S-nitrosoglutathione reductase (GSNOR) exerts crucial roles in the homeostasis of nitric oxide (NO) and reactive nitrogen species (RNS) in plant cells through indirect control of S-nitrosation, an important protein post-translational modification in signaling pathways of NO. Using cultivated and wild tomato species, we studied GSNOR function in interactions of key enzymes of reactive oxygen species (ROS) metabolism with RNS mediated by protein S-nitrosation during tomato root growth and responses to salinity and cadmium. Application of a GSNOR inhibitor N6022 increased both NO and S-nitrosothiol levels and stimulated root growth in both genotypes. Moreover, N6022 treatment, as well as S-nitrosoglutathione (GSNO) application, caused intensive S-nitrosation of important enzymes of ROS metabolism, NADPH oxidase (NADPHox) and ascorbate peroxidase (APX). Under abiotic stress, activities of APX and NADPHox were modulated by S-nitrosation. Increased production of H2O2 and subsequent oxidative stress were observed in wild Solanumhabrochaites, together with increased GSNOR activity and reduced S-nitrosothiols. An opposite effect occurred in cultivated S. lycopersicum, where reduced GSNOR activity and intensive S-nitrosation resulted in reduced ROS levels by abiotic stress. These data suggest stress-triggered disruption of ROS homeostasis, mediated by modulation of RNS and S-nitrosation of NADPHox and APX, underlies tomato root growth inhibition by salinity and cadmium stress.

Department of Biochemistry Faculty of Science Palacký University CZ 783 71 Olomouc Czech Republic

Present address Department of Environmental Protection Engineering Faculty of Technology Tomas Bata University in Zlín 760 01 Zlín Czech Republic

Present address Department of Immunology Faculty of Medicine and Dentistry Palacký University CZ 77900 Olomouc Czech Republic

Zobrazit více v PubMed

Kolbert Z. Implication of nitric oxide (NO) in excess element-induced morphogenic responses of the root system. Plant Physiol. Biochem. 2016;101:149–161. doi: 10.1016/j.plaphy.2016.02.003. PubMed DOI

Baxter A., Mittler R., Suzuki N. ROS as key players in plant stress signalling. J. Exp. Bot. 2014;65:1229–1240. doi: 10.1093/jxb/ert375. PubMed DOI

Yu M., Lamattina L., Spoel S.H., Loake G.J. Nitric oxide function in plant biology: A redox cue in deconvolution. New Phytol. 2014;202:1142–1156. doi: 10.1111/nph.12739. PubMed DOI

Yun B.W., Feechan A., Yin M., Saidi N.B., Le Bihan T., Yu M., Moore J.W., Kang J.G., Kwon E., Spoel S.H., et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature. 2011;478:264–268. doi: 10.1038/nature10427. PubMed DOI

Groß F., Durner J., Gaupels F. Nitric oxide, antioxidant and prooxidants in plant defence responses. Front. Plant Sci. 2013 doi: 10.3389/fpls.2013.00419. PubMed DOI PMC

Beligni M.V., Lamattina L. Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta. 1999;208:337–344. doi: 10.1007/s004250050567. DOI

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

Lin A., Wang Y., Tang J., Xue P., Li C., Liu L., Hu B., Yang F., Loake G.J., Chu C. 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

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

Begara-Morales J.C., Sánchez-Calvo B., Chaki M., Valderrama R., Mata-Pérez C., López-Jaramillo J., Padilla M.N., Carreras A., Corpas F.J., Barroso J.B. 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

Cheng T., Chen J., Abd Allah E.F., Wang P., Wang G., Hu X., Shi J. 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

de Pinto M.C., Locato V., Sgobba A., Romero-Puertas M.C., Gadaleta C., Delledonne M., De Gara L. 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

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., Mu J., Chen L., Feng J., Hu J., Li L. 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

Begara-Morales J.C., Sánchez-Calvo B., Chaki M., Mata-Pérez C., Valderrama R., Padilla M.N., López-Jaramillo J., Luque F., Corpas F.J., Barroso J.B. 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

Feechan A., Kwon E., Yun B.W., Wang Y., Pallas J.A., Loake G.J. 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

Liu L., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature. 2001;410:490–494. doi: 10.1038/35068596. PubMed DOI

Lee U., Wie C., Fernandez B.O., 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

Leterrier M., Chaki M., Airaki M., Valderrama R., Palma J.M., Barroso J.B., Corpas F.J. Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal. Behav. 2011;6:789–793. doi: 10.4161/psb.6.6.15161. PubMed DOI PMC

Airaki M., Leterrier M., Mateos R.M., Valderrama R., Chaki M., Barroso J.B., Del Río L.A., Palma J.M., Corpas F.J. Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ. 2012;35:281–295. doi: 10.1111/j.1365-3040.2011.02310.x. PubMed DOI

Kwon E., Feechan A., Yun B.W., Hwang B.H., Pallas J.A., Kang J.G., Loake G.J. AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta. 2012;236:887–900. doi: 10.1007/s00425-012-1697-8. PubMed DOI

Kubienová L., Kopečný D., Tylichová M., Briozzo P., Skopalová J., Šebela M., Navrátil M., Tâche R., Luhová L., Barroso J.B., 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

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 doi: 10.3389/fpls.2013.00430. PubMed DOI PMC

Jahnová J., Luhová L., Petřivalský M. S-Nitrosoglutathione Reductase-The Master Regulator of Protein S-Nitrosation in Plant NO Signaling. Plants. 2019;8:48. doi: 10.3390/plants8020048. PubMed DOI PMC

Camejo D., Romero-Puertas M.C., Rodríguez-Serrano M., Sandalio L.M., Lázaro J.J., Jiménez A., Sevilla F. 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

Gong B., Wen D., Wang X., Wei M., Yang F., Li Y., Shi Q. S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L. Plant Cell Physiol. 2015;56:790–802. doi: 10.1093/pcp/pcv007. PubMed DOI

Yang L., Tian D., Todd C.D., Luo Y., Hu X. Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J. Proteom. Res. 2013;12:1316–1330. doi: 10.1021/pr300971n. PubMed DOI

Frungillo L., Skelly M.J., Loake G.J., Spoel S.H., Salgado I. S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat. Commun. 2014 doi: 10.1038/ncomms6401. PubMed DOI PMC

Yang Y., Guo Y. Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol. 2018;217:523–539. doi: 10.1111/nph.14920. PubMed DOI

Dutta S., Mitra M., Agarwal P., Mahapatra K., De S., Sett U., Roy S. Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal. Behav. 2018 doi: 10.1080/15592324.2018.1460048. PubMed DOI PMC

Mlíčková K., Luhová L., Lebeda A., Mieslerová B., Peč P. Reactive oxygen species generation and peroxidase activity during Oidium neolycopersici infection on Lycopersicon species. Plant Physiol. Biochem. 2004;42:753–761. doi: 10.1016/j.plaphy.2004.07.007. PubMed DOI

Tománková K., Luhová L., Petřivalský M., Peč P., Lebeda A. Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiol Mol. Plant Pathol. 2006;68:22–32. doi: 10.1016/j.pmpp.2006.05.005. DOI

Piterková J., Hofman J., Mieslerová B., Sedlářová M., Luhová L., Lebeda A., Petřivalský M. 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

Tichá T., Sedlářová M., Činčalová L., Trojanová Z.D., Mieslerová B., Lebeda A., Luhová L., Petřivalský M. 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

Grandillo S., Chetelat R., Knapp S., Spooner D., Peralta I., Cammareri M., Ercolano M.R. Wild Crop Relatives: Genomic and Breeding Resources. Springer; Berlin/Heidelberg, Germany: 2011. Solanum sect. Lycopersicon; pp. 129–215.

Venema J.H., Dijk B.E., Bax J.M., van Hasselt P.R., Elzenga J.T.M. Grafting tomato (Solanum lycopersicum) onto the rootstock of a high-altitude accession of Solanum habrochaites improves suboptimal-temperature tolerance. Environ. Exp. Bot. 2008;63:359–367. doi: 10.1016/j.envexpbot.2007.12.015. DOI

Green L.S., Lawrence E.C., Patton A.K., Sun X., Rosenthal G.J., Richards J.P. Mechanism of inhibition for N6022, a first-in-class drug targeting S-nitrosoglutathione reductase. Biochemistry. 2012;51:2157–2168. doi: 10.1021/bi201785u. PubMed DOI

Moore K.P., Mani A.R. Measurement of protein nitration and S-nitrosothiol formation in biology and medicine. Meth. Enzymol. 2002;359:256–268. PubMed

Gow A., Doctor A., Mannick J., Gaston B. S-nitrosothiol measurements in biological systems. J. Chromatogr. 2007;851:140–151. doi: 10.1016/j.jchromb.2007.01.052. PubMed DOI PMC

Bradford M.M. Rapid and sensitive method for quantitation of mikrogram 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

Kubienová L., Tichá T., Jahnová J., Luhová L., Mieslerová B., Petřivalský M. Effect of abiotic stress stimuli on S nitrosoglutathione reductase in plants. Planta. 2014;239:139–146. doi: 10.1007/s00425-013-1970-5. PubMed DOI

Kaundal A., Rojas C.M., Mysore K.S. Measurement of NADPH oxidase activity in plants. Bio-Protocol. 2012 doi: 10.21769/BioProtoc.278. DOI

Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001 doi: 10.1093/nar/29.9.e45. PubMed DOI PMC

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

Corpas F.J., Carreras A., Esteban F.J., Chaki M., Valderrama R., Del Río L.A., Barroso J.B. Localization of S-nitrosothiols and assay of nitric oxide synthase and S-nitrosoglutathione reductase activity in plants. Meth. Enzymol. 2008;437:561–574. PubMed

Correa-Aragunde N., Graziano C.M., Lamattina L. Nitric oxide plays a central role in determining lateral root development in tomato. Planta. 2004;218:900–905. doi: 10.1007/s00425-003-1172-7. PubMed DOI

Pagnussat G.C., Simontacchi M., Puntarulo S., Lamattina L. Nitric oxide is required for root organogenesis. Plant Physiol. 2002;129:954–956. doi: 10.1104/pp.004036. PubMed DOI PMC

Fernández-Marcos M., Sanz L., Lewis D.R., Muday G.K., Lorenzo O. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PINFORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. USA. 2011;108:18506–18511. doi: 10.1073/pnas.1108644108. PubMed DOI PMC

Fernández-Marcos M., Sanz L., Lorenzo O. Nitric oxide: An emerging regulator of cell elongation during primary root growth. Plant Signal. Behav. 2012;7:196–200. doi: 10.4161/psb.18895. PubMed DOI PMC

Tichá T., Činčalová L., Kopečný D., Sedlářová M., Kopečná M., Luhová L., Petřivalský M. 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

Chen R., Sun S., Wang C., Li Y., Liang Y., An F. The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res. 2009;19:1377–1387. doi: 10.1038/cr.2009.117. PubMed DOI

Holzmeister C., Fröhlich A., Sarioglu H., Bauer N., Durner J., Lindermayr C. Proteomic analysis of defense response of wildtype Arabidopsis thaliana and plants with impaired NO homeostasis. Proteomics. 2011;11:1664–1683. doi: 10.1002/pmic.201000652. PubMed DOI

Shi Y.F., Wang D.L., Wang C., Culler A.H., Kreiser M.A., Suresh J., Cohen J.D., Pan J., Baker B., Liu J.Z. Loss of GSNOR1 Function Leads to Compromised Auxin Signaling and Polar Auxin Transport. Mol. Plant. 2015;8:1350–1365. doi: 10.1016/j.molp.2015.04.008. PubMed DOI

Liu H.Y., Yu X., Cui D.Y., Sun M.H., Sun W.N., Tang Z.C. The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res. 2007;17:638–649. doi: 10.1038/cr.2007.34. PubMed DOI

Zandonadi D.B., Santos M.P., Dobbss L.B., Olivares F.L., Canellas L.P., Binzel M.L., Okorokova-Facanha A.L., Facanha A.R. Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta. 2010;231:1026–1035. doi: 10.1007/s00425-010-1106-0. PubMed DOI

Kopyra M., Gwozdz E.A. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol. Biochem. 2003;41:1011–1017. doi: 10.1016/j.plaphy.2003.09.003. DOI

Kong J., Dong Y., Song Y., Bai X., Tian X., Xu L., Liu S., He Z. Role of exogenous nitric oxide in alleviating iron deficiency stress of peanut seedlings (Arachis hypogaea L.) J. Plant Growth Regul. 2016;35:31–43. doi: 10.1007/s00344-015-9504-y. DOI

Piterková J., Luhová L., Hofman J., Turečková V., Novák O., Petřivalský M., Fellner M. Nitric oxide is involved in light-specific responses of tomato during germination under normal and osmotic stress conditions. Ann. Bot. 2012;110:767–776. doi: 10.1093/aob/mcs141. PubMed DOI PMC

Goldstein S., Russo A., Samuni A. Reactions of PTIO and carboxy-PTIO with ·NO, ·NO2, and O2−. J. Biol. Chem. 2003;278:50949–50955. doi: 10.1074/jbc.M308317200. PubMed DOI

Foreman J., Demidchik V., Bothwell J.H., Mylona P. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442–446. doi: 10.1038/nature01485. PubMed DOI

Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistence. Nature. 1998;394:585–588. doi: 10.1038/29087. PubMed DOI

Wendehenne D., Durner J., Klessig D.F. Nitric oxide: A new player in plant signalling and defence responses. Curr. Opin. Plant Biol. 2004;7:449–455. doi: 10.1016/j.pbi.2004.04.002. PubMed DOI

Tada Y., Mori T., Shinogi T., Yao N., Takahashi S., Betsuyaku S., Mayama S. Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oat. Mol. Plant Microbe Inter. 2004;17:245–253. doi: 10.1094/MPMI.2004.17.3.245. PubMed DOI

Chaki M., Fernández-Ocana A.M., Valderrama R., Carreras A., Esteban F.J., Luque F., Gómez-Rodríguez M.V., Begara-Morales J.C., Corpas F.J., Barroso J.B. 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

Delledonne M., Zeier J., Marocco A., Lamb C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA. 2001;98:13454–13459. doi: 10.1073/pnas.231178298. PubMed DOI PMC

Farnese F.S., Menezes-Silva P.E., Gusman G.S., Oliveira J.A. When bad guys become good ones: The key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front. Plant Sci. 2016 doi: 10.3389/fpls.2016.00471. PubMed DOI PMC

Marino D., Dunand C., Puppo A., Pauly N. A burst of plant NADPH oxidases. Trend. Plant Sci. 2012;17:9–15. doi: 10.1016/j.tplants.2011.10.001. PubMed DOI

Clark D., Durner J., Navarre D.A., Klessig D.F. 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

Keyster M., Klein A., Egbich I., Jacobs A., Ludidi N. Nitric oxide increases the enzymatic activity of three ascorbate peroxidase isoforms in soybean root nodules. Plant Signal. Behav. 2011;6:956–961. doi: 10.4161/psb.6.7.14879. PubMed DOI PMC

Bai X., Yang L., Yang Y., Ahmad P., Yang Y., Hu X. Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J. Proteom. Res. 2012;10:4349–4364. doi: 10.1021/pr200333f. PubMed DOI

Martínez-Ruiz A., Lamas S. Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: Convergences and divergences. Cardiovasc. Res. 2007;75:220–228. doi: 10.1016/j.cardiores.2007.03.016. PubMed DOI

Kitajima S. Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-Cys peroxiredoxin. Photochem. Photobiol. 2008;84:1404–1409. doi: 10.1111/j.1751-1097.2008.00452.x. PubMed DOI

Gould K.S., Klinguer A., Pugin A., Wendehenne D. Nitric oxide production in tobacco leaf cells: A generalized stress response? Plant Cell Environ. 2003;26:1851–1862. doi: 10.1046/j.1365-3040.2003.01101.x. DOI

Corpas F.J., Hayashi M., Mano S., Nishimura M., Barroso J.B. Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol. 2009;151:2083–2094. doi: 10.1104/pp.109.146100. PubMed DOI PMC

David A., Yadav S., Bhatla S.C. Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol. Plant. 2010;140:342–354. doi: 10.1111/j.1399-3054.2010.01408.x. PubMed DOI

Valderrama R., Corpas F.J., Carreras A., Fernández-Ocaña A., Chaki M., Luque F., Gómez-Rodríguez M.V., Colmenero-Varea P., Del Río L.A., Barroso J.B. Nitrosative stress in plants. FEBS Lett. 2007;581:453–461. doi: 10.1016/j.febslet.2007.01.006. PubMed DOI

Tanou G., Job C., Rajjou L., Arc E., Belghazi M., Diamantidis G., Job D. 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

Tanou G., Filippou P., Belghazi M., Job D., Diamantidis G., Fotopoulos V. 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

Bandeoglu E., Eyidogan F., Yücel M., Öktem H.A. Antioxidant responses of shoots and roots of lentil to NaCl-salinity stress. Plant Growth Regul. 2004;42:69–77. doi: 10.1023/B:GROW.0000014891.35427.7b. DOI

Gueta-Dahan Y., Yaniv Z., Zilinskas B.A., Ben-Hayyim G. Salt and oxidative stress: Similar and specific responses and their relation to salt tolerance in citrus. Planta. 1997;203:460–469. doi: 10.1007/s004250050215. PubMed DOI

Molina A., Bueno P., Marín M.C., Rodríguez-Rosales M.P., Belver A., Venema K., Donaire J.P. Involvement of endogenous salicylic acid content, lipoxygenase and antioxidant enzyme activities in the response of tomato cell suspension cultures to NaCl. New Phytol. 2002;156:409–415. doi: 10.1046/j.1469-8137.2002.00527.x. PubMed DOI

Manai J., Gouiab H., Corpas F.J. Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J. Plant Physiol. 2014;171:1028–1035. doi: 10.1016/j.jplph.2014.03.012. PubMed DOI

Kopyra M., Stachoń-Wilk M., Gwozdz E.A. Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol. Plant. 2006;28:525–536. doi: 10.1007/s11738-006-0048-4. DOI

Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Deckert J., Rucińska-Sobkowiak R., Gzyl J., Pawlak-Sprada S., Gwóźdź E.A. Nitric oxide implication in cadmium-induced programmed cell death in roots and signaling response of yellow lupine plants. Plant Physiol. Biochem. 2012;58:124–134. doi: 10.1016/j.plaphy.2012.06.018. PubMed DOI

Piterková J., Luhová L., Navrátilová B., Sedlářová M., Petřivalský M. Early and long-term responses of cucumber cells to high cadmium concentration are modulated by nitric oxide and reactive oxygen species. Acta Physiol. Plant. 2015 doi: 10.1007/s11738-014-1756-9. DOI

Singh H.P., Batish D.R., Kaur G., Arora K., Kohli R.K. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ. Exp. Bot. 2008;63:158–167. doi: 10.1016/j.envexpbot.2007.12.005. DOI

Singh H.P., Kaur S., Batish D.R., Sharma V.P., Sharma N., Kohli R.K. Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice) Nitric Oxide. 2009;20:289–297. doi: 10.1016/j.niox.2009.02.004. PubMed DOI

Farnese F.S., Oliveira J.A., Paiva E., Menezes-Silva P.E., da Silva A.A., Campos F.V., Ribeiro C. The Involvement of Nitric Oxide in Integration of Plant Physiological and Ultrastructural Adjustments in Response to Arsenic. Front. Plant Sci. 2017 doi: 10.3389/fpls.2017.00516. PubMed DOI PMC

Ismail G.S.M. Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol. Plant. 2012;34:1303–1311. doi: 10.1007/s11738-012-0927-9. DOI

Piterková J., Petřivalský M., Luhová L., Mieslerová B., Sedlářová M., Lebeda A. 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

Ortega-Galisteo A.P., Rodríguez-Serrano M., Pazmiño D.M., Gupta D.K., Sandalio L.M., Romero-Puertas M.C. S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: Changes under abiotic stress. J. Exp. Bot. 2012;63:2089–2103. doi: 10.1093/jxb/err414. PubMed DOI PMC

Barroso J.B., Corpas F.J., Carreras A., Rodríguez-Serrano M., Esteban F.J., Fernández-Ocaña A., Chaki M., Romero-Puertas M.C., Valderrama R., Sandalio L.M., et al. Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J. Exp. Bot. 2006;57:1785–1793. doi: 10.1093/jxb/erj175. PubMed DOI

Leterrier M., Airaki M., Palma J.M., Chaki M., Barroso J.B., Corpas F.J. Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ. Pollut. 2012;166:136–143. doi: 10.1016/j.envpol.2012.03.012. PubMed DOI

Rodríguez-Serrano M.A., Romero-Puertas M.C., Zabalza A.N.A., Corpas F.J., Gómez M., Del Río L.A., Sandalio L.M. Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ. 2006;29:1532–1544. doi: 10.1111/j.1365-3040.2006.01531.x. PubMed DOI

Corpas F.J., Del Río L.A., Barroso J.B. Post-translational modifications mediated by reactive nitrogen species: Nitrosative stress responses or components of signal transduction pathways? Plant Signal. Behav. 2008;3:301–303. doi: 10.4161/psb.3.5.5277. PubMed DOI PMC

Protein S-nitrosation differentially modulates tomato responses to infection by hemi-biotrophic oomycetes of Phytophthora spp