Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Molecular mechanisms accompanying nitric oxide signalling through tyrosine nitration and S-nitrosylation of proteins in plants

Prachi Jain A and Satish C. Bhatla A B
+ Author Affiliations
- Author Affiliations

A Laboratory of Plant Physiology and Biochemistry, Department of Botany, University of Delhi, Delhi, India.

B Corresponding author. Email: bhatlasc@gmail.com

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology - https://doi.org/10.1071/FP16279
Submitted: 3 August 2016  Accepted: 1 February 2017   Published online: 22 March 2017

Abstract

Nitric oxide (NO) signalling in plants is responsible for modulation of a variety of plant developmental processes. Depending on the tissue system, the signalling of NO-modulated biochemical responses majorly involves the processes of tyrosine nitration or S-nitrosylation of specific proteins/enzymes. It has further been observed that there is a significant impact of various biotic/abiotic stress conditions on the extent of tyrosine nitration and S-nitrosylation of various metabolic enzymes, which may act as a positive or negative modulator of the specific routes associated with adaptive mechanisms employed by plants under the said stress conditions. In addition to recent findings on the modulation of enzymes of primary metabolism by NO through these two biochemical mechanisms, a major mechanism for regulating the levels of reactive oxygen species (ROS) under stress conditions has also been found to be through tyrosine nitration or S-nitrosylation of ROS-scavenging enzymes. Recent investigations have further highlighted the differential manner in which the ROS-scavenging enzymes may be S-nitrosylated and tyrosine nitrated, with reference to their tissue distribution. Keeping in mind the very recent findings on these aspects, the present review has been prepared to provide an analytical view on the significance of protein tyrosine nitration and S-nitrosylation in plant development.

Additional keywords: abiotic stress, nitric oxide, post-translational modifications, protein tyrosine nitration, reactive oxygen species, S-nitrosylation.


References

Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9, 4368–4380.
Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity.CrossRef | 1:CAS:528:DC%2BD1MXhtFarsbbJ&md5=71b0a80729928087652a4674ac070423CAS |

Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata-ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS Journal 275, 2862–2872.
S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata-ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition.CrossRef | 1:CAS:528:DC%2BD1cXnt1Cjsbs%3D&md5=f5311ee3600ac2c58d3e6872856b5e06CAS |

Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Del Rio LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant, Cell & Environment 35, 281–295.
Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress.CrossRef | 1:CAS:528:DC%2BC38XjtVKnsLk%3D&md5=33489a664d396f88aa3ef26fbe8be462CAS |

Alvarez C, Lozano-Juste J, Romero LC, García I, Gotor C, León J (2011) Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration. Journal of Biological Chemistry 286, 578–586.
Inhibition of Arabidopsis O-acetylserine(thiol)lyase A1 by tyrosine nitration.CrossRef | 1:CAS:528:DC%2BC3MXmvVei&md5=26422836bd0a7959c7e617d156bebc27CAS |

Anand P, Stamler JS (2012) Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. Journal of Molecular Medicine 90, 233–244.
Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease.CrossRef | 1:CAS:528:DC%2BC38Xjs1SrsL0%3D&md5=fe9544971ca541b1df19e2f0acb8d1e8CAS |

Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Science 177, 682–690.
Involvement of nitric oxide in water stress-induced responses of cucumber roots.CrossRef | 1:CAS:528:DC%2BD1MXht1OrurjE&md5=af56e08657d5a4bab9087645ac5ff227CAS |

Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. International Journal of Molecular Sciences 13, 15193–15208.
Nitric oxide-dependent posttranslational modification in plants: an update.CrossRef | 1:CAS:528:DC%2BC38XhvVequrrO&md5=8579ccf3004e44066309462a01f8864eCAS |

Astier J, Kulik A, Koen E, Besson-Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D (2012a) Protein S-nitrosylation: what’s going on in plants? Free Radical Biology & Medicine 53, 1101–1110.
Protein S-nitrosylation: what’s going on in plants?CrossRef | 1:CAS:528:DC%2BC38Xht12ltrfL&md5=0b9fafb9f2c698f6957fc41e94147c0fCAS |

Astier J, Besson-Bard A, Lamotte O, Bertoldo J, Bourque S, Terenzi H, Wendehenne D (2012b) Nitric oxide inhibits the ATPase activity of the chaperone-like AAA+ ATPase CDC48, a target for S-nitrosylation in cryptogein signalling in tobacco cells. The Biochemical Journal 447, 249–260.
Nitric oxide inhibits the ATPase activity of the chaperone-like AAA+ ATPase CDC48, a target for S-nitrosylation in cryptogein signalling in tobacco cells.CrossRef | 1:CAS:528:DC%2BC38XhsVWmsbrK&md5=b8d61cebae9d73cd5fbd78f69b70a074CAS |

Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6, e20714
Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation.CrossRef | 1:CAS:528:DC%2BC3MXntl2ht74%3D&md5=2c6468e5605b5bb0bbde4736943a6298CAS |

Bartesaghi S, Ferrer-Sueta G, Peluffo G, Valez V, Zhang H, Kalyanaraman B, Radi R (2007) Protein tyrosine nitration in hydrophilic and hydrophobic environments. Amino Acids 32, 501–515.
Protein tyrosine nitration in hydrophilic and hydrophobic environments.CrossRef | 1:CAS:528:DC%2BD2sXlsVGnsL0%3D&md5=18028929e92ae5dd022235571d61843cCAS |

Begara-Morales JC, Chaki M, Sanchez-Calvo B, Mata-Perez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. Journal of Experimental Botany 64, 1121–1134.
Protein tyrosine nitration in pea roots during development and senescence.CrossRef | 1:CAS:528:DC%2BC3sXjtlGrsLY%3D&md5=c6fd18c795bbc609614ffd0ac53f0ae1CAS |

Begara-Morales JC, Sanchez-Calvo B, Chaki M, Valderrama R, Mata-Perez C, Lopez-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. Journal of Experimental Botany 65, 527–538.
Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation.CrossRef | 1:CAS:528:DC%2BC2cXhs1ChsL8%3D&md5=d1f62557fd88d8747b3a3efa21370c4aCAS |

Begara-Morales JC, Sanchez-Calvo B, Chaki M, Mata-Perez C, Valderrama R, Padilla MN, Lopez-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. Journal of Experimental Botany 66, 5983–5996.
Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation.CrossRef | 1:CAS:528:DC%2BC2MXitVGju7rM&md5=6275328ee1d2bdb764c76b8203449143CAS |

Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inze D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. Journal of Biological Chemistry 282, 1352–1358.
Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue.CrossRef | 1:CAS:528:DC%2BD2sXit1KrtA%3D%3D&md5=574395847bf2ade2965d06235183baf1CAS |

Benhar M (2015) Nitric oxide and the thioredoxin system: a complex interplay in redox regulation. Biochimica et Biophysica Acta 1850, 2476–2484.
Nitric oxide and the thioredoxin system: a complex interplay in redox regulation.CrossRef | 1:CAS:528:DC%2BC2MXhsFeit7rI&md5=0d4f81b469b43117d73f84b0fa6d5730CAS |

Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nature Reviews. Molecular Cell Biology 10, 721–732.

Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. Journal of Proteomics 79, 87–99.
Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins.CrossRef | 1:CAS:528:DC%2BC3sXivFygu70%3D&md5=d51d858ffd7f87fe824083945b72170fCAS |

Castillo MC, Lozano-Juste J, Gonzalez-Guzman M, Rodriguez L, Rodriguez PL, Leon J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Science Signaling 8, ra89–ra89
Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants.CrossRef |

Cecconi D, Orzetti S, Vandelle E, Rinalducci S, Zolla L, Delledonne M (2009) Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis 30, 2460–2468.
Protein nitration during defense response in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD1MXptlGrt7Y%3D&md5=bb5f94c33b950ad74f384b74a0bf7571CAS |

Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gomez-Rodriguez MV, Begara-Morlaes JC, Corpas FJ, Barroso JB (2008) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant & Cell Physiology 50, 265–279.
Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction.CrossRef |

Chaki M, Valderrama R, Fernandez-Ocana AM, Carreras A, López-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Gómez-Rodríguez MV (2009) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. Journal of Experimental Botany 60, 4221–4234.
Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls.CrossRef | 1:CAS:528:DC%2BD1MXhtlGitL7P&md5=2c4819d6dd375a6af8a8a072321a774aCAS |

Chaki M, Valderrama R, Fernandez-Ocana AM, Carreras A, Gomez-Rodriguez MV, Lopez-Jaramillo J, Begara-Morales JC, Sanchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011a) 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 & Environment 34, 1803–1818.
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.CrossRef | 1:CAS:528:DC%2BC3MXhsVyls77M&md5=b29f462fd7e4211ef0491004d6296833CAS |

Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ (2011b) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. Journal of Experimental Botany 62, 1803–1813.
Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings.CrossRef | 1:CAS:528:DC%2BC3MXjsFyjtbk%3D&md5=91f4a0ef64d63824a965de069a3826e7CAS |

Chaki M, Carreras A, Lopez-Jaramillo J, Begara-Morales JC, Sanchez-Calvo B, Valderrama R, Corpas FJ, Barroso JB (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress. Nitric Oxide 29, 30–33.
Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (β-CA) activity under high temperature stress.CrossRef | 1:CAS:528:DC%2BC3sXitlakt7g%3D&md5=4ac8e34dfcfff2ca6aec237caca5f112CAS |

Chaki M, de Morales PA, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Annals of Botany 116, 637–647.
Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration.CrossRef |

Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytologist 199, 633–635.
Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants.CrossRef | 1:CAS:528:DC%2BC3sXhtFSrurfJ&md5=37aa6483db022d36edaf3b05a46c3486CAS |

Corpas FJ, Chaki M, Fernandez-Ocana A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Rio LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant & Cell Physiology 49, 1711–1722.
Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions.CrossRef | 1:CAS:528:DC%2BD1cXhsFSnsb%2FI&md5=30e6673360d97a7a3cf08376b3c300b3CAS |

Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiology 151, 2083–2094.
Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants.CrossRef | 1:CAS:528:DC%2BD1MXhsFOgtrjP&md5=c330595b93ef2d218d48688122d9c06cCAS |

Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Science 181, 604–611.
Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress.CrossRef | 1:CAS:528:DC%2BC3MXhtFaru7bJ&md5=63a8df8119ddd8e24e98da45b1d0202fCAS |

Corpas FJ, Palma JM, del Río LA, Barroso JB (2013a) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Frontiers in Plant Science 4, 29
Protein tyrosine nitration in higher plants grown under natural and stress conditions.CrossRef |

Corpas FJ, Leterrier M, Begara-Morales JC, Valderrama R, Chaki M, Lopez-Jaramillo J, Luque F, Palma JM, Padilla MN, Sanchez-Calvo B, Mata-Perez C (2013b) Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochimica et Biophysica Acta 1830, 4981–4989.
Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration.CrossRef | 1:CAS:528:DC%2BC3sXhsV2murrJ&md5=bb6521de7e0a60bedc453372d40d7130CAS |

Correa-Aragunde N, Foresi N, Lamattina L (2015) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. Journal of Experimental Botany 66, 2913–2921.
Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study.CrossRef | 1:CAS:528:DC%2BC2MXitVeltbvM&md5=e74516e1bf94ec853c2d67502ea17acbCAS |

David A, Yadav S, Baluška F, Bhatla SC (2015) Nitric oxide accumulation and protein tyrosine nitration as a rapid and long distance signalling response to salt stress in sunflower seedlings. Nitric Oxide 50, 28–37.
Nitric oxide accumulation and protein tyrosine nitration as a rapid and long distance signalling response to salt stress in sunflower seedlings.CrossRef | 1:CAS:528:DC%2BC2MXhsVCju77K&md5=264023aa2d9c2cfb34681f6106b483a9CAS |

De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanita di Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiology 150, 217–228.
Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures.CrossRef | 1:CAS:528:DC%2BD1MXlvFahs78%3D&md5=dc8708e82583a41c450421ed7e0257afCAS |

de Pinto MC, Locato V, Sgobba A, Romero-Puertas Mdel C, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco bright yellow-2 cells. Plant Physiology 163, 1766–1775.
S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco bright yellow-2 cells.CrossRef |

Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochemical and Biophysical Research Communications 416, 331–336.
Proteomics investigation of endogenous S-nitrosylation in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC3MXhs1Cqt7%2FP&md5=0d6eb64aced7c37b00328b06e50ab3c4CAS |

Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proceedings of the National Academy of Sciences of the United States of America 102, 8054–8059.
A central role for S-nitrosothiols in plant disease resistance.CrossRef | 1:CAS:528:DC%2BD2MXkvF2is7w%3D&md5=fea606e0f5bc7b47a18f4ff3a65cbc41CAS |

Feigl G, Kolbert Z, Lehotai N, Molnár Á, Ördög A, Bordé Á, Laskay G, Erdei L (2016) Different zinc sensitivity of Brassica organs is accompanied by distinct responses in protein nitration level and pattern. Ecotoxicology and Environmental Safety 125, 141–152.
Different zinc sensitivity of Brassica organs is accompanied by distinct responses in protein nitration level and pattern.CrossRef | 1:CAS:528:DC%2BC2MXitVSktrnP&md5=58c9bf9e7f9c6acfb836ccff578154e2CAS |

Feng J, Wang C, Chen Q, Chen H, Ren B, Li X, Zuo J (2013) S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nature Communications 4, 1529–1537.
S-nitrosylation of phosphotransfer proteins represses cytokinin signaling.CrossRef |

Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64, 839–863.
Systemic acquired resistance: turning local infection into global defense.CrossRef | 1:CAS:528:DC%2BC3sXosFSku7s%3D&md5=f35d750d5ce34701442028b741fa1f2bCAS |

Galetskiy D, Lohscheider JN, Kononikhin AS, Popov IA, Nikolaev EN, Adamska I (2011) Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. Plant Molecular Biology 77, 461–473.
Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress.CrossRef | 1:CAS:528:DC%2BC3MXhtlWrtLbN&md5=1bbb9752444218369dd15951f7e22ebbCAS |

García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 126, 1196–1204.
Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress.CrossRef |

Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H (2004) Biological significance of nitric oxide-mediated protein modifications. American Journal of Physiology. Lung Cellular and Molecular Physiology 287, L262–L268.
Biological significance of nitric oxide-mediated protein modifications.CrossRef | 1:CAS:528:DC%2BD2cXmvVKnu7k%3D&md5=ca6c47dc99bda4e0faed2754b452a1cbCAS |

Guerra D, Ballard K, Truebridge I, Vierling E (2016) S-Nitrosation of conserved cysteines modulates activity and stability of S-nitrosoglutathione reductase (GSNOR). Biochemistry 55, 2452–2464.
S-Nitrosation of conserved cysteines modulates activity and stability of S-nitrosoglutathione reductase (GSNOR).CrossRef | 1:CAS:528:DC%2BC28XlslSrtr4%3D&md5=ec59e4973a2623e1ef421145cd98db5dCAS |

Holtgrefe S, Gohlke J, Starmann J, Druce S, Klocke S, Altmann B, Wojtera J, Lindermayr C, Scheibe R (2008) Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiologia Plantarum 133, 211–228.
Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications.CrossRef | 1:CAS:528:DC%2BD1cXntFahtb4%3D&md5=9db3d138ad197ddac578064f803d914aCAS |

Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2014) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. Journal of Experimental Botany 66, 989–999.
Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration.CrossRef |

Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218, 938–946.
Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD2cXjt1ait7c%3D&md5=7996c1d2f98912d299f411034e694f2eCAS |

Jia L, Bonaventura C, Bonaventura J, Stamler JS (1996) S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380, 221–226.
S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control.CrossRef | 1:CAS:528:DyaK28XhvVahs78%3D&md5=3603b6722d3e4911e58a949a5434a5cdCAS |

Jovanović AM, Durst S, Nick P (2010) Plant cell division is specifically affected by nitrotyrosine. Journal of Experimental Botany 61, 901–909.
Plant cell division is specifically affected by nitrotyrosine.CrossRef |

Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiologia Plantarum 148, 371–386.
Proteomic analysis of S-nitrosylated proteins in potato plant.CrossRef | 1:CAS:528:DC%2BC3sXhtFejsbjN&md5=cbba95f34df5f5ad4ad6aadfa3490f6fCAS |

Kubienová L, Kopečný D, Tylichová M, Briozzo P, Skopalová J, Šebela M, Navrátil M, Tâche R, Luhová L, Barroso JB, Petřivalský M (2013) Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95, 889–902.
Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum.CrossRef |

Lamotte O, Bertoldo JB, Besson-Bard A, Rosnoblet C, Aimé S, Hichami S, Terenzi H, Wendehenne D (2014) Protein S-nitrosylation: specificity and identification strategies in plants. Frontiers in Chemistry 2, 114–123

Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012a) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environmental Pollution 166, 136–143.
Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC38Xms12gtb0%3D&md5=3f56f1141876ec2eae90c9afe3f63f93CAS |

Leterrier M, Barroso JB, Valderrama R, Palma JM, Corpas FJ (2012b) NADP-dependent isocitrate dehydrogenase from Arabidopsis roots contributes in the mechanism of defence against the nitro-oxidative stress induced by salinity. Scientific World Journal 2012, 694740
NADP-dependent isocitrate dehydrogenase from Arabidopsis roots contributes in the mechanism of defence against the nitro-oxidative stress induced by salinity.CrossRef |

Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiology 158, 451–464.
Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice.CrossRef | 1:CAS:528:DC%2BC38XltFSnt7w%3D&md5=83e3426ce9c118734917f2af8c68e280CAS |

Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. Journal of Biological Chemistry 281, 4285–4291.
Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation.CrossRef | 1:CAS:528:DC%2BD28XhtlKkur0%3D&md5=8c455fbba1defa5978864b9dac61431fCAS |

Lindermayr C, Sell S, Muller B, Leister D, Durner J (2010) Redox regulation of the NPR1–TGA1 system of Arabidopsis thaliana by nitric oxide. The Plant Cell 22, 2894–2907.
Redox regulation of the NPR1–TGA1 system of Arabidopsis thaliana by nitric oxide.CrossRef | 1:CAS:528:DC%2BC3cXhtlegsbvO&md5=4871074856473af5dec320880d5922c1CAS |

Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Aheam G, McMahon TJ, Dickfeld T, Marshall HE, Que LG, Stamler JS (2004) Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617–628.
Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock.CrossRef | 1:CAS:528:DC%2BD2cXhvVKqsr4%3D&md5=74f47c5130440f30b7a3d6c485494170CAS |

Lozano-Juste J, Colom-Moreno R, Leon J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. Journal of Experimental Botany 62, 3501–3517.
In vivo protein tyrosine nitration in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC3MXoslOmtrY%3D&md5=71e19b539a1f8db56b40a0874f763a1cCAS |

Melo PM, Silva LS, Ribeiro I, Seabra AR, Carvalho HG (2011) Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiology 157, 1505–1517.
Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration.CrossRef | 1:CAS:528:DC%2BC3MXhsFehur3E&md5=31aa6feddd5576888a3dead233129e0cCAS |

Ortega-Galisteo AP, Rodriguez-Serrano M, Pazmin DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-nitrosylated proteins in pea (Pisum sativum L) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany 63, 2089–2103.
S-nitrosylated proteins in pea (Pisum sativum L) leaf peroxisomes: changes under abiotic stress.CrossRef | 1:CAS:528:DC%2BC38Xjslehsbo%3D&md5=c5b9f9936220c1b222071ecb333d75d6CAS |

Paige JS, Xu G, Stancevic B, Jaffrey SR (2008) Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chemistry & Biology 15, 1307–1316.
Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability.CrossRef | 1:CAS:528:DC%2BD1cXhsFajt7vI&md5=74727b6125a5cf939d28868e2c49505bCAS |

Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J (2010) Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiology 152, 1514–1528.
Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation.CrossRef | 1:CAS:528:DC%2BC3cXmsF2ltr4%3D&md5=066de67bff00ccded44664b59cf54d41CAS |

Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. The Plant Cell 16, 2785–2794.
Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity.CrossRef | 1:CAS:528:DC%2BD2cXptVShs74%3D&md5=e4b09aecbda24d330cdb71384d55275eCAS |

Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proceedings of the National Academy of Sciences of the United States of America 101, 4003–4008.
Nitric oxide, oxidants, and protein tyrosine nitration.CrossRef | 1:CAS:528:DC%2BD2cXivFarsL8%3D&md5=168f9c0c099a4ee3652b83f790fb1e52CAS |

Radi R (2013) Peroxynitrite, a stealthy biological oxidant. Journal of Biological Chemistry 288, 26464–26472.
Peroxynitrite, a stealthy biological oxidant.CrossRef | 1:CAS:528:DC%2BC3sXhsVClt7vL&md5=d8de101708ae2a916c5c97fb1d37fa10CAS |

Romero-Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. The Plant Cell 19, 4120–4130.
S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration.CrossRef | 1:CAS:528:DC%2BD1cXhvF2htLs%3D&md5=cc7fba2601162a1265f0d8d5263bfbe8CAS |

Romero-Puertas MC, Campostrini N, Matte A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8, 1459–1469.
Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response.CrossRef | 1:CAS:528:DC%2BD1cXltVOmsLc%3D&md5=1713ef7996a51cff0135a6e6d17d55ceCAS |

Romero-Puertas MC, Rodriguez-Serrano M, Sandalio LM (2013) Protein S-nitrosylation in plants under abiotic stress: an overview. Frontiers in Plant Science 4, 373
Protein S-nitrosylation in plants under abiotic stress: an overview.CrossRef |

Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annual Review of Plant Biology 59, 143–166.
The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation.CrossRef | 1:CAS:528:DC%2BD1cXntFaqsL0%3D&md5=83c2791f741e9a9d2741803039330921CAS |

Sainz M, Calvo-Begueria L, Perez-Rontome C, Wienkoop S, Abian J, Staudinger C, Bartesaghi S, Radi R, Becana M (2015) Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. The Plant Journal 81, 723–735.
Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism.CrossRef | 1:CAS:528:DC%2BC2MXjtFaks7w%3D&md5=8aa0cbe19c454011bd4e9f2b5a364da1CAS |

Saito S, Yamamoto-Katou A, Yoshioka H, Doke N, Kawakita K (2006) Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant & Cell Physiology 47, 689–697.
Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells.CrossRef | 1:CAS:528:DC%2BD28XmvVOmtb8%3D&md5=e19878635422ec4df793c35b6bddf3d8CAS |

Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. Journal of Integrative Plant Biology 50, 231–243.
Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants.CrossRef | 1:CAS:528:DC%2BD1cXisVegsr8%3D&md5=12c4970fe0b639abcbf2b6e7e0089108CAS |

Signorelli S, Corpas FJ, Borsani O, Barroso JB, Monza J (2013) Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Science 201–202, 137–146.
Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus.CrossRef |

Smith BC, Marletta MA (2012) Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling. Current Opinion in Chemical Biology 16, 498–506.
Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling.CrossRef | 1:CAS:528:DC%2BC38Xhs1ajsb%2FI&md5=bc9a88f1bacae47ba96198d2dfd057f2CAS |

Szuba A, Kasprowicz-Maluśki A, Wojtaszek P (2015) Nitration of plant apoplastic proteins from cell suspension cultures. Journal of Proteomics 120, 158–168.
Nitration of plant apoplastic proteins from cell suspension cultures.CrossRef | 1:CAS:528:DC%2BC2MXlsVWitrs%3D&md5=6d8dbc33c30e67551f327e358c12988eCAS |

Takahashi M, Shigeto J, Sakamoto A, Izumi S, Asada K, Morikawa H (2015) Dual selective nitration in Arabidopsis: almost exclusive nitration of PsbO and PsbP, and highly susceptible nitration of four non-PSII proteins, including peroxiredoxin II E. Electrophoresis 36, 2569–2578.
Dual selective nitration in Arabidopsis: almost exclusive nitration of PsbO and PsbP, and highly susceptible nitration of four non-PSII proteins, including peroxiredoxin II E.CrossRef | 1:CAS:528:DC%2BC2MXhtlyltL7F&md5=c8b3a9526b2e479f4938778b19e73ebcCAS |

Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal 60, 795–804.
Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity.CrossRef | 1:CAS:528:DC%2BD1MXhs1WhtrzF&md5=b5460d03011786d6279226438a2c9d5cCAS |

Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. The Plant Journal 72, 585–599.
Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress.CrossRef | 1:CAS:528:DC%2BC38Xhs1Sht7nF&md5=335a369f840a5400ba94b2c8ddd1bacfCAS |

Tavares CP, Vernal J, Delena RA, Lamattina L, Cassia R, Terenzi H (2014) S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana. Biochimica et Biophysica Acta 1844, 810–817.
S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC2cXkslKjtr0%3D&md5=1f35265e3d70265d165addb8663fc3a2CAS |

Terrile MC, Paris R, Calderon-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongue CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. The Plant Journal 70, 492–500.
Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor.CrossRef | 1:CAS:528:DC%2BC38XmslOgu74%3D&md5=e877d169329e6a4f9edb90eb468b434dCAS |

Turko IV, Murad F (2002) Protein nitration in cardiovascular diseases. Pharmacological Reviews 54, 619–634.
Protein nitration in cardiovascular diseases.CrossRef | 1:CAS:528:DC%2BD38Xps1GrsL4%3D&md5=50c5c1817a6683dd196fdcdb94e59f49CAS |

Valderrama R, Corpas FJ, Carreras A, Gomez-Rodriguez MV, Chaki M, Pedrajas JR, Fernandez-Ocana ANA, del Rio LA, Barroso JB (2006) The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant, Cell & Environment 29, 1449–1459.
The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants.CrossRef | 1:CAS:528:DC%2BD28XnsVGjs7g%3D&md5=3d4c2b7ec3456a6989c3c25f4c525c31CAS |

Valderrama R, Corpas FJ, Carreras A, Fernandez-Ocana A, Chaki M, Luque F, Gomez-Rodriguez MV, Colmenero-Varea P, del Rio LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Letters 581, 453–461.
Nitrosative stress in plants.CrossRef | 1:CAS:528:DC%2BD2sXhtVKnu70%3D&md5=8f2f295de5514ee217bbf109142592c3CAS |

Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A, Taylor P, Xue P, Yang FQ, Xie ZS, Pallas JA, Chu CC, Loake GJ (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. Journal of Biological Chemistry 284, 2131–2137.
S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity.CrossRef | 1:CAS:528:DC%2BD1MXlvFaruw%3D%3D&md5=3b6df74973bd34d8bcf2a358e1f2f423CAS |

Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proceedings of the National Academy of Sciences of the United States of America 112, 613–618.
Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1.CrossRef | 1:CAS:528:DC%2BC2MXltVag&md5=7cd34338d28a1344a635832c5dfea190CAS |

Wawer I, Bucholc M, Astier J, Anielska-Mazur A, Dahan J, Kulik A, Wyslouch-Cieszynska A, Zareba-Koziol M, Krzywinska E, Dadlez M, Dobrowolska G, Wendehenne D (2010) Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. The Biochemical Journal 429, 73–83.
Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity.CrossRef | 1:CAS:528:DC%2BC3cXnsVaqu7k%3D&md5=e9f1c64967c604f25bd2daccf336bbd0CAS |

Xu S, Guerra D, Lee U, Vierling E (2013) S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Frontiers in Plant Science 4, 430
S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis.CrossRef |

Yadav S, David A, Baluška F, Bhatla SC (2013) Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls. Plant Signaling & Behavior 8, e23196
Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls.CrossRef |

Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiology 167, 1604–1615.
S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses.CrossRef | 1:CAS:528:DC%2BC2MXmtFais7s%3D&md5=c4dbf50fdd8a9476dec955ddab68e071CAS |

Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GA (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264–268.
S-nitrosylation of NADPH oxidase regulates cell death in plant immunity.CrossRef | 1:CAS:528:DC%2BC3MXht1GqsL%2FN&md5=4cbe8cbfcb7e7618ba74cf2519557f5eCAS |

Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. Journal of Biological Chemistry 288, 22777–22789.
Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC3sXht1WhtLrE&md5=827bf30e865f7ba4ce1b322590992d60CAS |

Zaffagnini M, De Mia M, Morisse S, Di Giacinto N, Marchand CH, Maes A, Lemaire SD, Trost P (2016) Protein S-nitrosylation in photosynthetic organisms: a comprehensive overview with future perspectives. Biochimica et Biophysica Acta 1864, 952–966.
Protein S-nitrosylation in photosynthetic organisms: a comprehensive overview with future perspectives.CrossRef | 1:CAS:528:DC%2BC28XisVegtbw%3D&md5=99773a43c247fd3f550f1d6718bea3e6CAS |

Ziogas V, Tanou G, Belghazi M, Filippou P, Fotopoulos V, Grigorios D, Molassiotis A (2015) Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants. Plant Molecular Biology 89, 433–450.
Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants.CrossRef | 1:CAS:528:DC%2BC2MXhsFGku7vL&md5=436bb1dafdb073cf98d2b2ffc1c62533CAS |



Export Citation