Russian Journal of Plant Physiology

, Volume 64, Issue 2, pp 207–214 | Cite as

Effect of nitric oxide donor on salt resistance of Arabidopsis jin1 mutants and wild-type plants

  • T. O. Yastreb
  • Yu. E. Kolupaev
  • Yu. V. Karpets
  • A. P. Dmitriev
Research Papers


The effect of NO donor sodium nitroprusside (SNP) on salt resistance of 4-week-old Arabidopsis thaliana L. wild-type Columbia-0 (Col-0) plants and jin1 mutants defective in the jasmonate signaling have been investigated. As affected by 0.5 mM, SNP salt resistance of wild-type plants rose, which was exhibited in a smaller growth inhibition and preserving the pool of photosynthetic pigments after salt stress (200 mM NaCl). The positive effect of SNP leveled by treatment of plant with NO scavenger: 0.5 mM PTIO (2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide). However, SNP treatment had no significant effect on the salt tolerance of jin1 genotype plants. In the case of wild-type plants but not jin1 mutants, treatment by NO donor increased activity of antioxidant enzymes—superoxide dismutase, guaiacol peroxidase, and catalase—in the leaves, which was especially noticeable in salt stress conditions. In wild-type plants treated by NO donor, proline content in the leaves after salt stress was lower and sugar content was higher than that in the untreated ones. In jin1 mutants, NO donor treatment resulted in a significant increase in proline content in the leaves under salt stress, without changing sugar content. A conclusion was made on the participation of transcript factor JIN1/MYC2 in NO-dependent induction of some plant defense responses to salt stress.


Arabidopsis thaliana nitric oxide salt resistance antioxidant enzymes compatible osmolytes transcript factor JIN1/MYC2 



2-phenyl-4,4,5,5-tetramethylimidazoline- 1-oxyl-3-oxide (NO scavenger)


guaiacol peroxidase




sodium nitroprusside (NO donor)


superoxide dismutase


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Ziogas, V., Tanou, G., Filippou, P., Diamantidis, G., Vasilakakis, M., Fotopoulos, V., and Molassiotis, A., Nitrosative responses in citrus plants exposed to six abiotic stress conditions, Plant Physiol. Biochem., 2013, vol. 68, pp. 118–126.CrossRefPubMedGoogle Scholar
  2. 2.
    Zhao, M.G., Chen, L., Zhang, L.L., and Zhang, W.H., Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis, Plant Physiol., 2009, vol. 151, pp. 755–767.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Karpets, Yu.V., Kolupaev, Yu.E., and Vainer, A.A., Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance, Russ. J. Plant Physiol., 2015, vol. 62, pp. 65–70.CrossRefGoogle Scholar
  4. 4.
    Zhao, M.G., Tian, Q.Y., and Zhang, W.H., Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis, Plant Physiol., 2007, vol. 144, pp. 206–217.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Shi, H.T., Li, R.J., Cai, W., Liu, W., Wang, C.L., and Lu, Y.T., Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance, Plant Cell Physiol., 2012, vol. 53, pp. 344–357.CrossRefPubMedGoogle Scholar
  6. 6.
    Tan, J., Zhao, H., Hong, J., Han, Y., Li, H., and Zhao, W., Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline accumulation in wheat seedlings subjected to osmotic stress, World J. Agric. Sci., 2008, vol. 4, pp. 307–313.Google Scholar
  7. 7.
    Kholodova, V.P., Grinin, A.L., Bashmakova, E.B., Meshcheryakov, A.B., and Kuznetsov, Vl.V., NO-dependent accumulation of inorganic ions and proline determines the protective effect of nitric oxide on mustard growth under the conditions of salinization, Dokl. Biol. Sci., 2011, vol. 439, pp. 236–239.CrossRefPubMedGoogle Scholar
  8. 8.
    Wu, X., Zhu, W., Zhang, H., Ding, H., and Zhang, H.J., Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicon esculentum Mill.), Acta Physiol. Plant., 2011, vol. 33, pp. 1199–1209.CrossRefGoogle Scholar
  9. 9.
    Siddiqui, M.H., Al-Whaibi, M.H., and Basalah, M.O., Role of nitric oxide in tolerance of plants to abiotic stress, Protoplasma, 2011, vol. 248, pp. 447–455.CrossRefPubMedGoogle Scholar
  10. 10.
    Shi, H., Ye, T., Zhu, J.K., and Chan, Z., Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis, J. Exp. Bot., 2014, vol. 65, pp. 4119–4131.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Mamaeva, A.S., Fomenkov, A.A., Nosov, A.V., Moshkov, I.E., Mur, L.A.J., Hall, M.A., and Novikova, G.V., Regulatory role of nitric oxide in plants, Russ. J. Plant Physiol., 2015, vol. 62, pp. 427–440.CrossRefGoogle Scholar
  12. 12.
    Zhang, A., Jiang, M., Zhang, J., Ding, H., Xu, S., Hu, X., and Tan, M., Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves, New Phytol., 2007, vol. 175, pp. 36–50.CrossRefPubMedGoogle Scholar
  13. 13.
    Liang, X., Zhang, L., Natarajan, S.K., and Becker, D.F., Proline mechanisms of stress survival, Antioxid. Redox Signal., 2013, vol. 19, pp. 998–1011.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    López-Carrión, A.I., Castellano, R., Rosales, M.A., Ruiz, J.M., and Romero, L., Role of nitric oxide under saline stress: implications on proline metabolism, Biol. Plant., 2008, vol. 52, pp. 587–591.CrossRefGoogle Scholar
  15. 15.
    Ton, J., Flors, V., and Mauch-Mani, B., The multifaceted role of ABA in disease resistance, Trends Plant Sci., 2009, vol. 14, pp. 310–317.CrossRefPubMedGoogle Scholar
  16. 16.
    Lackman, P., González-Guzmán, M., Tilleman, S., Carqueijeiro, I., Pérez, A.C., Moses, T., Seo, M., Kanno, Y., Häkkinen, S.T., Montagu, M.C.E.V., Thevelein, J.M., Maaheimo, H., Oksman-Caldentey, K.M., Rodriguez, P.L., Rischer, H., et al., Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco, Proc. Natl. Acad. Sci. USA, 2011, vol. 108, pp. 5891–5896.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Palmieri, M.C., Sell, S., Huang, X., Scherf, M., Werner, T., Durner, J., and Lindermayr, C., Nitric oxideresponsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach, J. Exp. Bot., 2008, vol. 59, pp. 177–186.CrossRefPubMedGoogle Scholar
  18. 18.
    Huang, X., Stettmaier, K., Michel, C., Hutzler, P., Mueller, M.J., and Durner, J., Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana, Planta, 2004, vol. 218, pp. 938–946.CrossRefPubMedGoogle Scholar
  19. 19.
    Shan, C., Zhou, Y., and Liu, M., Nitric oxide participates in the regulation of the ascorbate–glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress, Protoplasma, 2015, vol. 252, pp. 1397–1405.CrossRefPubMedGoogle Scholar
  20. 20.
    Gibeaut, D.M., Hulett, J., Cramer, G.R., and Seemann, J.R., Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions, Plant Physiol., 1997, vol. 115, pp. 317–319.PubMedGoogle Scholar
  21. 21.
    Yastreb, T.O., Kolupaev, Yu.E., Lugovaya, A.A., and Dmitriev, A.P., Content of osmolytes and flavonoids under salt stress in Arabidopsis thaliana plants defective in jasmonate signaling, Appl. Biochem. Microbiol., 2016, vol. 52, pp. 210–215.CrossRefGoogle Scholar
  22. 22.
    Shlyk, A.A., Determination of chlorophylls and carotenoids in extracts of green leaves, Biokhimicheskie metody v fiziologii rastenii (Biochemical Methods in Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971, pp. 154–170.Google Scholar
  23. 23.
    Karpets, Yu.V., Kolupaev, Yu.E., Lugovaya, A.A., and Oboznyi, A.I., Effect of jasmonic acid on the pro- /antioxidant system of wheat coleoptiles as related to hyperthermia tolerance, Russ. J. Plant Physiol., 2014, vol. 61, pp. 339–346.CrossRefGoogle Scholar
  24. 24.
    Alscher, R.G., Erturk, N., and Heath, L.S., Role of superoxide dismutases (SODs) in controlling oxidative stress in plants, J. Exp. Bot., 2002, vol. 53, pp. 1331–1341.CrossRefPubMedGoogle Scholar
  25. 25.
    Bates, L.S., Walden, R.P., and Tear, G.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, pp. 205–210.CrossRefGoogle Scholar
  26. 26.
    Kolupaev, Yu.E., Ryabchun, N.I., Vayner, A.A., Yastreb, T.O., and Oboznyi, A.I., Antioxidant enzyme activity and osmolyte content in winter cereal seedlings under hardening and cryostress, Russ. J. Plant Physiol., 2015, vol. 62, pp. 499–506.CrossRefGoogle Scholar
  27. 27.
    Merzlyak, M.N., Pogosyan, S.I., Yuferova, S.G., and Shevyreva, V.A., The use of 2-thiobarbituric acid in the study of lipid peroxidation in plant tissues, Biol. Nauki, 1978, no. 9, pp. 86–94.Google Scholar
  28. 28.
    Kartashov, A.V., Radyukina, N.L., Ivanov, Yu.V., Pashkovskii, P.P., Shevyakova, N.I., and Kuznetsov, Vl.V., Role of antioxidant systems in wild plant adaptation to salt stress, Russ. J. Plant Physiol., 2008, vol. 55, pp. 463–468.CrossRefGoogle Scholar
  29. 29.
    de Carvalho, K., de Campos, M.K.F., Domingues, D.S., Pereira, L.F.P., and Vieira, L.G.V., The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo, Mol. Biol. Rep., 2013, vol. 40, pp. 3269–3279.CrossRefPubMedGoogle Scholar
  30. 30.
    Sin’kevich, M.S., Deryabin, A.N., and Trunova, T.I., Characteristics of oxidative stress in potato plants with modified carbohydrate metabolism, Russ. J. Plant Physiol., 2009, vol. 56, pp. 168–174.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2017

Authors and Affiliations

  • T. O. Yastreb
    • 1
  • Yu. E. Kolupaev
    • 1
  • Yu. V. Karpets
    • 1
  • A. P. Dmitriev
    • 2
  1. 1.Dokuchaev National Agrarian UniversityKharkivUkraine
  2. 2.Institute of Cell Biology and Genetic EngineeringNational Academy of Sciences of UkraineKyivUkraine

Personalised recommendations