Abstract
The effect of donors of hydrogen sulfide (50 μM sodium hydrosulfide NaHS) and nitric oxide (500 μM sodium nitroprusside, SNP) on the salt resistance of wild type (Col-0) Arabidopsis plants (A-rabidopsis thaliana L. Heynh.) and those defective in jasmonate signaling—coi1 (mutant for the gene encoding protein COI1 involved in the removal of repressor proteins of transcriptional factors of jasmonate signaling) and jin1 (mutant defective in the gene encoding the transcription factor JIN1/MYC2)—have been compared. NO and H2S donors had a similar positive effect on the salt resistance of wild-type plants, which was manifested in a decrease under their influence of water deficiency of leaves, a decrease in oxidative damage, and stabilization of membrane permeability and chlorophyll content under the influence of 175 mM NaCl. The activity of superoxide dismutase (SOD) and catalase (CAT) also increased under the influence of NaHS and SNP treatment during salinization in Col-0 plants but the stress-induced accumulation of proline decreased. Pretreatment of coi1 and jin1 mutants with NO and H2S donors did not prevent the increase in lipid peroxidation caused by the action of NaCl and did not contribute to a decrease in membrane permeability and preservation of the pool of chlorophylls under stress conditions. In both mutants treated with NaHS or SNP, there was no increase in the activity of SOD and CAT under the action of salt. Donor treatment of NO and H2S did not affect the magnitude of the water deficit and the content of proline in the leaves of the mutant jin1. However, the mutant coi1 presalt treatment with NaHS or SNP reduced the manifestation of water deficiency and proline accumulation. The conclusion is drawn on the involvement of jasmonate signaling components in the implementation of the stress-protective action of donors of hydrogen sulfide and nitric oxide. It is assumed that the transcription factor JIN1/MYC2 plays a more important role in the processes of salt resistance induction of Arabidopsis plants by exogenous NO and H2S compared to protein COI1.
Similar content being viewed by others
REFERENCES
Yamasaki, H. and Cohen, M.F., Biological consilience of hydrogen sulfide and nitric oxide in plants: gases of primordial earth linking plant, microbial and animal physiologies, Nitric Oxide, 2016, vols. 55–56, p. 91.
Kolupaev, Yu.E., Karpets, Yu.V., Beschasniy, S.P., and Dmitriev, A.P., Gasotransmitters and their role in adaptive reactions of plant cells, Cytol. Genet., 2019, vol. 53, p. 392.
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, p. 236.
Chen, J., Wang, W.H., Wu, F.H., He, E.M., Liu, X., Shangguan, Z.P., and Zheng, H.L., Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots, Sci. Rep., 2015, vol. 5, p. 12516. https://doi.org/10.1038/srep12516
Shan, C., Wang, T., Zhou, Y., and Wang, W., Hydrogen sulfide is involved in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Arabidopsis thaliana,Biol. Plant., 2018, vol. 62, p. 188.
Maslennikova, D.R., Allagulova, Ch.R., Fedorova, K.A., Plotnikov, A.A., Aval’baev, A.M., and Shakirova, F.M., Cytokinins contribute to realization of nitric oxide growth-stimulating and protective effects on wheat plants, Russ. J. Plant Physiol., 2017, vol. 64, p. 665.
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, p. 938.
Banerjee, A., Tripathi, D.K., and Roychoudhury, A., Hydrogen sulphide trapeze: environmental stress amelioration and phytohormone crosstalk, Plant Physiol. Biochem., 2018, vol. 132, p. 46.
Barrera-Ortiz, S., Garnica-Vergara, A., Esparza-Reynoso, S., García-Cárdenas, E.,·Raya-González, J., Ruiz-Herrera, L.F.,·and López-Bucio, J., Jasmonic acid-ethylene crosstalk via ETHYLENE INSENSITIVE 2 reprograms Arabidopsis root system architecture through nitric oxide accumulation, J. Plant Growth Regul., 2018, vol. 37, p. 438.
Li, H., Li, M., Wei, X., Zhang, X., Xue, R., Zhao, Y., and Zhao, H., Transcriptome analysis of drought-responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves, Mol. Genet. Genomics, 2017, vol. 292, p. 1091.
Corpas, F.J., González-Gordo, S., Canas, A., and Palma, J.M., Nitric oxide (NO) and hydrogen sulfide (H2S) in plants: which is first? J. Exp. Bot., 2019, vol. 70, p. 4391.
Paul, S. and Roychoudhury, A., Regulation of physiological aspects in plants by hydrogen sulfide and nitric oxide under challenging environment, Physiol. Plant., 2020, vol. 168, p. 374. https://doi.org/10.1111/ppl.13021
Ton, J., Flors, V., and Mauch-Mani, B., The multifaceted role of ABA in disease resistance, Trends Plant Sci., 2009, vol. 14, p. 310.
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, p. 5891.
Palmieri, M.C., Sell, S., Huang, X., Scherf, M., Werner, T., Durner, J., and Lindermayr, C., Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach, J. Exp. Bot., 2008, vol. 59, p. 177.
Yastreb, T.O., Kolupaev, Yu.E., Karpets, Yu.V., and Dmitriev, A.P., Effect of nitric oxide donor on salt resistance of Arabidopsis jin1 mutants and wild-type plants, Russ. J. Plant Physiol., 2017, vol. 64, p. 207.
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, p. 210.
Goncharova, E.A., Vodnyi status kul’turnykh rastenii i ego diagnostika (Water Status of Cultivated Plants and Its Diagnosis), St. Petersburg: Vavilov Res. Inst. Plant Industry, 2005.
Khokhlova, L.P., Valiullina, R.N., Mider, D.R., and Akberova, N.I., Membrane thermostability and gene expression of small heat-shock protein (sHSP) in wheat shoots exposed to elevated temperatures and water deficiency. Biol. Membr., 2015, vol. 32, p. 59.
Shlyk, A.A., Shlyk, A.A., Determining chlorophylls and carotenoids in extracts of green leaves, in Biokhimicheskie netody v fiziologii rastenii (Biochemical Methods in Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971.
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, p. 1331.
Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 1976, vol. 72, p. 248.
Bates, L.S., Walden, R.P., and Tear, G.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, p. 205.
Shi, H., Ye, T., Han, N., Bian, H., Liu, X., and Chan, Z.J., Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis, Integr.Plant Biol., 2015, vol. 57, p. 628.
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 (Lycopersicom esculentum Mill.), Acta Physiol. Plant., 2011, vol. 33, p. 1199.
Kuznetsov, Vl.V. and Shevyakova, N.I., Proline under stress: biological role, metabolism, and regulation, Russ. J. Plant Physiol., 1999, vol. 46, p. 274.
Shevyakova, N.I., Bakulina, E.A., and Kuznetsov, Vl.V., Proline antioxidant role in the common ice plant subjected to salinity and paraquat treatment inducing oxidative stress, Russ. J. Plant Physiol., 2009, vol. 56, p. 663.
Li, Z.G., Yang, S.Z., Long, W.B., Yang, G.X., and Shen, Z.Z., Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings, Plant Cell Envir-on., 2013, vol. 36, p. 1564.
Scuffi, D., Álvarez, C., Laspina, N., Gotor, C., Lamattina, L., and García-Mata, C., Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure, Plant Physiol., 2014, vol. 166, p. 2065.
Xing, H., Tan, L., An, I., Zhao, Z., Wang, S., and Zhang, C., Evidence for the involvement of nitric oxide and reactive oxygen species in osmotic stress tolerance of wheat seedlings: inverse correlation between leaf abscisic acid accumulation and leaf water loss, Plant Growth Regul., 2004, vol. 42, p. 61.
Funding
This work was carried out as part of the Role of Signaling Mediators and Compounds with Hormonal Activity in the Formation of Adaptive Plant Responses to Abiotic Stressors project funded by the state budget of Ukraine (state registration no. 0117U002427).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
COMPLIANCE WITH ETHICAL STANDARDS
This article does not contain any research involving humans and animals as research objects.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
Additional information
Abbreviations: PTIO—2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (NO scavenger); CAT—catalase; SNP—sodium nitroprusside (NO donor); SOD—superoxide dismutase.
Rights and permissions
About this article
Cite this article
Yastreb, T.O., Kolupaev, Y.E., Shkliarevskyi, M.A. et al. Participation of Jasmonate Signaling Components in the Development of Arabidopsis thaliana’s Salt Resistance Induced by H2S and NO Donors. Russ J Plant Physiol 67, 827–834 (2020). https://doi.org/10.1134/S1021443720050192
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443720050192