Skip to main content
SpringerLink
Log in

Regulation of protein phosphorylation by nitric oxide in cell culture of Arabidopsis thaliana

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Effect of nitric oxide (NO) on phosphorylation of soluble proteins in the cell culture of wild-type Arabidopsis thaliana (L.) Heynh. (ecoptype Columbia, Col-0) was studied. Among the identified proteins whose phosphorylation was affected by the NO donor treatment, the enzymes of primary metabolism (glyceraldehyde-3-phosphate dehydrogenase, enolase) and regulatory proteins (14-3-3-like protein GF14ω, protein-disulfide isomerase-like protein, chaperonin-60α) were detected. The results clarify possible mechanisms of NO action on primary metabolism, cell cycle, and stress-induced responses of cultured plant cells.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

APF:

aminophenyl fluorescein

DAF-FM:

4-amino-5-methylamino-2′,7′-difluorescein diacetate

DTT:

dithiothreitol

GAPC2:

glyceraldehyde-3-phosphate dehydrogenase

MALDI-TOF MS:

matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

MAPK:

mitogenactivated protein kinase

NO-РТМ:

NO-dependent posttranslational protein modification

RNS:

reactive nitrogen species

SNP:

sodium nitroprusside

References

  1. Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., and Hancock, J.T., Hydrogen peroxide and nitric oxide as signalling molecules in plants, J. Exp. Bot., 2002, vol. 53, pp. 1237–1247.

    Article  CAS  PubMed  Google Scholar 

  2. Thomas, D.D., Ridnour, L.A., Isenberg, J.S., Flores-Santana, W., Switzer, C.H., Donzelli, S., Hussain, P., Vecoli, C., Paolocci, N., Ambs, S., Colton, C.A., Harris, C.C., Robert, D.D., and Wink, D.A., The chemical biology of nitric oxide: implication in cellular signaling, Free Radic. Biol. Med., 2008, vol. 45, pp. 18–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Begara-Morales, J.C., Sánchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pérez, C., Padilla, M.N., Corpas, F.J., and Barroso, J.B., Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs), Front. Plant Sci., 2016, vol. 7, p.–152. doi 10.3389/fpls.2016.0015

    Article  PubMed  PubMed Central  Google Scholar 

  4. Corpas, F.J., Palma, J.M., and Barroso, J.B., Protein tyrosine nitration in higher plants grown under natural and stress conditions, Front. Plant Sci., 2013, vol. 4. doi 10.3389/fpls.2013.00029

  5. Lozano-Juste, J., Colom-Moreno, R., and Leon, J., In vivo protein tyrosine nitration in Arabidopsis thaliana, J. Exp. Bot., 2011, vol. 62, pp. 3501–3517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Astier, J., Kulik, A., Koen, E., Besson-Bard, A., Bourque, S., Jeandroz, S., Lamotte, O., and Wendehenne, D., Protein S-nitrosylation: what’s going on in plants? Free Radic. Biol. Med., 2012, vol. 53, pp. 1101–1110.

    Article  CAS  PubMed  Google Scholar 

  7. Baudouin, E., The language of nitric oxide signaling, Plant Biol., 2011, vol. 13, pp. 233–242.

    Article  CAS  PubMed  Google Scholar 

  8. Schenk, R.U. and Hildebrandt, A., Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures, Can. J. Bot., 1972, vol. 50, pp. 199–204.

    Article  CAS  Google Scholar 

  9. Mur, L.A.J., Mandon, J., Cristescu, S.M., Harren, F.J.M., and Prats, E., Methods of nitric oxide detection in plants: a commentary, Plant Sci., 2011, vol. 181, pp. 509–519.

    Article  CAS  PubMed  Google Scholar 

  10. Abello, N., Kerstjens, H.A.M., Postma, D.S., and Bischoff, R., Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine- nitrated proteins, J. Proteome Res., 2009, vol. 8, pp. 3222–3238.

    Article  CAS  PubMed  Google Scholar 

  11. Kolbert, Z., Peto, A., Lehotai, N., Feigl, G., Ordog, A., and Erdei, L., In vivo and in vitro studies on fluorophore specificity, Acta Biol. Szeged., 2012, vol. 56, pp. 37–41.

    Google Scholar 

  12. Delledonne, M., Xia, Y., Dixon, R.A., and Lamb, C., Nitric oxide functions as a signal in plant disease resistance, Nature, 1998, vol. 394, pp. 585–588.

    Article  CAS  PubMed  Google Scholar 

  13. Napoli, C., Paolisso, G., Casamassimi, A., Al-Omran, M., Barbieri, M., Sommese, L., Infante, T., and Ignarro, L.J., Effects of nitric oxide on cell proliferation, J. Am. Coll. Cardiol., 2013, vol. 62, pp. 89–95.

    Article  CAS  PubMed  Google Scholar 

  14. Sirover, M.A., Subcellular dynamics of multifunctional protein regulation: mechanisms of GAPDH intracellular translocation, J. Cell. Biochem., 2012, vol. 113, pp. 2193–2200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Romero-Puertas, M.C., Campostrini, N., Mattè, A., Righetti, P.G., Perazzolli, M., Zolla, L., Roepstorff, P., and Delledonne, M., Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response, Proteomics, 2008, vol. 8, pp. 1459–1469.

    Article  CAS  PubMed  Google Scholar 

  16. Naletova, I.N., Muronetz, V.I., and Schmalhausen, E.V., Unfolded, oxidized, and thermoinactivated forms of glyceraldehyde-3-phosphate dehydrogenase interact with the chaperonin GroEL in different ways, Biochim. Biophys. Acta, 2006, vol. 1764, pp. 831–838.

    Article  CAS  PubMed  Google Scholar 

  17. Cheong, K., Choi, J., Choi, J., Park, J., Jang, S., and Lee, Y.H., Eukaryotic DNAJ/K database: a comprehensive phylogenomic analysis platform for the DNAJ/K family, Genom. Inform., 2013, vol. 11, pp. 52–54.

    Article  Google Scholar 

  18. Wang, Z., Hao, Y., and Lowe, A.W., The adenocarcinoma- associated antigen, AGR2 promotes tumor growth, cell migration, and cellular transformation, Cancer Res., 2008, vol. 68, pp. 492–497.

    CAS  PubMed  Google Scholar 

  19. Yu, H., Zhao, J., Lin, L., Zhang, Y., Zhong, F., Liu, Y., Yu, Y., Shen, H., Han, M., He, F., and Yang, P., Proteomic study explores AGR2 as pro-metastatic protein in HCC, Mol. BioSyst., 2012, vol. 8, pp. 2710–2718.

    Article  CAS  PubMed  Google Scholar 

  20. De Boer, A.H., van Kleeff, P.J.M., and Gao, J., Plant 14-3-3 proteins as spiders in a web of phosphorylation, Protoplasma, 2013, vol. 250, pp. 425–440.

    Article  CAS  PubMed  Google Scholar 

  21. Ötvös, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szűcs, A., Bottka, S., Dudits, D., and Fehér, A., Nitric oxide is required for, and promotes auxin-mediated activation of cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures, Plant J., 2005, vol. 43, pp. 849–860.

    Article  PubMed  Google Scholar 

  22. Correa-Aragunde, N., Graziano, M., Chevalier, Ch., and Lamattina, L., Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato, J. Exp. Bot., 2006, vol. 57, pp. 581–588.

    Article  CAS  PubMed  Google Scholar 

  23. Bai, S., Li, M., Yao, T., Wang, H., Zhang, Y., Xiao, L., Wang, J., Zhang, Zh., Hua, Y., Liu, W., and He, Y., Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana, Nitric Oxide, 2012, vol. 26, pp. 54–60.

    Article  CAS  PubMed  Google Scholar 

  24. Yoon, G.M. and Kieber, J.J., 14-3-3 Regulates 1-aminocyclopropane-1-carboxylate synthase protein turnover in Arabidopsis, Plant Cell, 2013, vol. 25, pp. 1016–1028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Oh, Ch.S., Pedley, K.F., and Martin, G.B., Tomato 14- 3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKKα Plant Cell, 2010, vol. 22, pp. 260–272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lalle, M., Visconti, S., Marra, M., Camoni, L., Velasco, R., and Aducci, P., ZmMPK6, a novel maize MAP kinase that interacts with 14-3-3 proteins, Plant Mol. Biol., 2005, vol. 59, pp. 713–722.

    Article  CAS  PubMed  Google Scholar 

  27. Liu, Y. and Zhang, S., Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis, Plant Cell, 2004, vol. 16, pp. 3386–3399.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Fomenkov, A.A., Nosov, A.V., Rakitin, V.Yu., Sukhanova, E.S., Mamaeva, A.S., Sobol’kova, G.I., Nosov, A.M., and Novikova, G.V., Ethylene in the proliferation of cultured plant cells: regulating or just going along? Russ. J. Plant Physiol., 2015, vol. 62, pp. 815–822.

    Article  CAS  Google Scholar 

  29. Narang, H., Dhariwala, F.A., and Krishna, M., Effect of nitric oxide donor and gamma irradiation on modifications of ERK and JNK in murine peritoneal macrophages, J. Cell Commun. Signal., 2007, vol. 1, pp. 219–226.

    Article  PubMed  Google Scholar 

  30. Feng, X., Sun, T., Bei, Y., Ding, S., Zheng, W., Lu, Y., and Shen, P., S-Nitrosylation of ERK inhibits ERK phosphorylation and induces apoptosis, Sci. Rep., 2013, vol. 3, p. 1814. doi 10.1038/srep01814

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow, 127276, Russia

    A. S. Mamaeva, A. A. Fomenkov, A. V. Nosov & G. V. Novikova

Authors
  1. A. S. Mamaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Fomenkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. V. Nosov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. V. Novikova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. V. Novikova.

Additional information

Original Russian Text © A.S. Mamaeva, A.A. Fomenkov, A.V. Nosov, G.V. Novikova, 2017, published in Fiziologiya Rastenii, 2017, Vol. 64, No. 5, pp. 346–354.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mamaeva, A.S., Fomenkov, A.A., Nosov, A.V. et al. Regulation of protein phosphorylation by nitric oxide in cell culture of Arabidopsis thaliana . Russ J Plant Physiol 64, 657–664 (2017). https://doi.org/10.1134/S1021443717050077

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443717050077

Keywords

Search

Navigation