Russian Journal of Plant Physiology

, Volume 62, Issue 4, pp 427–440 | Cite as

Regulatory role of nitric oxide in plants

  • A. S. Mamaeva
  • A. A. Fomenkov
  • A. V. Nosov
  • I. E. Moshkov
  • L. A. J. Mur
  • M. A. Hall
  • G. V. NovikovaEmail author


Research performed over the last few years identified nitric oxide (NO) as an intracellular signaling molecule involved in regulation of plant physiological processes at all stages of the life cycle. Nevertheless, some extremely important aspects of NO biology are still far from being clarified. There exist different points of view on NO formation and utilization in plants. The mechanisms of perception and transduction of the NO signal are not yet fully understood, and the origin of specificity underlying coordinated activation of responses to NO remains unresolved. It is reasonable to expect that the deep knowledge of NO functioning in animals may provide some keys to these questions. Such a comparative analysis is a way to reveal similarities and emphasize the differences in the current understanding of the NO role in plants. The present lecture highlights these aspects of NO functioning.


plants nitric oxide protein modification signal transduction stress phytohormones 



cytochrome c-oxidase


Cu-amine oxidase








electron transport chain




S-nitroso-glutathione reductase


nitrite-NO reductase


NO synthase


nitrate reductase


non-symbiotic hemoglobins


reactive oxygen species


sodium nitroprusside


xanthine oxidoreductase


soluble guanylate cyclase


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  1. 1.
    Palmer, R.M., Ferrige, A.G., and Moncada, S., Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor, Nature, 1987, vol. 327, pp. 524–526.PubMedCrossRefGoogle Scholar
  2. 2.
    Durner, J., Wendehenne, D., and Klessig, D.F., Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADF-ribose, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 10328–10333.PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    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.PubMedCrossRefGoogle Scholar
  4. 4.
    Marsh, N. and Marsh, A., A short history of nitroglycerine and nitric oxide in pharmacology and physiology, Clin. Exp. Pharmacol. Physiol., 2000, vol. 27, pp. 313–319.PubMedCrossRefGoogle Scholar
  5. 5.
    Arnold, W.P., Mittal, C.K., Katsuki, S., and Murad, F., Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations, Proc. Natl. Acad. Sci. USA, 1977, vol. 74, pp. 3203–3207PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Gryglewski, R.J., Palmer, R.M., and Moncada, S., Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor, Nature, 1986, vol. 320, pp. 454–456.PubMedCrossRefGoogle Scholar
  7. 7.
    Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G., Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide, Proc. Natl. Acad. Sci. USA, 1987, vol. 84, pp. 9265–9269.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Palmer, R.M., Ashton, D.S., and Moncada, S., Vascular endothelial cells synthesize nitric oxide from L-arginine, Nature, 1988, vol. 333, pp. 664–666.PubMedCrossRefGoogle Scholar
  9. 9.
    Forstermann, U. and Sessa, W.C., Nitric oxide synthases: regulation and function, Eur. Heart J., 2012, vol. 33, pp. 829–837.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Russwurm, M. and Koesling, D., No activation of guanylyl cyclase, EMBO J., 2004, vol. 23, pp. 4443–4450.PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Friebe, A. and Koesling, D., Regulation of nitric oxidesensitive guanylyl cyclase, Circ. Res., 2003, vol. 93, pp. 96–105.PubMedCrossRefGoogle Scholar
  12. 12.
    Casteel, D.E., Zhang, T., Zhuang, S., and Pilz, R.B., cGMP-dependent protein kinase anchoring by IRAG regulates its nuclear translocation and transcriptional activity, Cell. Signal., 2008, vol. 20, pp. 1392–1399.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Gupta, K.J., Fernie, A.R., Kaiser, W.M., and van Dongen, J.T., On the origins of nitric oxide, Trends Plant Sci., 2011, vol. 16, pp. 160–168.PubMedCrossRefGoogle Scholar
  14. 14.
    Foresi, N., Correa-Aragunde, N., Parisi, G., Calo, G., Salerno, G., and Lamattina, L., Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent, Plant Cell, 2010, vol. 22, pp. 3816–3830.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Guo, F.Q., Okamoto, M., and Crawford, M.J., Identification of a plant nitric oxide synthase gene involved in hormonal signaling, Science, 2003, vol. 302, pp. 100–103.PubMedCrossRefGoogle Scholar
  16. 16.
    Moreau, M., Lindermayr, C., Durner, J., and Klessig, D.F., NO synthesis and signaling in plants — where do we stand? Physiol. Plant., 2010, vol. 138, pp. 372–383.PubMedCrossRefGoogle Scholar
  17. 17.
    Zemojtel, T., Fröhlich, A., Palmieri, M.C., Kolanczyk, M., Mikula, I., Wyrwicz, L.S., Wanker, E.E., Mundlos, S., Vingron, M., Martasek, P., and Durner, J., Plant nitric oxide synthase: a never-ending story? Trends Plant Sci., 2006, vol. 11, pp. 524–525.PubMedCrossRefGoogle Scholar
  18. 18.
    Flores-Pérez, U., Sauret-Güeto, S., Gas, E., Jarvis, P., and Rodríguez-Concepción, M., A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids, Plant Cell, 2008, vol. 20, pp. 1303–1315.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Tun, N.N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Iochevet, E., Floh, S., and Scherer, G.F.E., Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings, Plant Cell Physiol., 2006, vol. 47, pp. 346–354.PubMedCrossRefGoogle Scholar
  20. 20.
    Wimalasekera, R., Villar, C., Begum, T., and Scherer, G.F., COPER AMINE OXIDASE1 (CuAO) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction, Mol. Plant, 2001, vol. 4, pp. 663–678.CrossRefGoogle Scholar
  21. 21.
    Flores, T., Todd, C.D., Tovar-Mendez, A., Dhanoa, P.K., Correa-Aragunde, N., Hoyos, M.E., Brownfield, D.M., Mullen, R.T., Lamattina, L., and Polacco, J.C., Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development, Plant Physiol., 2008, vol. 147, pp. 1936–1946.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Lillo, C., Meyer, C., Lea, U.S., Provan, F., and Oltedal, S., Mechanisms and importance of post-translational regulation of nitrate reductase, J. Exp. Bot., 2004, vol. 55, pp. 1275–1282.PubMedCrossRefGoogle Scholar
  23. 23.
    Desikan, R., Griffiths, R., Hancock, J., and Neill, S., A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 16314–16318.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Dordas, C., Hasinoff, B.B., Rivoal, J., and Hill, R.D., Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures, Planta, 2004, vol. 219, pp. 66–72.PubMedCrossRefGoogle Scholar
  25. 25.
    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.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Cantrel, C., Vazquez, T., Puyaubert, J., Rezé, N., Lesch, M., Kaiser, W.M., Dutilleul, C., Guillas, I., Zachowski, A., and Baudouin, E., Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana, New Phytol., 2011, vol. 189, pp. 415–427.PubMedCrossRefGoogle Scholar
  27. 27.
    Schlicht, M. and Kombrink, E., The role of nitric oxide in the interaction of Arabidopsis thaliana with the biotrophic fungi, Golovinomyces orontii and Erysiphe pisi, Front. Plant Sci., 2013, vol. 4, doi 10.3389/fpls.2013.00351Google Scholar
  28. 28.
    Rockel, P., Strube, F., Rockel, A., Wildt, J., and Kaiser, W.M., Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro, J. Exp. Bot., 2002, vol. 53, pp. 103–110.PubMedCrossRefGoogle Scholar
  29. 29.
    Stöhr, C., Strube, F., Marx, G., Ullrich, W.R., and Rockel, P., A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite, Planta, 2001, vol. 212, pp. 835–841.PubMedCrossRefGoogle Scholar
  30. 30.
    Gupta, K.J. and Kaiser, W.M., Production and scavenging of nitric oxide by barley root mitochondria, Plant Cell Physiol., 2010, vol. 51, pp. 576–584.PubMedCrossRefGoogle Scholar
  31. 31.
    Stoimenova, M., Igamberdiev, A.U., Gupta, K.J., and Hill, R.D., Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria, Planta, 2007, vol. 226, pp. 465–474.PubMedCrossRefGoogle Scholar
  32. 32.
    Cantu-Medellin, N. and Kelley, E.E., Xanthine oxidoreductase-catalyzed reduction of nitrite to nitric oxide: insights regarding where, when and how, Nitric Oxide, 2013, vol. 34, pp. 19–26.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Corpas, F.J., Palma, J.M., Sandalio, L.M., Valderrama, R., Barroso, J.B., and del Rio, L.A., Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves, J. Plant Physiol., 2008, vol. 165, pp. 1319–1330.PubMedCrossRefGoogle Scholar
  34. 34.
    Tischner, R., Galli, M., Heimer, Y.M., Bielefeld, S., Okamoto, M., Mack, A., and Crawford, N.M., Interference with the citrulline-based nitric oxide synthase assay by argininosuccinate lyase activity in Arabidopsis extracts, FASEB J., 2007, vol. 274, pp. 4238–4245.Google Scholar
  35. 35.
    Hill, R.D., Non-symbiotic haemoglobins: what’s happening beyond nitric oxide scavenging? AoB PLANTS, 2012, doi 10.1093/aobpla/pls004Google Scholar
  36. 36.
    Igamberdiev, A.U., Bykova, N.V., and Hill, R.D., Scavenging of nitric oxide by barley hemoglobin is facilitated by a monodehydroascorbate reductase mediated ascorbate reduction of methemoglobin, Planta, 2006, vol. 223, pp. 1033–1040.PubMedCrossRefGoogle Scholar
  37. 37.
    Sarkar, T., Biswas, P., Ghosh, S.K., and Ghosh, S., Nitric oxide production by necrotrophic pathogen Macrophomina phaseolina and the host plant in charcoal rot disease jute: complexity of the interplay between necrotroph-host plant interactions, PLoS ONE, 2014, vol. 9, doi 10.1371/journal.pone.0107348Google Scholar
  38. 38.
    Boccara, M., Mills, C.E., Zeier, J., Anzi, Ch., Lamb, Ch., Poole, R.K., and Delledonne, M., Flavohaemoglobin HmpX from Erwinia chrysanthemi confers nitrosative stress tolerance and affects the plant hypersensitive reaction by intercepting nitric oxide produced by the host, Plant J., 2005, vol. 43, pp. 226–237.PubMedCrossRefGoogle Scholar
  39. 39.
    Garcia-Mata, C. and Lamattina, L., Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress, Plant Physiol., 2001, vol. 126, pp. 1196–1204.PubMedCrossRefGoogle Scholar
  40. 40.
    Sun, Ch., Lu, L., Liu, L., Liu, W., Yu, Y., Liu, X., Hu, Y., Jin, Ch., and Lin, X., Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum), New Phytol., 2014, vol. 201, pp. 1240–1250.PubMedCrossRefGoogle Scholar
  41. 41.
    Correa-Aragunde, N., Graziano, M., and Lamattina, L., Nitric oxide plays a central role in determining lateral root development in tomato, Planta, 2004, vol. 218, pp. 900–905.PubMedCrossRefGoogle Scholar
  42. 42.
    Del Giudice, J., Cam, Y., Damiani, I., Fung-Chat, F., Meilhoc, E., Bruand, C., Brouquisse, R., Puppo, A., and Boscari, A., Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis, New Phytol., 2011, vol. 191, pp. 405–417.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Serrano, I., Romero-Puertas, M.C., Rodriguez-Serrano, M., Sandalio, L.M., and Olmedilla, A., Peroxynitrite mediates programmed cell death both in papillar cells and in self-incompatible pollen in the olive (Olea europaea L.), J. Exp. Bot., 2012, vol. 63, pp. 1479–1493.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Beligni, M.V. and Lamattina, L., Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants, Planta, 2000, vol. 210, pp. 215–221.PubMedCrossRefGoogle Scholar
  45. 45.
    Mur, L.A.J., Mandon, J., Persijn, S., Cristescu, S.M., Moshkov, I.E., Novikova, G.V., Hall, M.A., Harren, F.J.M., Hebelstrup, K., and Gupta, K.J., Nitric oxide in plants: an assessment of the current state of knowledge, AoB PLANTS, 2013, vol. 5, doi 10.1093/aobpla/pls052Google Scholar
  46. 46.
    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.PubMedCrossRefGoogle Scholar
  47. 47.
    Vitecek, J., Reinohl, V., and Jones, R.L., Measuring NO production by plant tissues and suspension cultured cells, Mol. Plant, 2008, vol. 1, pp. 270–284.PubMedCrossRefGoogle Scholar
  48. 48.
    Cristescu, S.M., Persijn, S.T., te Lintel, Hekkert, S., and Harren, F.J.M., Laser-based system for trace gas detection in life sciences, Appl. Phys. B, 2008, vol. 92, pp. 343–349.CrossRefGoogle Scholar
  49. 49.
    Sikora, A., Zielonka, J., Lopez, M., Joseph, J., and Kalyanaraman, B., Direct oxidation of boronates by peroxynitrite: mechanism and implications in fluorescence imaging of peroxynitrite, Free Radic. Biol. Med., 2009, vol. 47, pp. 1401–1407.PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H.J., and Nagano, T., Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species, J. Biol. Chem., 2003, vol. 278, pp. 3170–3175.PubMedCrossRefGoogle Scholar
  51. 51.
    D’Alessandro, S., Posocco, B., Costa, A., Zahariou, G., Schiavo, F., Carbonera, D., and Zottini, M., Limits in the use of cPTIO as nitric oxide scavenger and EPR probe in plant cells and seedlings, Front. Plant Sci., 2013, vol. 4, doi 10.3389/fpls.2013.00340Google Scholar
  52. 52.
    Miller, M.R. and Megson, I.L., Recent developments in nitric oxide donor drugs, Brit. J. Pharmacol., 2007, vol. 151, pp. 305–321.CrossRefGoogle Scholar
  53. 53.
    Floryszak-Wieczorek, J., Milczarek, G., Arasimowicz, M., and Ciszewski, A., Do nitric oxide donors mimic endogenous NO-related response in plants? Planta, 2006, vol. 224, pp. 1363–1372.PubMedCrossRefGoogle Scholar
  54. 54.
    Merchante, C., Alonso, J.M., and Stepanova, A.N., Ethylene signaling: simple ligand, complex regulation, Curr. Opin. Plant Biol., 2013, vol. 16, pp. 554–560.PubMedCrossRefGoogle Scholar
  55. 55.
    Ludidi, N. and Gehring, C., Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana, J. Biol. Chem., 2003, vol. 278, pp. 6490–6494.PubMedCrossRefGoogle Scholar
  56. 56.
    Astier, J. and Lindermayr, C., Nitric oxide-dependent posttranslational modification in plants: an update, Int. J. Mol. Sci., 2012, vol. 13, pp. 15193–15208.PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    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.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Marozkina, N.V. and Gaston, B., S-Nitrosylation signaling regulates cellular protein interactions, Biochim. Biophys. Acta, 2012, vol. 1820, pp. 722–729.PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    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.PubMedCrossRefGoogle Scholar
  60. 60.
    Corpas, F.J., Palma, J.M., del Rio, L.A., 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.2013.00029Google Scholar
  61. 61.
    Ischiropoulus, H., Protein tyrosine nitration — an update, Arch. Biochem. Biophys., 2009, vol. 484, pp. 117–121.CrossRefGoogle Scholar
  62. 62.
    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.PubMedCrossRefGoogle Scholar
  63. 63.
    Kato, H., Takemoto, D., and Kawakita, K., Proteomic analysis of S-nitrosylated proteins in potato plant, Physiol. Plant., 2013, vol. 148, pp. 371–386.PubMedCrossRefGoogle Scholar
  64. 64.
    Begara-Morales, J.C., Chaki, M., Sanchez-Calvo, B., Mata-Pérez, C., Leterrier, M., Palma, J.M., Barroso, J.B., and Corpas, F.J., Protein tyrosine nitration in pea roots during development and senescence, J. Exp. Bot., 2013, vol. 64, pp. 1121–1134.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Baudouin, E., The language of nitric oxide signaling, Plant Biol., 2011, vol. 13, pp. 233–242.PubMedCrossRefGoogle Scholar
  66. 66.
    Spadaro, D., Yun, B.W., Spoel, S.H., Chu, C., Wang, Y.Q., and Loake, G.J., The redox switch: dynamic regulation of protein function by cysteine modifications, Physiol. Plant., 2010, vol. 138, pp. 360–371.PubMedCrossRefGoogle Scholar
  67. 67.
    Beligni, M.V., Fath, A., Bethke, P.C., Lamattina, L., and Jones, R.L., Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers, Plant Physiol., 2002, vol. 129, pp. 1642–1650.PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Wang, Y., Loake, G.J., and Chu, C., Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death, Front. Plant Sci., 2013, vol. 4, doi 10.3389/fpls.2013.00314Google Scholar
  69. 69.
    Yang, F., Ding, F., Duan, X., Zhang, J., Li, X., and Yang, Y., ROS generation and proline metabolism in calli of halophyte Nitraria tangutorum Bobr. to sodium nitroprusside treatment, Protoplasma, 2014, vol. 251, pp. 71–80.PubMedCrossRefGoogle Scholar
  70. 70.
    Lin, C.C., Jih, P.J., Lin, H.H., Lin, J.S., Chang, L.L., Shen, Y.H., and Jeng, S.T., Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding, Plant Mol. Biol., 2011, vol. 77, pp. 235–249.PubMedCrossRefGoogle Scholar
  71. 71.
    Grob, F., Durner, J., and Gaupels, F., Nitric oxide, antioxidants and prooxidants in plant defence responses, Front. Plant Sci., 2013, doi 10.3389/fpls.2013.00419Google Scholar
  72. 72.
    Molassiotis, A. and Fotopoulos, V., Oxidative and nitrosative signaling in plants. Two branches in the same tree? Plant Signal. Behav., 2011, vol. 6, pp. 210–214.PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Chaki, M., Valderrama, R., Fernandez-Ocana, A.M., Carreras, A., Lopez-Jaramillo, J., Luque, F., Palma, J.M., Pedrajas, J.R., Begara-Morales, J.C., Sanchez-Calvo, B., Gomez-Rodriguez, M.V., Corpas, F.J., and Barroso, J.B., Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls, J. Exp. Bot., 2009, vol. 60, pp. 4221–4234.PubMedCrossRefGoogle Scholar
  74. 74.
    Fares, A., Rossignol, M., and Peltier, J.B., Proteomics investigation of endogenous S-nitrosylation in Arabidopsis, Biochem. Biophys. Res. Commun., 2011, vol. 416, pp. 331–336.PubMedCrossRefGoogle Scholar
  75. 75.
    Begara-Morales, J.C., Sanchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pérez, C., Lopez-Jaramillo, J., Padilla, M.N., Carreras, A., Corpas, F.J., and Barroso, J.B., Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation, J. Exp. Bot., 2014, vol. 65, pp. 527–538.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Freschi, L., Nitric oxide and phytohormone interactions: current status and perspectives, Front. Plant Sci., 2013, vol. 4, doi 10.3389/fpls.2013.00398Google Scholar
  77. 77.
    Shen, Q., Wang, Y., Tian, H., and Guo, F., Nitric oxide mediates cytokinin functions in cell proliferation and meristem maintenance in Arabidopsis, Mol. Plant, 2013, vol. 6, pp. 1214–1225.PubMedCrossRefGoogle Scholar
  78. 78.
    Liu, W.Z., Kong, D.D., Gu, X.X., Gao, H.B., Wang, J.Z., Xia, M., Gao, Q., Tian, L.L., Xu, Z.H., Bao, F., Hu, Y., Ye, N.S., Pei, Z.M., and He, Y.K., Cytokinins can act as suppressors of nitric oxide in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2013, vol. 110, pp. 41548–41553.Google Scholar
  79. 79.
    Feng, J., Wang, C., Chen, Q., Chen, H., Ren, B., Li, X., and Zuo, J., S-Nitrosylation of phosphotransfer proteins represses cytokinin signaling, Nat. Commun., 2013, vol. 4, doi 10.1038/ncomms2541Google Scholar
  80. 80.
    Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., and Neill, S.J., ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis, Plant J., 2006, vol. 45, pp. 113–122.PubMedCrossRefGoogle Scholar
  81. 81.
    Liu, Y., Shi, L., Ye, N., Liu, R., Jia, W., and Zhang, J., Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis, New Phytol., 2009, vol. 183, pp. 1030–1042.PubMedCrossRefGoogle Scholar
  82. 82.
    Pagnussat, G.C., Simontacchi, M., Puntarulo, S., and Lamattina, L., Nitric oxide is required for root organogenesis, Plant Physiol., 2002, vol. 129, pp. 954–956.PubMedCentralPubMedCrossRefGoogle Scholar
  83. 83.
    Ötvös, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szücs, 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.PubMedCrossRefGoogle Scholar
  84. 84.
    Fernandez-Marcos, M., Sanza, L., Lewis, D.R., Muday, G.K., and Lorenzo, O., Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport, Proc. Natl. Acad. Sci. USA, 2011, vol. 108, pp. 18506–18511.PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Terrile, M.C., París, R., Calderón-Villalobos, L.I.A., Iglesias, M.J., Lamattina, L., Estelle, M., and Casalongué, C.A., Nitric oxide influences auxin signaling trough S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE1 auxin receptor, Plant J., 2012, vol. 70, pp. 492–500.PubMedCentralPubMedCrossRefGoogle Scholar
  86. 86.
    Lozano-Juste, J. and Leon, J., Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis, Plant Physiol., 2011, vol. 156, pp. 1410–1423.PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Flores, F.B., Sanchez-Bel, P., Valdenegro, M., Romojaro, F., Martinez-Madrid, M.C., and Egea, M.I., Effects of a pretreatment with nitric oxide on peach (Prunus persica L.) storage at room temperature, Eur. Food Res. Technol., 2008, vol. 227, pp. 1599–1611.CrossRefGoogle Scholar
  88. 88.
    Lindermayr, C., Saalbach, G., Bahnweg, G., and Durner, J., Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation, J. Biol. Chem., 2006, vol. 281, pp. 4285–4291.PubMedCrossRefGoogle Scholar
  89. 89.
    Gibbs, D.J., Md Isa, N., Movahedi, M., Lozano-Juste, J., Mendiondo, G.M., Berckhan, S., Marin-de la Rosa, N., Conde, J.V., Correia, C.S., Pearce, S.P., Bassel, G.W., Hamali, B., Talloji P., Tomé, D.F.A., Coego, A., Beynon, J., Alabadí, D., Bachmair, A., Leon, J., Gray, J.E., Theodoulou, F.L., and Holdsworth, M.J., Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors, Mol. Cell, 2014, vol. 53, pp. 369–379.PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Varshavsky, A., The N-end rule pathway and regulation by proteolysis, Protein Sci., 2011, vol. 20, pp. 1298–1345.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • A. S. Mamaeva
    • 1
  • A. A. Fomenkov
    • 1
  • A. V. Nosov
    • 1
  • I. E. Moshkov
    • 1
  • L. A. J. Mur
    • 2
  • M. A. Hall
    • 2
  • G. V. Novikova
    • 1
    Email author
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Institute of Biological, Environmental, and Rural SciencesAberystwyth UniversityAberystwythUK

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