Skip to main content
Log in

Effects of exogenous nitric oxide on photosynthesis

  • Review
  • Published:
Photosynthetica

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Arg:

arginine

DAF-2DA:

diaminofluorescein diacetate

Chl:

chlorophyll

Fv/Fm :

maximal quantum yield of PSII photochemistry

Fv :

variable fluorescence

GSNO:

S-nitrosoglutathione

L-NNA:

(Nω-nitro-L-arginine)

NOS:

nitric oxide synthase

NPQ:

nonphotochemical chlorophyll fluorescence quenching

PBIT:

S,S′-1,3-phenylene-bis(1,2-ethanediyl)-bisisothiourea

PS:

photosystem

qE :

energy dependent quenching of chlorophyll fluorescence

qN :

nonphotochemical quenching of Fv

qp :

photochemical quenching of Fv

RNS:

reactive nitrogen species

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

SNAP:

S-nitroso-N-acetylpenicillamine

SNP:

sodium nitroprusside

ϕPSII :

effective quantum yield of photochemical energy conversion in PSII

References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bethke, P.C., Badger, M.R., Jones, R.L.: Apoplastic synthesis of nitric oxide by plant tissues. — Plant Cell 16: 332–341, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Culotta, E., Koshland, D.E., Jr.: NO news is good news. — Science 258: 1862–1865, 1992.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Fedoroff, N.: Redox regulatory mechanisms in cellular stress responses. — Ann. Bot. 98: 289–300, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Graziano, M., Beligni, M.V., Lamattina, L.: Nitric oxide improves internal iron availability in plants. — Plant Physiol. 130: 1852–1859, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • He, Y., Tang, R.H., Hao, Y. et al.: Nitric oxide represses the Arabidopsis floral transition. — Science 24: 1968–1971, 2004.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hill, A.C., Bennett, J.H.: Inhibition of apparent photosynthesis by nitrogen oxides. — Atmos. Environ. 4, 341–348, 1970.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Hogg, N.: Biological chemistry and clinical potential of Snitrosothiols. — Free Radic. Biol. Med. 28: 1478–1486, 2000.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hu, X., Neill S.J., Tang, Z., Cai, W.: Nitric oxide mediates gravitropic bending in soybean roots. — Plant Physiol. 137: 663–670, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Kangasjärvi, S., Neukermans, J., Li, S. et al.: Photosynthesis, photorespiration, and light signalling in defence responses. — J. Exp. Bot. 63: 1619–1636, 2012.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Knowles, R.G., Moncada, S.: Nitric oxide synthases in mammals. — Biochem. J. 298: 249–258, 1994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Lancaster, J.R.,Jr: Diffusion of free nitric oxide. — Meth. Enzymol. 268: 31–50, 1996.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Procházková, D., Wilhelmová, N.: Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. — Nitric Oxide-Biol. Ch. 24: 61–65, 2011.

    Article  Google Scholar 

  • Puntarulo, S., Jasid, S., Simontacchi, M.: Reactive nitrogen species-dependent effects on soybean chloroplasts. — Plant Signals Behav. 2: 96–98, 2007.

    Article  Google Scholar 

  • Radi, R.: Peroxynitrite reactions and diffusion in biology. — Chem. Res. Toxicol. 11: 720–721, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Ramamurthi, A., Lewis, R.S.: Measurements and modelling of nitric oxide release rates for nitric oxide donors. — Chem. Res. Toxicol. 10: 408–413, 1997.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Saxe, H.: Stomatal-dependent and stomatal-independent uptake of NOx. — New Phytol. 103: 199–205, 1986.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Snyder, S.H.: Nitric oxide: first in a new class of neurotransmitters. — Science 257: 494–496, 1992.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Takahashi, S., Yamasaki, H.: Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. — FEBS Lett. 512: 145–148, 2002.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Tanno, M., Sueyoshi, S., Miyata, N., Nakagawa S.: Nitric oxide generation from aromatic N-nitrosoureas at ambient temperature. — Chem. Pharm. Bull. 44: 18491852, 1996.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Tewari, R.K., Prommer, J., Watanabe, M.: Endogenous nitric oxide generation in protoplast chloroplasts. — Plant Cell. Rep. 32: 31–44, 2013.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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]

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Wilson, I.D., Neill, S.J., Hancock, J.T.: Nitric oxide synthesis and signalling in plants. — Plant Cell Environ. 31: 622–631, 2008.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wodala, B., Deák, Z., Vass, I. et al.: Nitric oxide modifies photosynthetic electron transport in pea leaves. — Acta Biol. Szeged. 49: 7–8, 2005.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zottini, M., Formentin, E., Scattolin M. et al.: Nitric oxide affects plant mitochondrial functionality in vivo. — FEBS Lett. 515: 75–78, 2002.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Procházková.

Additional information

Acknowledgements: This research was supported by Grant Agency of the Czech Republic, Grant No. P501/11/1239.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Procházková, D., Haisel, D., Wilhelmová, N. et al. Effects of exogenous nitric oxide on photosynthesis. Photosynthetica 51, 483–489 (2013). https://doi.org/10.1007/s11099-013-0053-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-013-0053-y

Additional key words

Navigation