Regulation of protein function by reversible S-nitrosation, a post-translational modification based on the attachment of nitroso group to cysteine thiols, has emerged among key mechanisms of NO signalling in plant development and stress responses. S-nitrosoglutathione is regarded as the most abundant low-molecular-weight S-nitrosothiol in plants, where its intracellular concentrations are modulated by S-nitrosoglutathione reductase. We analysed modulations of S-nitrosothiols and protein S-nitrosation mediated by S-nitrosoglutathione reductase in cultivated Solanum lycopersicum (susceptible) and wild Solanum habrochaites (resistant genotype) up to 96 h post inoculation (hpi) by two hemibiotrophic oomycetes, Phytophthora infestans and Phytophthora parasitica. S-nitrosoglutathione reductase activity and protein level were decreased by P. infestans and P. parasitica infection in both genotypes, whereas protein S-nitrosothiols were increased by P. infestans infection, particularly at 72 hpi related to pathogen biotrophy-necrotrophy transition. Increased levels of S-nitrosothiols localised in both proximal and distal parts to the infection site, which suggests together with their localisation to vascular bundles a signalling role in systemic responses. S-nitrosation targets in plants infected with P. infestans identified by a proteomic analysis include namely antioxidant and defence proteins, together with important proteins of metabolic, regulatory and structural functions. Ascorbate peroxidase S-nitrosation was observed in both genotypes in parallel to increased enzyme activity and protein level during P. infestans pathogenesis, namely in the susceptible genotype. These results show important regulatory functions of protein S-nitrosation in concerting molecular mechanisms of plant resistance to hemibiotrophic pathogens.

Department of Biochemistry Faculty of Science Masaryk University Kamenice 753 5 CZ 625 00 Brno Czech Republic

Department of Biochemistry Palacký University Šlechtitelů 27 CZ 783 71 Olomouc Czech Republic

Department of Botany Faculty of Science Palacký University Šlechtitelů 27 CZ 783 71 Olomouc Czech Republic

Zobrazit více v PubMed

Kolbert Z, et al. A forty year journey: the generation and roles of NO in plants. Nitric Oxide. 2019;93:53–70. doi: 10.1016/j.niox.2019.09.006. PubMed DOI

Umbreen S, et al. Specificity in nitric oxide signalling. J. Exp. Bot. 2018;69:3439–3448. doi: 10.1093/jxb/ery184. PubMed DOI

Lindermayr C, Saalbach G, Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 2005;137:921–930. doi: 10.1104/pp.104.058719. PubMed DOI PMC

Begara-Morales JC, et al. Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot. 2015;66:5983–5996. doi: 10.1093/jxb/erv306. PubMed DOI PMC

Holtgrefe S, et al. Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol. Plant. 2008;133:211–228. doi: 10.1111/j.1399-3054.2008.01066.x. PubMed DOI

Lindermayr C, Saalbach G, Bahnweg G, Durner J. Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J. Biol. Chem. 2006;281:4285–4291. doi: 10.1074/jbc.M511635200. PubMed DOI

Yun BW, et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature. 2011;478:264–268. doi: 10.1038/nature10427. PubMed DOI

Chaki M, et al. Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower mildew interaction. Plant Cell Physiol. 2009;50:265–279. doi: 10.1093/pcp/pcn196. PubMed DOI

Begara-Morales JC, et al. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 2014;65:527–538. doi: 10.1093/jxb/ert396. PubMed DOI PMC

Hu J, et al. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol. 2015;167:1731–1746. doi: 10.1104/pp.15.00026. PubMed DOI PMC

Jahnová, J., Luhová, L. & Petřivalský, M. S-nitrosoglutathione reductase—the master regulator of protein S-Nitrosation in plant NO signaling. Plants (Basel)8, 48 (2019). PubMed PMC

Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell. 2008;20:786–802. doi: 10.1105/tpc.107.052647. PubMed DOI PMC

Kwon E, et al. AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta. 2012;236:887–900. doi: 10.1007/s00425-012-1697-8. PubMed DOI

Xu S, Guerra D, Lee U, Vierling E. S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front. Plant Sci. 2013;4:430. doi: 10.3389/fpls.2013.00430. PubMed DOI PMC

Tichá T, et al. Characterization of S-nitrosoglutathione reductase from Brassica and Lactuca spp. and its modulation during plant development. Nitric Oxide. 2017;68:68–76. doi: 10.1016/j.niox.2016.12.002. PubMed DOI

Gong B, Yan Y, Zhang L, Cheng F, Liu Z, Shi Q. Unravelling GSNOR-mediated S-nitrosylation and multiple developmental programs in tomato plants. Plant Cell Physiol. 2019;60:2523–2537. doi: 10.1093/pcp/pcz143. PubMed DOI

Hussain A, Yun BW, Kim JH, Gupta KJ, Hyung NI, Loake GJ. Novel and conserved functions of S-nitrosoglutathione reductase in tomato. J. Exp. Bot. 2019;70:4877–4886. doi: 10.1093/jxb/erz234. PubMed DOI PMC

Feechan A, et al. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl Acad. Sci. USA. 2005;102:8054–8059. doi: 10.1073/pnas.0501456102. PubMed DOI PMC

Tada Y, et al. Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science. 2008;321:952–956. doi: 10.1126/science.1156970. PubMed DOI PMC

Yun BW, et al. Nitric oxide and S-nitrosoglutathione function additively during plant immunity. N. Phytol. 2016;211:516–526. doi: 10.1111/nph.13903. PubMed DOI

Rusterucci C, Espunya MC, Diaz M, Chabannes M, Martinez MC. S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol. 2007;143:1282–1292. doi: 10.1104/pp.106.091686. PubMed DOI PMC

Piterková J, et al. Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol. Plant Pathol. 2009;10:501–513. doi: 10.1111/j.1364-3703.2009.00551.x. PubMed DOI PMC

Tichá T, et al. Involvement of S-nitrosothiols modulation by S-nitrosoglutathione reductase in defence responses of lettuce and wild Lactuca spp. to biotrophic mildews. Planta. 2018;247:1203–1215. doi: 10.1007/s00425-018-2858-1. PubMed DOI

Jahnová J, et al. Differential modulation of S-nitrosoglutathione reductase and reactive nitrogen species in wild and cultivated tomato genotypes during development and powdery mildew infection. Plant Physiol. Biochem. 2020;155:297–310. doi: 10.1016/j.plaphy.2020.06.039. PubMed DOI

Meng Y, Zhang Q, Ding W, Shan W. Phytophthora parasitica: a model oomycete plant pathogen. Mycology. 2014;5:43–51. doi: 10.1080/21501203.2014.917734. PubMed DOI PMC

Nowicki M, Foolad MR, Nowakowska M, Kozik EU. Potato and tomato late blight caused by Phytophthora infestans: an overview of pathology and resistance breeding. Plant Dis. 2011;96:4–17. doi: 10.1094/PDIS-05-11-0458. PubMed DOI

Piterková J, et al. Dual role of nitric oxide in Solanum spp.—Oidium neolycopersici interactions. Environ. Exp. Bot. 2011;74:37–44. doi: 10.1016/j.envexpbot.2011.04.016. DOI

Kubienová L, et al. Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie. 2013;95:889–902. doi: 10.1016/j.biochi.2012.12.009. PubMed DOI

Foolad MR, Merk HL, Ashrafi H. Genetics, genomics and breeding of late blight and early blight resistance in tomato. CRC Crit. Rev. Plant Sci. 2008;27:75–107. doi: 10.1080/07352680802147353. DOI

Elsayed AY, da Silva DJH, Souza Carneiro PC, Gomide Mizubiti ES. The inheritance of late blight resistance derived from Solanum habrochaites. Crop Breed. Appl. Biotechnol. 2012;12:199–205. doi: 10.1590/S1984-70332012000300006. DOI

Lindermayr C, Durner J. S-Nitrosylation in plants: pattern and function. J. Proteom. 2009;73:1–9. doi: 10.1016/j.jprot.2009.07.002. PubMed DOI

Yu M, Yun BW, Spoel SH, Loake GJ. A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. Curr. Opin. plant Biol. 2012;15:424–430. doi: 10.1016/j.pbi.2012.03.005. PubMed DOI

Janus Ł, et al. Normoergic NO-dependent changes, triggered by a SAR inducer in potato, create more potent defense responses to Phytophthora infestans. Plant Sci. 2013;211:23–34. doi: 10.1016/j.plantsci.2013.06.007. PubMed DOI

Valderrama R, et al. Nitrosative stress in plants. FEBS Lett. 2007;581:453–461. doi: 10.1016/j.febslet.2007.01.006. PubMed DOI

Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 2001;3:193–197. doi: 10.1038/35055104. PubMed DOI

Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866–1875. doi: 10.1105/tpc.105.033589. PubMed DOI PMC

Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L. Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J. Exp. Bot. 2013;64:3339–3349. doi: 10.1093/jxb/ert172. PubMed DOI

Yang H, et al. S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol. 2015;167:1604–1615. doi: 10.1104/pp.114.255216. PubMed DOI PMC

Puyaubert J, Fares A, Rézé N, Peltier JB, Baudouin E. Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: Effect of cold stress on cysteine nitrosylation level. Plant Sci. 2014;215:150–156. doi: 10.1016/j.plantsci.2013.10.014. PubMed DOI

Jedelská T, Kraiczová VŠ, Berčíková L, Činčalová L, Luhová L, Petřivalský M. Tomato root growth inhibition by salinity and cadmium is mediated by S-nitrosative modifications of ROS metabolic enzymes controlled by S-nitrosoglutathione reductase. Biomolecules. 2019;9:393. doi: 10.3390/biom9090393. PubMed DOI PMC

Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol. Biochem. 2008;46:941–950. doi: 10.1016/j.plaphy.2008.06.011. PubMed DOI

Iseli B, Boller T, Neuhaus JM. The N-terminal cysteine-rich domain of tobacco class I chitinase is essential for chitin binding but not for catalytic or antifungal activity. Plant Physiol. 1993;103:221–226. doi: 10.1104/pp.103.1.221. PubMed DOI PMC

Park CJ, Seo YS. Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol. J. 2015;31:323–333. doi: 10.5423/PPJ.RW.08.2015.0150. PubMed DOI PMC

Maldonado-Alconada AM, et al. Proteomic analysis of Arabidopsis protein S-nitrosylation in response to inoculation with Pseudomonas syringae. Acta Physiol. Plant. 2011;33:1493–1514. doi: 10.1007/s11738-010-0688-2. DOI

Martínez-Ruiz A, et al. S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc. Natl Acad. Sci. USA. 2005;102:8525–8530. doi: 10.1073/pnas.0407294102. PubMed DOI PMC

Huang B, Li FA, Wu CH, Wang DL. The role of nitric oxide on rosuvastatin-mediated S-nitrosylation and translational proteomes in human umbilical vein endothelial cells. Proteome Sci. 2012;10:43. doi: 10.1186/1477-5956-10-43. PubMed DOI PMC

Pajares M, et al. Redox control of protein degradation. Redox Biol. 2015;6:409–420. doi: 10.1016/j.redox.2015.07.003. PubMed DOI PMC

Nakamura T, et al. Aberrant protein S-nitrosylation in neurodegenerative diseases. Neuron. 2013;78:596–614. doi: 10.1016/j.neuron.2013.05.005. PubMed DOI PMC

Dielen AS, Badaoui S, Candresse T, German-Retana S. The ubiquitin/26S proteasome system in plant-pathogen interactions: a never-ending hide-and-seek game. Mol. Plant Pathol. 2010;11:293–308. doi: 10.1111/j.1364-3703.2009.00596.x. PubMed DOI PMC

Bhaskar PB, et al. Sgt1, but not Rar1, is essential for the RB-mediated broad-spectrum resistance to potato late blight. BMC Plant Biol. 2008;8:8. doi: 10.1186/1471-2229-8-8. PubMed DOI PMC

Ballvora A, et al. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 2002;30:361–371. doi: 10.1046/j.1365-313X.2001.01292.x. PubMed DOI

Qutob D, Tedman-Jones J, Gijzen M. Effector-triggered immunity by the plant pathogen Phytophthora. Trends Microbiol. 2006;14:470–473. doi: 10.1016/j.tim.2006.09.004. PubMed DOI

Du Y, Berg J, Govers F, Bouwmeester K. Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and the effector AVR1. N. Phytol. 2015;207:735–747. doi: 10.1111/nph.13355. PubMed DOI

Sevilla F, et al. The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J. Exp. Bot. 2015;66:2945–2955. doi: 10.1093/jxb/erv146. PubMed DOI

Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH. Selective protein denitrosylation activity of Thioredoxin-h5 modulates plant Immunity. Mol. Cell. 2014;56:153–162. doi: 10.1016/j.molcel.2014.08.003. PubMed DOI

Romero-Puertas MC, Delledonne M. S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Free Radic. Res. 2007;41:4120–4130. PubMed PMC

Camejo D, et al. Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J. Proteom. 2013;79:87–99. doi: 10.1016/j.jprot.2012.12.003. PubMed DOI

Chang AH, et al. Respiratory substrates regulate S-nitrosylation of mitochondrial proteins through a thiol-dependent pathway. Chem. Res. Toxicol. 2014;27:794–804. doi: 10.1021/tx400462r. PubMed DOI PMC

Wang SB, et al. Redox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ. Res. 2011;109:750–757. doi: 10.1161/CIRCRESAHA.111.246124. PubMed DOI PMC

Miedes E, Vanholme R, Boerjan W, Molina A. The role of the secondary cell wall in plant resistance to pathogens. Front. Plant Sci. 2014;5:358. doi: 10.3389/fpls.2014.00358. PubMed DOI PMC

Böhm FMLZ, Ferrarese MDLL, Zanardo DIL, Magalhaes JR, Ferrarese-Filho O. Nitric oxide affecting root growth, lignification and related enzymes in soybean seedlings. Acta Physiol. Plant. 2010;32:1039–1046. doi: 10.1007/s11738-010-0494-x. DOI

Enkhardt U, Pommer U. Influence of nitric oxide and nitrite on the activity of cinnamic acid 4-hydroxylase of Zea mays in vitro. J. Appl. Bot. 2000;74:151–154.

Monzón GC, Regente M, Pinedo M, Lamattina L, de la Canal L. Effects of nitric oxide on sunflower seedlings: a balance between defense and development. Plant Signal. Behav. 2015;10:e992285. doi: 10.4161/15592324.2014.992285. PubMed DOI PMC

Jain P, von Toerne C, Lindermayr C, Bhatla SC. S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing in sunflower seedlings. Physiol. Plant. 2018;162:49–72. doi: 10.1111/ppl.12641. PubMed DOI

Romero JM, Carrizo ME, Curtino JA. Characterization of human triosephosphate isomerase S-nitrosylation. Nitric Oxide. 2018;77:26–34. doi: 10.1016/j.niox.2018.04.004. PubMed DOI

Wang J, et al. Nitric oxide modifies root growth by S-nitrosylation of plastidial glyceraldehyde-3-phosphate dehydrogenase. Biochem. Biophys. Res. Commun. 2017;488:88–94. doi: 10.1016/j.bbrc.2017.05.012. PubMed DOI

Swatek KN, Graham K, Agrawal GK, Thelen JJ. The 14-3-3 isoforms Chi and Epsilon differentially bind client proteins from developing Arabidopsis seed. J. Proteome Res. 2011;10:4076–4087. doi: 10.1021/pr200263m. PubMed DOI

Sedlářová M, Binarová P, Lebeda A. Changes in microtubular alignment in Lactuca spp. (Asteraceae) epidermal cells during early stages of infection by Bremia lactucae (Peronosporaceae) Phyton. 2001;41:21–33.

Kasprowicz A, Szuba A, Volkmann D, Baluska F, Wojtaszek P. Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J. Exp. Bot. 2009;60:1605–1617. doi: 10.1093/jxb/erp033. PubMed DOI PMC

Pasqualini S, et al. Roles for NO and ROS signalling in pollen germination and pollen-tube elongation in Cupressus arizonica. Biol. Plant. 2015;59:735–744. doi: 10.1007/s10535-015-0538-6. DOI

Rodríguez-Serrano M, et al. 2,4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics. J. Exp. Bot. 2014;65:4783–4793. doi: 10.1093/jxb/eru237. PubMed DOI PMC

Bradford MM. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Xue Y, et al. GPS-SNO: computational prediction of protein S-nitrosylation sites with a modified GPS algorithm. PLoS ONE. 2010;5:e11290. doi: 10.1371/journal.pone.0011290. PubMed DOI PMC

Xu Y, Ding J, Wu LY, Chou KC. iSNO-PseAAC: predict cysteine S-nitrosylation sites in proteins by incorporating position specific amino acid propensity into pseudo amino acid composition. PLoS ONE. 2013;8:e55844. doi: 10.1371/journal.pone.0055844. PubMed DOI PMC

Clark D, Durner J, Navarre DA, Klessig DF. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol. Plant-Microbe Interact. 2000;13:1380–1384. doi: 10.1094/MPMI.2000.13.12.1380. PubMed DOI

Lin A, et al. Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol. 2012;158:451–464. doi: 10.1104/pp.111.184531. PubMed DOI PMC

Tanou G, et al. Oxidative and nitrosative‐based signaling and associated post‐translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 2012;72:585–599. doi: 10.1111/j.1365-313X.2012.05100.x. PubMed DOI

Correa-Aragunde N, Foresi N, Lamattina L. Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J. Exp. Bot. 2015;66:2913–2921. doi: 10.1093/jxb/erv073. PubMed DOI

de Pinto MC, et al. S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol. 2013;163:1766–1775. doi: 10.1104/pp.113.222703. PubMed DOI PMC

Fares A, Rossignol M, Peltier JB. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem. Biophys. Res. Commun. 2011;416:331–336. doi: 10.1016/j.bbrc.2011.11.036. PubMed DOI

Kato H, Takemoto D, Kawakita K. Proteomic analysis of S‐nitrosylated proteins in potato plant. Physiol. Plant. 2013;148:371–386. doi: 10.1111/j.1399-3054.2012.01684.x. PubMed DOI

Abat JK, Saigal P, Deswal R. S-Nitrosylation—another biological switch like phosphorylation? Physiol. Mol. Biol. Plants. 2008;14:119–130. doi: 10.1007/s12298-008-0011-5. PubMed DOI PMC

Cheng T, et al. Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress. Planta. 2015;242:1361–1390. doi: 10.1007/s00425-015-2374-5. PubMed DOI

Tanou G, Job C, Belghazi M, Molassiotis A, Diamantidis G, Job D. Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants. J. Proteome Res. 2010;9:5994–6006. doi: 10.1021/pr100782h. PubMed DOI

Eaton P, et al. Reversible cysteine-targeted oxidation of proteins during renal oxidative stress. J. Am. Soc. Nephrol. 2003;14(suppl 3):S290–S296. doi: 10.1097/01.ASN.0000078024.50060.C6. PubMed DOI

Vescovi M, Zaffagnini M, Festa M, Trost P, Schiavo FL, Costa A. Nuclear accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase in cadmium-stressed Arabidopsis roots. Plant Physiol. 2013;162:333–346. doi: 10.1104/pp.113.215194. PubMed DOI PMC

Wawer I, et al. Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. Biochem. J. 2010;429:73–83. doi: 10.1042/BJ20100492. PubMed DOI

Henry E, Fung N, Liu J, Drakakaki G, Coaker G. Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLoS Genet. 2015;11:e1005199. doi: 10.1371/journal.pgen.1005199. PubMed DOI PMC

Testard A, et al. Calcium-and nitric oxide-dependent nuclear accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase in response to long chain bases in tobacco BY-2 cells. Plant Cell Physiol. 2016;57:2221–2231. doi: 10.1093/pcp/pcw137. PubMed DOI

Tanou G, et al. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J. 2009;60:795–804. doi: 10.1111/j.1365-313X.2009.04000.x. PubMed DOI

Bedhomme M, et al. Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem. J. 2012;445:337–347. doi: 10.1042/BJ20120505. PubMed DOI

Zaffagnini M, et al. Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J. Biol. Chem. 2013;288:22777–22789. doi: 10.1074/jbc.M113.475467. PubMed DOI PMC

Doulias PT, et al. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc. Natl. Acad. Sci. 2010;107:16958–16963. doi: 10.1073/pnas.1008036107. PubMed DOI PMC