Protein S-nitrosylation in plant abiotic stresses
Jing Zhang A and Weibiao Liao
A B
+ Author Affiliations
- Author Affiliations
A College of Horticulture, Gansu Agricultural University, 1 Yinmen Village, Anning District, Lanzhou 730070, PR China.
B Corresponding author. Email: liaowb@gsau.edu.cn
Functional Plant Biology 47(1) 1-10 https://doi.org/10.1071/FP19071
Submitted: 8 March 2019 Accepted: 26 July 2019 Published: 2 December 2019
Abstract
Plants are exposed to various environmental stresses that affect crop growth and production. During stress, various physiological and biochemical changes including the production of nitric oxide (NO), take place. It is clear that NO could work through either transcriptional or post-translational level. The redox-based post-translational modification S-nitrosylation – the covalent attachment of an NO moiety to a reactive cysteine thiol of a protein to form an S-nitrosothiol (SNO) – has attracted increasing attention in the regulation of abiotic stress signalling. So far, the relevance of S-nitrosylation of certain proteins has been investigated under abiotic stress. In this work, we focus on the current state of knowledge regarding S-nitrosylation in plants under abiotic stress, and provide a better understanding of the relevance of S-nitrosylation in plant response to abiotic stress.
Additional keywords: nitric oxide, NO, plant resistance, stress proteins.
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 | GoogleScholarGoogle Scholar | 19655309PubMed |
Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Delrio 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 | GoogleScholarGoogle Scholar |
Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sánchez-Vicente I, Nambara E, Lorenzo O (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nature Communications 6, 8669
| S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth.Crossref | GoogleScholarGoogle Scholar | 26493030PubMed |
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 | GoogleScholarGoogle Scholar | 23203119PubMed |
Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Science 181, 527–533.
| S-nitrosylation: an emerging post-translational protein modification in plants.Crossref | GoogleScholarGoogle Scholar | 21893248PubMed |
Astier J, Kulik E, Koen A, Besson-Bard S, Bourque S, Jeandroz O, Lamotte D, Wendehenne D (2012) 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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 21887310PubMed |
Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocana A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. Journal of Experimental Botany 57, 1785–1793.
| Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress.Crossref | GoogleScholarGoogle Scholar | 16595575PubMed |
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2013) 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 | GoogleScholarGoogle Scholar | 24288182PubMed |
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-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 | GoogleScholarGoogle Scholar | 26116026PubMed |
Camejo D, del Carmen Romero-Puertas M, 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 | GoogleScholarGoogle Scholar | 23238061PubMed |
Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) 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 and 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 | GoogleScholarGoogle Scholar | 21676000PubMed |
Chen X, Tian D, Kong X, Chen Q, EF A-A, Hu X, Jia A (2016) The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii. Planta 244, 651–669.
| The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 27116428PubMed |
Corpas FJ, Chaki M, Fernandez-Ocana A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río 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 | GoogleScholarGoogle Scholar |
Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO–) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Annals of Botany 113, 87–96.
| Peroxynitrite (ONOO–) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress.Crossref | GoogleScholarGoogle Scholar | 24232384PubMed |
Cui B, Pan Q, Clarke D, Villarreal MO, Umbreen S, Yuan B, Shan W, Jiang J, Loake GJ (2018) S-nitrosylation of the zinc finger protein SRG1 regulates plant immunity. Nature Communications 9, 4226
| S-nitrosylation of the zinc finger protein SRG1 regulates plant immunity.Crossref | GoogleScholarGoogle Scholar | 30315167PubMed |
De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Schiavo FL (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 | GoogleScholarGoogle Scholar | 19261736PubMed |
de Pinto MC, Locato V, Sgobba A, del Carmen Romero-Puertas M, Gadadeta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of the programmed cell death signaling in tobacco By-2 cells. Plant Physiology 163, 1766–1775.
Elviri L, Speroni F, Careri M, Mangia A, di Toppi LS, Zottini M (2010) Identification of in vivo nitrosylated phytochelatins in Arabidopsis thaliana cells by liquid chromatography-direct electrospray-linear ion trap-mass spectrometry. Journal of Chromatography A 1217, 4120–4126.
| Identification of in vivo nitrosylated phytochelatins in Arabidopsis thaliana cells by liquid chromatography-direct electrospray-linear ion trap-mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 20227082PubMed |
Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant, Cell & Environment 40, 462–472.
| Nitric oxide function in plant abiotic stress.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 22115780PubMed |
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 | GoogleScholarGoogle Scholar | 15911759PubMed |
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 | GoogleScholarGoogle Scholar | 11457969PubMed |
García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiology 128, 790–792.
| Nitric oxide and abscisic acid cross talk in guard cells.Crossref | GoogleScholarGoogle Scholar | 11891235PubMed |
Gietler M, Nykiel M, Orzechowski S, Fettke J, Zagdańska B (2016) Proteomic analysis of S-nitrosylated and S-glutathionylated proteins in wheat seedlings with different dehydration tolerances. Plant Physiology and Biochemistry 108, 507–518.
| Proteomic analysis of S-nitrosylated and S-glutathionylated proteins in wheat seedlings with different dehydration tolerances.Crossref | GoogleScholarGoogle Scholar | 27596017PubMed |
Gong B, Wen D, Wang X, Wei M, Yang F, Li Y, Shi Q (2014) S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L. Plant & Cell Physiology 56, 790–802.
| S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 27064847PubMed |
Hess DT, Stamler JS (2012) Regulation by S-nitrosylation of protein post translational modification Journal of Biological Chemistry 287, 4411–4418.
| Regulation by S-nitrosylation of protein post translational modificationCrossref | GoogleScholarGoogle Scholar | 22147701PubMed |
Hogg N (2000) Biological chemistry and clinical potential of S-nitrosothiols. Free Radical Biology and Medicine 28, 1478–1486.
| Biological chemistry and clinical potential of S-nitrosothiols.Crossref | GoogleScholarGoogle Scholar | 10927172PubMed |
Hong SW, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures Plant Physiology 132, 757–767.
| Arabidopsis hot mutants define multiple functions required for acclimation to high temperaturesCrossref | GoogleScholarGoogle Scholar | 12805605PubMed |
Hu J, Yang H, Mu J, Lu T, Peng J, Deng X, Kong Z, Bao S, Cao X, Zuo J (2017) Nitric oxide regulates protein methylation during stress responses in plants. Molecular Cell 67, 702–710.e4.
| Nitric oxide regulates protein methylation during stress responses in plants.Crossref | GoogleScholarGoogle Scholar | 28757206PubMed |
Jain P, von Toerne C, Lindermayr C, Bhatla SC (2018) S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing in sunflower seedlings. Physiologia Plantarum 162, 49–72.
| S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing in sunflower seedlings.Crossref | GoogleScholarGoogle Scholar | 28902403PubMed |
Jourd’heuil D, Mai CT, Laroux FS, Wink DA, Grisham MB (1998) The reaction of S-nitrosoglutathione with superoxide. Biochemical and Biophysical Research Communications 244, 525–530.
| The reaction of S-nitrosoglutathione with superoxide.Crossref | GoogleScholarGoogle Scholar | 9514894PubMed |
Kovacs I, Lindermayr C (2013) Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Frontiers in Plant Science 4, 137
| Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation.Crossref | GoogleScholarGoogle Scholar | 23717319PubMed |
Lamotte O, Bertoldo JB, Besson-Bard A, Rosnoblet C, Aimé S, Hichami S, Terenzi H, Wendehenne D (2015) Protein S-nitrosylation: specificity and identification strategies in plants. Frontiers in Chemistry 2, 114
| Protein S-nitrosylation: specificity and identification strategies in plants.Crossref | GoogleScholarGoogle Scholar | 25750911PubMed |
Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. The Plant Cell 20, 786–802.
| Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18326829PubMed |
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) 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 | GoogleScholarGoogle Scholar | 22504427PubMed |
Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang H, 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 | GoogleScholarGoogle Scholar | 22106097PubMed |
Malik SI, Hussein A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated denitrosylation in the plant defence response. Plant Science 181, 540–544.
| GSNOR-mediated denitrosylation in the plant defence response.Crossref | GoogleScholarGoogle Scholar | 21893250PubMed |
Marino SM, Gladyshev VN (2010) Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation. Journal of Molecular Biology 395, 844–859.
| Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation.Crossref | GoogleScholarGoogle Scholar | 19854201PubMed |
Nakamura T, Lipton SA (2011) Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases Cell Death and Differentiation 18, 1478–1486.
| Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseasesCrossref | GoogleScholarGoogle Scholar | 21597461PubMed |
Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño 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 | GoogleScholarGoogle Scholar | 22213812PubMed |
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 | GoogleScholarGoogle Scholar | 15367716PubMed |
Puyaubert J, Fares A, Rézé N, Peltier JB, Baudouin E (2014) Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Science 215–216, 150–156.
| Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level.Crossref | GoogleScholarGoogle Scholar | 24388526PubMed |
Romero-Puertas MC, Rodríguez-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 | GoogleScholarGoogle Scholar | 24065977PubMed |
Sehrawat A, Deswal R (2014a) Sub-proteome S-nitrosylation analysis in Brassica juncea hints at the regulation of Brassicaceae specific as well as other vital metabolic pathway(s) by nitric oxide and suggests post-translational modifications cross-talk. Nitric Oxide 43, 97–111.
| Sub-proteome S-nitrosylation analysis in Brassica juncea hints at the regulation of Brassicaceae specific as well as other vital metabolic pathway(s) by nitric oxide and suggests post-translational modifications cross-talk.Crossref | GoogleScholarGoogle Scholar | 25175897PubMed |
Sehrawat A, Deswal R (2014b) S-nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signaling. Journal of Proteome Research 13, 2599–2619.
| S-nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signaling.Crossref | GoogleScholarGoogle Scholar | 24684139PubMed |
Sehrawat A, Gupta R, Deswal R (2013a) Nitric oxide‐cold stress signalling crosstalk, evolution of a novel regulatory mechanism. Proteomics 13, 1816–1835.
| Nitric oxide‐cold stress signalling crosstalk, evolution of a novel regulatory mechanism.Crossref | GoogleScholarGoogle Scholar | 23580434PubMed |
Sehrawat A, Abat JK, Deswal R (2013b) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Frontiers in Plant Science 4, 342
| RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea.Crossref | GoogleScholarGoogle Scholar | 24032038PubMed |
Sengupta R, Holmgren A (2012) Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation. Antioxidants & Redox Signalling 18, 259–269.
| Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation.Crossref | GoogleScholarGoogle Scholar |
Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochemical and Biophysical Research Communications 361, 1048–1053.
| Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation.Crossref | GoogleScholarGoogle Scholar | 17686455PubMed |
Sun J, Steenbergen C, Murphy E (2006) S-nitrosylation: NO-related redox signaling to protect against oxidative stress. Antioxidants & Redox Signalling 8, 1693–1705.
| S-nitrosylation: NO-related redox signaling to protect against oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Athannasios M, 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 | GoogleScholarGoogle Scholar | 19682288PubMed |
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 | GoogleScholarGoogle Scholar | 22780834PubMed |
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. Proteins and Proteomics 1844, 810–817.
| S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Letters 581, 453–461.
| Nitrosative stress in plants.Crossref | GoogleScholarGoogle Scholar | 17240373PubMed |
Vanzo E, Ghirardo A, Merl-Pham J, Lindermayr C, Heller W, Hauck SM, Durner J, Schnitzler JP (2014) S-nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS One 9, e106886
| S-nitroso-proteome in poplar leaves in response to acute ozone stress.Crossref | GoogleScholarGoogle Scholar | 25192423PubMed |
Wang D, Liu Y, Tan X, Liu H, Zeng G, Hu X, Jian H, Gu Y (2015a) Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress. Environmental Science and Pollution Research International 22, 3489–3497.
| Effect of exogenous nitric oxide on antioxidative system and S-nitrosylation in leaves of Boehmeria nivea (L.) Gaud under cadmium stress.Crossref | GoogleScholarGoogle Scholar | 25242592PubMed |
Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015b) 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 | GoogleScholarGoogle Scholar | 25550508PubMed |
Wang P, Zhu JK, Lang Z (2015c) Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant Signaling & Behavior 10, e1031939
| Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins.Crossref | GoogleScholarGoogle Scholar |
Wawer I, Bucholc M, Astier J, Anielska-Mazur A, Dahan J, Kulik A, Wysłouch-Cieszynska A, Zaręba-Kozioł M, Krzywinska E, Dadlez M, Dobrowolska G (2010) Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. 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 | GoogleScholarGoogle Scholar | 20397974PubMed |
Zhan N, Wang C, Chen L, Yang H, Feng J, Gong X, Ren B, Wu R, Mu J, Li Y, Liu Z, Zhou Y, Peng J, Wang K, Huang X, Xiao S, Liu Z (2018) S-nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants. Molecular Cell 71, 142–154.e6.
| S-nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants.Crossref | GoogleScholarGoogle Scholar | 30008318PubMed |
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167, 313–324.
| Abiotic stress signaling and responses in plants.Crossref | GoogleScholarGoogle Scholar | 27716505PubMed |
Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiology and Biochemistry 68, 118–126.
| Nitrosative responses in citrus plants exposed to six abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 23685754PubMed |
