36729-36733, 1999. Go to original source...
    4. Bartesaghi, S., Valez, V., Trujillo, M. et al.: Mechanistic studies of peroxynitrite-mediated tyrosine nitration in membranes using the hydrophobic probe N-t-BOC-L-tyrosine tert-butyl ester. - Biochemistry 45: 6813-6825, 2006. Go to original source...
    5. Beligni, M.V., Lamattina, L.: Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyls elongation, three light inducible responses in plants. - Planta 210: 215-221, 2000. Go to original source...
    6. Bethke, P.C., Badger, M.R., Jones, R.L.: Apoplastic synthesis of nitric oxide by plant tissues. - Plant Cell 16: 332-341, 2004. Go to original source...
    7. Booij-James, I.S., Edelman, M., Mattoo, A.K.: Nitric oxide donor-mediated inhibition of phosphorylation shows that light-mediated degradation of photosystem II D1 protein and phosphorylation are not tightly linked. - Planta 229: 1347-1352, 2009. Go to original source...
    8. Chaki, M., Valderrama, R., Fernández-Ocaña, A.M. et al.: High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. - Plant Cell Environ. 34: 1803-1818, 2011. Go to original source...
    9. Cooney, R.V., Harwood, P.J., Custer, L.J., Franke, A.A.: Lightmediated conversion of nitrogen dioxide to nitric oxide by carotenoids. - Environ. Health Perspect. 102: 460-462, 1994. Go to original source...
    10. Corpas, F.J., del Río, L.A., Barroso, J.B.: Post-translational modification mediated by reactive nitrogen species. - Plant Signals Behav. 5: 301-303, 2008. Go to original source...
    11. Corpas, F.J., Chaki, M., Leterrier, M., Barroso, J.B.: Protein tyrosine nitration. A new challenge in plants. - Plant Signals Behav. 10: 920-923, 2009. Go to original source...
    12. Culotta, E., Koshland, D.E., Jr.: NO news is good news. - Science 258: 1862-1865, 1992. Go to original source...
    13. Ding, F., Wang, X.F., Shi, Q.H. et al.: Exogenous nitric oxide alleviated the inhibition of photosynthesis and antioxidant enzyme activities in iron-deficient Chinese cabbage (Brassica chinensis L.). - Agr. Sci. China 7: 168-179, 2008. Go to original source...
    14. Ederli, L., Reale, L., Madeo, L. et al.: NO release by nitric oxide donors in vitro and in planta. - Plant Physiol. Biochem. 47: 42-48, 2009. Go to original source...
    15. Fan, H.F., Duc, X., Zhu, Z.J.: Effects of exogenous nitric oxide on plant growth, membrane lipid peroxidation and photosynthesis in cucumber seedling leaves under low temperature. - Hort. Sci. 23: 538-542, 2011.
    16. Fedoroff, N.: Redox regulatory mechanisms in cellular stress responses. - Ann. Bot. 98: 289-300, 2006. Go to original source...
    17. Ferreira, F.J., Guo, C., Coleman J.R.: Reduction of plastidlocalized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship. - Plant Physiol. 147: 585-594, 2008. Go to original source...
    18. Foissner, I., Wendehenne, D., Langebartels, C., Durner, J.: In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. - Plant J. 23: 817-824, 2000. Go to original source...
    19. Galetskiy, D, Lohscheider, J.N., Kononikhin, A.S., et al.: Mass spectrometric characterization of photooxidative protein modifications in Arabidopsis thaliana thylakoid membranes. - Rapid Commun. Mass Sp. 25: 184-190, 2011a. Go to original source...
    20. Galetskiy, D., Lohscheider, J.N., Kononikhin, A.S., Popov, I.A., Nikolaev, E.N., Adamska, I.: Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. - Plant Mol. Biol. 77: 461-473, 2011b. Go to original source...
    21. Gao, Z., Lin, Y., Wang, X. et al.: Sodium nitroprusside (SNP) alleviates the oxidative stress induced by NaHCO3 and protects chloroplast from damage in cucumber. - Afr. J. Biotechnol. 11: 6974-6982, 2012. Go to original source...
    22. García-Mata, C., Lamattina, L.: Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. - Plant Physiol. 126: 1196-1204, 2001. Go to original source...
    23. Gas, E., Flores-Pérez, Ú., Sauret-Güeto, S., Rodríguez-Concepción, M.: Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. - Plant Cell 21: 18-23, 2009. Go to original source...
    24. Gill, S.S., Hasanuzzaman, M., Nahar, K., Macovei, A., Tuteja, N.: Importance of nitric oxide in cadmium stress tolerance in crop plants. - Plant Physiol. Biochem. 63: 254-261, 2013. Go to original source...
    25. González-Pérez, S., Quijano, C., Romero, N. et al.: Peroxynitrite inhibits electron transport on the acceptor side of higher plant photosystem II. - Arch. Biochem. Biophys. 473:25-33, 2008. Go to original source...
    26. Gould, K.S., Lamotte, O., Klinguer, A. et al.: Nitric oxide production in tobacco leaf cells: a generalized stress response? - Plant Cell Environ. 26: 1851-1862, 2003. Go to original source...
    27. Graziano, M., Beligni, M.V., Lamattina, L.: Nitric oxide improves internal iron availability in plants. - Plant Physiol. 130: 1852-1859, 2002. Go to original source...
    28. Griebel, T., Zeier, J.: Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signalling controls systemic acquired resistance rather than local defense. - Plant Physiol. 147: 790-801, 2008. Go to original source...
    29. Hayat, S., Yadav, S., Ali, B., Ahmad, A.: Interactive effect of nitric oxide and brassinosteroids on photosynthesis and the antioxidant system of Lycopersicon esculentum. - Russ. J. Plant Physiol. 57: 212-221, 2010. Go to original source...
    30. He, Y., Tang, R.H., Hao, Y. et al.: Nitric oxide represses the Arabidopsis floral transition. - Science 24: 1968-1971, 2004. Go to original source...
    31. Heckathorn, S.A., Mueller, K., LaGuidice, S. et al.: Chloroplast small heat-shock proteins protect photosynthesis during heavy metal stress. - Amer. J. Bot. 91: 1312-1318, 2004. Go to original source...
    32. Hill, A.C., Bennett, J.H.: Inhibition of apparent photosynthesis by nitrogen oxides. - Atmos. Environ. 4, 341-348, 1970. Go to original source...
    33. Hirotsu, N., Makino, A., Ushio, A., Mae, T.: Changes in the thermal dissipation and the electron flow in the water-water cycle in rice grown under conditions of physiologically low temperature. - Plant Cell Physiol. 45: 635-644, 2004. Go to original source...
    34. Hogg, N.: Biological chemistry and clinical potential of Snitrosothiols. - Free Radic. Biol. Med. 28: 1478-1486, 2000. Go to original source...
    35. Hsu, Y.T., C.H. Kao, C.H.: Cadmium toxicity is reduced by nitric oxide in rice leaves. - Plant Growth Regul. 42: 227-238, 2004. Go to original source...
    36. Hu, X., Neill S.J., Tang, Z., Cai, W.: Nitric oxide mediates gravitropic bending in soybean roots. - Plant Physiol. 137: 663-670, 2005. Go to original source...
    37. Jasid, S., Simontacchi, M., Bartoli, C.S., Puntarulo, S.: Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. - Plant. Physiol. 142: 1246-1255, 2006. Go to original source...
    38. Jhanji, S., Setia, R.C., Kaur, N. et al.: Role of nitric oxide in cadmium-induced stress on growth, photosynthetic components and yield of Brassica napus L. - J. Environ. Biol. 33: 1027-1032, 2012.
    39. Kangasjärvi, S., Neukermans, J., Li, S. et al.: Photosynthesis, photorespiration, and light signalling in defence responses. - J. Exp. Bot. 63: 1619-1636, 2012. Go to original source...
    40. Kazemi, N., Khavar-Nejad, R.A., Fahimi, H. et al.: Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. - Sci. Hortic-Amsterdam 126: 402-407, 2010. Go to original source...
    41. Knowles, R.G., Moncada, S.: Nitric oxide synthases in mammals. - Biochem. J. 298: 249-258, 1994. Go to original source...
    42. Kumar, H., Sharma, D., Kumar, V.: Nickel induced oxidative stress and role of antioxidant defence in barley roots and leaves. - Int. J. Environ. Biol. 2: 121-128, 2012.
    43. Lamattina, L., García-Mata, C., Graziano, M., Pagnussat, G.: Nitric oxide: The versatility of an extensive signal molecule. - Annu. Rev. Plant Biol. 54: 109-136, 2003. Go to original source...
    44. Lancaster, J.R.,Jr: Diffusion of free nitric oxide. - Meth. Enzymol. 268: 31-50, 1996. Go to original source...
    45. Laspina, N.V., Groppa, M.D., Tomaro, M.L., Benavides, M.P.: Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. - Plant Sci. 169: 323-330, 2005. Go to original source...
    46. Liu, J., Wang, J., Wang, X., Wang, X., Wang, R.: Regulation of exogenous nitric oxide on photosynthetic physiological response of Lolium perenne seedlings under NaHCO3 stress. - Acta Ecol. Sinica 32: 3460-3466, 2012. Go to original source...
    47. Lum, H.-K., Lee, C.-H., Butt, Y.K.-C., Lo, S.C.-L.: Sodium nitroprusside affects the level of photosynthetic enzymes and glucose metabolism in Phaseolus aureus (mung bean). - Nitric Oxide-Biol. Ch. 12: 220-230, 2005. Go to original source...
    48. Murgia, I., de Pinto, M.C., Delledonne, M., Soave, C., de Gara, L.: Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and redox state in plant cells. - J. Plant Physiol. 161: 777-783, 2004. Go to original source...
    49. Ördög, A., Wodala, B., Rózsavölgyi, T., et al.: Regulation of guard cell photosynthetic electron transport by nitric oxide. - J. Exp. Bot. 64: 1357-1366, 2013. Go to original source...
    50. Planchet, E., Gupta, J.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. 41: 732-743, 2005. Go to original source...
    51. Procházková, D., Wilhelmová, N.: Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. - Nitric Oxide-Biol. Ch. 24: 61-65, 2011. Go to original source...
    52. Puntarulo, S., Jasid, S., Simontacchi, M.: Reactive nitrogen species-dependent effects on soybean chloroplasts. - Plant Signals Behav. 2: 96-98, 2007. Go to original source...
    53. Radi, R.: Peroxynitrite reactions and diffusion in biology. - Chem. Res. Toxicol. 11: 720-721, 1998. Go to original source...
    54. Ramamurthi, A., Lewis, R.S.: Measurements and modelling of nitric oxide release rates for nitric oxide donors. - Chem. Res. Toxicol. 10: 408-413, 1997. Go to original source...
    55. Roberts, M.R., Paul, N.D.: Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. - New Phytol. 170: 677-699, 2006. Go to original source...
    56. Rodrigo, J., Springall, D.R., Uttenthal, O., Bentura, M.L., Abadia-Molina, F., Riveros Moreno, V., Martinez-Murillo, R., Polak, J.M., Moncada, S.: Locations of nitric oxide synthase in the adult rat brain. - Philos. T. Roy Soc. B 345: 175-221, 1994. Go to original source...
    57. Sanakis, Y., Goussias, C., Mason, R.P., Petrouleas, V.: NO interacts with the tyrosine radical YD. of photosystem II to form an iminoxyl radical. - Biochemistry 36: 1411-1417, 1997. Go to original source...
    58. Saxe, H.: Stomatal-dependent and stomatal-independent uptake of NOx. - New Phytol. 103: 199-205, 1986. Go to original source...
    59. Shi, S.Y., Wang, G., Wang, Y.D. et al.: Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. - Nitric Oxide-Biol. Ch. 13: 1-9, 2005. Go to original source...
    60. Snyder, S.H.: Nitric oxide: first in a new class of neurotransmitters. - Science 257: 494-496, 1992. Go to original source...
    61. Stöhr, C., Strube, F., Marx, G. et al.: A plasma membranebound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. - Planta 212: 835-841, 2001. Go to original source...
    62. Takahashi, S., Yamasaki, H.: Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. - FEBS Lett. 512: 145-148, 2002. Go to original source...
    63. Tan, J.H., Zhao, J., Hong, Y. et al.: Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and praline accumulation in wheat seedlings subjected to osmotic stress. - World J. Agr. Sci. 4: 307-313, 2008.
    64. Tanno, M., Sueyoshi, S., Miyata, N., Nakagawa S.: Nitric oxide generation from aromatic N-nitrosoureas at ambient temperature. - Chem. Pharm. Bull. 44: 1849-1852, 1996. Go to original source...
    65. Tewari, R.K., Kumar, P., Kim, S. et al.: Nitric oxide retards xanthine oxidase-mediated superoxide anion generation in Phalaenopsis flower: an implication of NO in the senescence and oxidative stress regulation. - Plant Cell Reports 28: 267-279, 2009. Go to original source...
    66. Tewari, R.K., Prommer, J., Watanabe, M.: Endogenous nitric oxide generation in protoplast chloroplasts. - Plant Cell. Rep. 32: 31-44, 2013. Go to original source...
    67. Uchida, A., Jagendorf, A.T., Hibino, T. et al.: Effects of hydrogen peroxide and nitric oxide on both salt and heat tolerance in rice. - Plant Sci. 163: 515-523, 2002. Go to original source...
    68. Vladkova, R., Dobrikova, A.G., Singh, R. et al.: Photoelectron transport ability of chloroplast thylakoid membranes treated with NO donor SNP: changes in flash oxygen evolution and chlorophyll fluorescence. - Nitric Oxide-Biol. Ch. 24: 84-90, 2011. Go to original source...
    69. Wang, M., Li, Q., Fu, S., Dong, B.: [Effects of exogenous nitric oxide on photosynthetic characteristics of poplar leaves under water stress.] - Ying Yong Sheng Tai Xue Bao: 16: 218-222, 2005. [In Chinese] Go to original source...
    70. Wendehenne, D., Pugin A., Klessig D.F., Durner, J.: Nitric oxide: comparative synthesis and signalling in animal and plant cells. - Trends Plant Sci. 4: 177-183, 2001. Go to original source...
    71. Wilhelmová, N., Fuksová, H., Srbová, M. et al.: The effect of plant cytokinin hormones on the production of ethylene, nitric oxide, and protein nitrotyrosine in ageing tobacco leaves. - BioFactors 27: 203-211, 2006. Go to original source...
    72. Wilson, I.D., Neill, S.J., Hancock, J.T.: Nitric oxide synthesis and signalling in plants. - Plant Cell Environ. 31: 622-631, 2008. Go to original source...
    73. Wodala, B., Deák, Z., Vass, I. et al.: In vivo target sites of nitric oxide in photosynthetic electron transport as studied by chlorophyll fluorescence in pea leaves. - Plant Physiol. 146: 1920-1927, 2008. Go to original source...
    74. Wodala, B., Deák, Z., Vass, I. et al.: Nitric oxide modifies photosynthetic electron transport in pea leaves. - Acta Biol. Szeged. 49: 7-8, 2005.
    75. Wu, X.X., Ding, H.D., Chen, J.L. et al.: Attenuation of saltinduced changes in photosynthesis by exogenous nitric oxide in tomato (Lycopersicon esculentum Mill. L.) seedlings. - Afr. J. Biotech. 9: 7837-7846, 2010. Go to original source...
    76. Xiong, J., An, L., Lu, H., Zhu, C.: Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. - Planta 230: 755-765, 2009. Go to original source...
    77. Xiong, J., Fu, G., Tao, L., Zhu, C.: Roles of nitric oxide in alleviating heavy metal toxicity in plants. - Arch. Biochem. Biophys. 497: 13-20, 2010. Go to original source...
    78. Yamasaki, H.: Nitrite dependent nitric oxide production pathway: implication for involvement of active nitrogen species in photoinhibition in vivo. - Philos. T. Roy Soc. B 355: 1477-1488, 2000. Go to original source...
    79. Yang, J.D., Zhao, H.L., Zhang, T.H., Yun, J.F.: Effects of exogenous nitric oxide on photochemical activity of photosystem II in potato leaf tissue under non-stress condition. - Acta Bot. Sin. 46: 1009-1014, 2004.
    80. Yang, W., Sun, Y., Chen, S. et al.: The effect of exogenously applied nitric oxide on photosynthesis and antioxidant activity in heat stressed chrysanthemum. - Biol. Plant. 55: 737-740, 2011. Go to original source...
    81. Zhang, Z., Davies, L.R., Martin, S.M. et al.: The nitric oxide donor S-nitroso-N-acetylpenicillamine (SNAP) increases free radical generation and degrades left ventricular function after myocardial ischemic-reperfusion. - Resuscitation 59: 345-352, 2003. Go to original source...
    82. Zottini, M., Formentin, E., Scattolin M. et al.: Nitric oxide affects plant mitochondrial functionality in vivo. - FEBS Lett. 515: 75-78, 2002. Go to original source...

    Return to the content