Nitration of diverse biomolecules, including proteins, lipids and nucleic acid, by reactive nitrogen species represents one of the key mechanisms mediating nitric oxide (NO) biological activity across all types of organisms. 8-nitroguanosine 3'5'-cyclic monophosphate (8-nitro-cGMP) has been described as a unique electrophilic intermediate involved in intracellular redox signaling. In animal cells, 8-nitro-cGMP is formed from guanosine-5'-triphosphate by a combined action of reactive nitrogen (RNS) and oxygen species (ROS) and guanylate cyclase. As demonstrated originally in animal models, 8-nitro-cGMP shows certain biological activities closely resembling its analog cGMP; however, its regulatory functions are mediated mainly by its electrophilic properties and chemical interactions with protein thiols resulting in a novel protein post-translational modification termed S-guanylation. In Arabidopsis thaliana, 8-nitro-cGMP was reported to mediate NO-dependent signaling pathways controlling abscisic acid (ABA)-induced stomatal closure, however, its derivative 8-mercapto-cGMP (8-SH-cGMP) was later shown as the active component of hydrogen sulfide (H2S)-mediated guard cell signaling. Here we present a survey of current knowledge on biosynthesis, metabolism and biological activities of nitrated nucleotides with special attention to described and proposed functions of 8-nitro-cGMP and its metabolites in plant physiology and stress responses.

Department of Biochemistry Faculty of Science Palacký University Olomouc Czechia

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Abada A., Elazar Z. (2014). Getting ready for building: signaling and autophagosome biogenesis. EMBO Rep. 15 839–852. 10.15252/embr.201439076 PubMed DOI PMC

Agurla S., Gayatri G., Raghavendra A. S. (2014). Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens. Nitric Oxide 43 89–96. 10.1016/j.niox.2014.07.004 PubMed DOI

Agurla S., Raghavendra A. S. (2016). Convergence and divergence of signaling events in guard cells during stomatal closure by plant hormones or microbial elicitors. Front. Plant Sci. 7:1332. 10.3389/fpls.2016.01332 PubMed DOI PMC

Ahmed K. A., Sawa T., Ihara H., Kasamatsu S., Yoshitake J., Rahaman M. M., et al. (2012). Regulation by mitochondrial superoxide and NADPH oxidase of cellular formation of nitrated cyclic GMP: potential implications for ROS signalling. Biochem. J. 441 719–730. 10.1042/BJ20111130 PubMed DOI

Ahmed K. A., Zhang T., Ono K., Tsutsuki H., Ida T., Akashi S., et al. (2017). Synthesis and characterization of 8-nitroguanosine 3′,5′-Cyclic monophosphorothioate Rp-Isomer as a potent inhibitor of protein kinase G1α. Biol. Pharm. Bull. 40 365–374. 10.1248/bpb.b16-00880 PubMed DOI

Akaike T., Ida T., Wei F. Y., Nishida M., Kumagai Y., Alam M. M., et al. (2017). Cysteinyl-tRNA synthetase governs cysteine polysulfidation and mitochondrial bioenergetics. Nat. Comm. 8:1177. 10.1038/s41467-017-01311-y PubMed DOI PMC

Akaike T., Nishida M., Fujii S. (2013). Regulation of redox signalling by an electrophilic cyclic nucleotide. J. Biochem. 153 131–138. 10.1093/jb/mvs145 PubMed DOI

Akaike T., Okamoto S., Sawa T., Yoshitake J., Tamura F., Ichimori K., et al. (2003). 8-Nitroguanosine formation in viral pneumonia and its implication for pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 100 685–690. 10.1073/pnas.0235623100 PubMed DOI PMC

Akashi S., Ahmed K. A., Sawa T., Ono K., Tsutsuki H., Burgoyne J. R., et al. (2016). Persistent activation of cGMP-Dependent protein kinase by a nitrated cyclic nucleotide via site specific protein S-Guanylation. Biochemistry 55 751–761. 10.1021/acs.biochem.5b00774 PubMed DOI

Arasimowicz-Jelonek M., Floryszak-Wieczorek J. (2019). A physiological perspective on targets of nitration in NO-based signaling networks in plants. J. Exp. Bot. 70 4379–4389. 10.1093/jxb/erz300 PubMed DOI

Astier J., Gross I., Durner J. (2018). Nitric oxide production in plants: an update. J. Exp. Bot. 69 3401–3411. 10.1093/jxb/erx420 PubMed DOI

Balmant K. M., Zhang T., Chen S. (2016). Protein phosphorylation and redox modification in stomatal guard cells. Front. Physiol. 7:26. 10.3389/fphys.2016.00026 PubMed DOI PMC

Begara-Morales J. C., Sánchez-Calvo B., Chaki M., Valderrama R., Mata-Pérez C., Padilla M. N., et al. (2016). Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front. Plant Sci. 7:152. 10.3389/fpls.2016.00152 PubMed DOI PMC

Corpas F. J., Barroso J. B. (2015). Nitric oxide from a “green” perspective. Nitric Oxide 45 15–19. 10.1016/j.niox.2015.01.007 PubMed DOI

Cosker F., Lima F. J., Lahlou S., Magalhaes P. J. (2014). Cytoprotective effect of 1-nitro-2-phenylethane in mice pancreatic acinar cells subjected to taurocholate: putative role of guanylyl cyclase-derived 8-nitro-cyclic-GMP. Biochem. Pharmacol. 15 191–201. 10.1016/j.bcp.2014.07.030 PubMed DOI

Daszkowska-Golec A., Szarejko I. (2013). Open or close the gate - stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci. 4:138. 10.3389/fpls.2013.00138 PubMed DOI PMC

Dmitrieva S. A., Ponomareva A. A., Gurjanov O. P., Mazina A. B., Andrianov V. V., Iyudin V. S., et al. (2018). Spermine induces autophagy in plants: possible role of no and reactive oxygen species. Dokl. Biochem. Biophys. 483 341–343. 10.1134/S1607672918060121 PubMed DOI

Donaldson L., Meier S., Gehring C. (2016). The Arabidopsis cyclic nucleotide interactome. Cell Commun. Signal. 14:10. 10.1186/s12964-016-0133-2 PubMed DOI PMC

Dubovskaya L. V., Bakakina Y. S., Kolesneva E. V., Sodel D. L., Mcainsh M. R., Hetherington A. M., et al. (2011). cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytol. 191 57–69. 10.1111/j.1469-8137.2011.03661.x PubMed DOI

Farnese F. S., Menezes-Silva P. E., Gusman G. S., Oliveira J. A. (2016). 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. 7:471. 10.3389/fpls.2016.00471 PubMed DOI PMC

Fujii S., Sawa T., Ihara H., Tong K. I., Ida T., Okamoto T., et al. (2010). The critical role of nitric oxide signaling, via protein S-guanylation and nitrated cyclic GMP, in the antioxidant adaptive response. J. Biol. Chem. 285 23970–23984. 10.1074/jbc.M110.145441 PubMed DOI PMC

Fukuto J. M., Ignarro L. J., Nagy P., Wink D. A., Kevil C. G., Feelisch M., et al. (2018). Biological hydropersulfides and related polysulfides - a new concept and perspective in redox biology. FEBS Lett. 592 2140–2152. 10.1002/1873-3468.13090 PubMed DOI PMC

Gayatri G., Agurla S., Raghavendra A. S. (2013). Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front. Plant Sci. 4:425. 10.3389/fpls.2013.00425 PubMed DOI PMC

Gehring C., Turek I. S. (2017). Cyclic nucleotide monophosphates and their cyclases in plant signaling. Front. Plant Sci. 8:1704. 10.3389/fpls.2017.01704 PubMed DOI PMC

Gotor C., García I., Crespo J. L., Romero L. C. (2013). Sulfide as a signaling molecule in autophagy. Autophagy 9 609–611. 10.4161/auto.23460 PubMed DOI PMC

Gross I., Durner J. (2016). In search of enzymes with a role in 3′, 5′-cyclic guanosine monophosphate metabolism in plants. Front. Plant Sci. 7:576. 10.3389/fpls.2016.00576 PubMed DOI PMC

Guoguo S., Akaike T., Tao J., Qi C., Nong Z., Hui L. (2012). HGF-mediated inhibition of oxidative stress by 8-nitro-cGMP in high glucose-treated rat mesangial cells. Free Radic. Res. 46 1238–1248. 10.3109/10715762.2012.701292 PubMed DOI

Hofius D., Li L., Hafrén A., Coll N. S. (2017). Autophagy as an emerging arena for plant-pathogen interactions. Curr. Opin. Plant Biol. 38 117–123. 10.1016/j.pbi.2017.04.017 PubMed DOI

Honda K., Yamada N., Yoshida R., Ihara H., Sawa T., Akaike T., et al. (2015). 8-Mercapto-cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis. Plant Cell Physiol. 56 1481–1489. 10.1093/pcp/pcv069 PubMed DOI

Ida T., Sawa T., Ihara H., Tsuchiya Y., Watanabe Y., Kumagai Y., et al. (2014). Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc. Natl. Acad. Sci. U.S.A. 111 7606–7611. 10.1073/pnas.1321232111 PubMed DOI PMC

Ihara H., Kasamatsu S., Kitamura A., Nishimura A., Tsutsuki H., Ida T., et al. (2017). Exposure to electrophiles impairs reactive persulfide-dependent redox signaling in neuronal cells. Chem. Res. Toxicol. 30 1673–1684. 10.1021/acs.chemrestox.7b00120 PubMed DOI

Ihara H., Sawa T., Nakabeppu Y., Akaike T. (2011). Nucleotides function as endogenous chemical sensors for oxidative stress signaling. J. Clin. Biochem.Nutr. 48 33–39. 10.3164/jcbn.11-003FR PubMed DOI PMC

Isner J.-C., Olteanu V.-A., Hetherington A. J., Coupel-Ledru A., Sun P., Pridgeon A. J., et al. (2019). Short- and long-term effects of UVA on Arabidopsis are mediated by a novel cGMP phosphodiesterase. Curr. Biol. 29 2580–2585. 10.1016/j.cub.2019.06.071 PubMed DOI PMC

Ito C., Saito Y., Nozawa T., Fujii S., Sawa T., Inoue H., et al. (2013). Endogenous nitrated nucleotide is a key mediator of autophagy and innate defense against bacteria. Mol. Cell 52 794–804. 10.1016/j.molcel.2013.10.024 PubMed DOI

Joudoi T., Shichiri Y., Kamizono N., Akaike T., Sawa T., Yoshitake J., et al. (2013). Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell 25 558–571. 10.1105/tpc.112.105049 PubMed DOI PMC

Kasamatsu S., Nishimura A., Morita M., Matsunaga T., Abdul Hamid H., Akaike T. (2016). Redox signaling regulated by cysteine persulfide and protein polysulfidation. Molecules 121:E1721. 10.3390/molecules21121721 PubMed DOI PMC

Kasamatsu S., Watanabe Y., Sawa T., Akaike T., Ihara H. (2014). Redox signal regulation via nNOS phosphorylation at Ser847 in PC12 cells and rat cerebellar granule neurons. Biochem. J. 459 251–263. 10.1042/BJ20131262 PubMed DOI

Khan S., Fujii S., Matsunaga T., Nishimura A., Ono K., Ida T., et al. (2018). Reactive persulfides from Salmonella typhimurium downregulate autophagy-mediated innate immunity in macrophages by inhibiting electrophilic signaling. Cell Chem. Biol 25 1403.e4–1413.e4. 10.1016/j.chembiol.2018.08.007 PubMed DOI

Kunieda K., Tsutsuki H., Ida T., Kishimoto Y., Kasamatsu S., Sawa T., et al. (2015). 8-Nitro-cGMP enhances SNARE complex formation through S-guanylation of Cys90 in SNAP25. ACS Chem. Neurosci. 6 1715–1725. 10.1021/acschemneuro.5b00196 PubMed DOI

Kurauchi Y., Hisatsune A., Isohama Y., Sawa T., Akaike T., Katsuki H. (2013). Nitric oxide/soluble guanylyl cyclase signaling mediates depolarization-induced protection of rat mesencephalic dopaminergic neurons from MPP+ cytotoxicity. Neurosci. 231 206–215. 10.1016/j.neuroscience.2012.11.044 PubMed DOI

Laureano-Marín A. M., Moreno I., Romero L. C., Gotor C. (2016). Negative regulation of autophagy by sulfide is independent of reactive oxygen species. Plant Physiol. 171 1378–1391. 10.1104/pp.16.00110 PubMed DOI PMC

Leary A. Y., Savage Z., Tumtas Y., Bozkurt T. O. (2019). Contrasting and emerging roles of autophagy in plant immunity. Curr. Opin. Plant. Biol. 52 46–53. 10.1016/j.pbi.2019.07.002 PubMed DOI

Lee J. M., Niles J. C., Wishnok J. S., Tannenbaum S. R. (2002). Peroxynitritexreacts with 8-nitropurines to yield 8-oxopurines. Chem. Res. Toxicol. 15 7–14. 10.1021/tx010093d PubMed DOI

Lemtiri-Chlieh F., Thomas L., Marondedze C., Irving H., Gehring C. (2011). “Cyclic nucleotides and nucleotide cyclases in plant stress responses, abiotic stress Response,” in Plants - Physiological, Biochemical and Genetic Perspectives, ed. Shanker A. (Venkateswarlu: IntechOpen; ).

Ma N., Adachi Y., Hiraku Y., Horiki N., Horiike S., Imoto I., et al. (2004). Accumulation of 8-nitroguanine in human gastric epithelium induced by Helicobacter pylori infection. Biochem. Biophys. Res. Commun. 319 506–510. 10.1016/j.bbrc.2004.04.193 PubMed DOI

Masuda M., Nishino H., Ohshima H. (2002). Formation of 8-nitroguanosine in cellular RNA as a biomarker of exposure to reactive nitrogen species. Chem. Biol. Interact. 139 187–197. 10.1016/s0009-2797(01)00299-x PubMed DOI

Mizushima N., Komatsu M. (2011). Autophagy: renovation of cells and tissues. Cell 147 728–741. 10.1016/j.cell.2011.10.026 PubMed DOI

Nakagawa I., Amano A., Mizushima N., Yamamoto A., Yamaguchi H., Kamimoto T., et al. (2004). Autophagy defends cells against invading group a Streptococcus. Science 306 1037–1040. 10.1126/science.1103966 PubMed DOI

Niles J. C., Wishnok J. S., Tannenbaum S. R. (2001). A novel nitroimidazole compound formed during the reaction of peroxynitrite with 2’,3′,5′-tri-O-acetyl-guanosine. J. Am. Chem. Soc. 123 12147–12151. 10.1021/ja004296k PubMed DOI

Nishida M., Kumagai Y., Ihara H., Fujii S., Motohashi H., Akaike T. (2016). Redox signaling regulated by electrophiles and reactive sulfur species. J. Clin. Biochem. Nutr. 58 91–98. 10.3164/jcbn.15-111 PubMed DOI PMC

Nishida M., Sawa T., Kitajima N., Ono K., Inoue H., Ihara H., et al. (2012). Hydrogen sulfide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 8 714–724. 10.1038/nchembio.1018 PubMed DOI PMC

Ohshima H., Sawa T., Akaike T. (2006). 8-nitroguanine, a product of nitrative DNA damage caused by reactive nitrogen species: formation, occurrence, and implications in inflammation and carcinogenesis. Antioxid. Redox Signal. 8 1033–1045. 10.1089/ars.2006.8.1033 PubMed DOI

Pinlaor S., Yongvanit P., Hiraku Y., Ma N., Semba R., Oikawa S., et al. (2003). 8-Nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochem. Biophys. Res. Commun. 309 567–571. 10.1016/j.bbrc.2003.08.039 PubMed DOI

Rahaman M. M., Sawa T., Ahtesham A. K., Khan S., Inoue H., Irie A., et al. (2014). S-guanylation proteomics for redox-based mitochondrial signaling. Antioxid. Redox. Signal. 20 295–307. 10.1089/ars.2012.4606 PubMed DOI PMC

Rawet-Slobodkin M., Elazar Z. (2013). 8-nitro-cGMP-a new player in antibacterial autophagy. Mol. Cell 52 767–768. 10.1016/j.molcel.2013.12.006 PubMed DOI

Sadhu A., Moriyasu Y., Acharya K., Bandyopadhyay M. (2019). Nitric oxide and ROS mediate autophagy and regulate Alternaria alternata toxin-induced cell death in tobacco BY-2 cells. Sci. Rep. 9:8973. 10.1038/s41598-019-45470-y PubMed DOI PMC

Saito Y., Sawa T., Yoshitake J., Ito C., Fujii S., Akaike T., et al. (2012). Nitric oxide promotes recycling of 8-nitro-cGMP, a cytoprotective mediator, into intact cGMP in cells. Mol. Biosyst. 8 2909–2915. 10.1039/c2mb25189b PubMed DOI

Samanta A., Thunemann M., Feil R., Stafforst T. (2014). Upon the photostability of 8-nitro-cGMP and its caging as a 7-dimethylaminocoumarinyl ester. Chem. Commun. 50 7120–7123. 10.1039/c4cc02828g PubMed DOI

Sawa T., Akaike T., Ichimori K., Akuta T., Kaneko K., Nakayama H., et al. (2003). Superoxide generation mediated by 8-nitroguanosine, a highly redox-active nucleic acid derivative. Biochem. Biophys. Res. Commun. 311 300–306. 10.1016/j.bbrc.2003.10.003 PubMed DOI

Sawa T., Arimoto H., Akaike T. (2010). Regulation of redox signaling involving chemical conjugation of protein thiols by nitric oxide and electrophiles. Bioconjug. Chem. 21 1121–1129. 10.1021/bc900396u PubMed DOI

Sawa T., Ihara H., Ida T., Fujii S., Nishida M., Akaike T. (2013). Formation, signaling functions, and metabolisms of nitrated cyclic nucleotide. Nitric Oxide 34 10–18. 10.1016/j.niox.2013.04.004 PubMed DOI

Sawa T., Tatemichi T., Akaike T., Barbina A., Ohshima H. (2006). Analysis of urinary 8-nitroguanine, a marker of nitrative nucleic acid damage, by high-performance liquid chromatography-electrochemical detection coupled with immunoaffinity purification: association with cigarette smoking. Free Radic. Biol. Med. 40 711–720. 10.1016/j.freeradbiomed.2005.09.035 PubMed DOI

Sawa T., Zaki M. H., Okamoto T., Akuta T., Tokutomi Y., Kim-Mitsuyama S., et al. (2007). Protein S-guanylation by the biological signal 8-nitroguanosine 3′,5′-cyclic monophosphate. Nat Chem. Biol. 3 727–735. 10.1038/nchembio.2007.33 PubMed DOI

Scuffi D., Lamattina L., García-Mata C. (2016). Gasotransmitters and stomatal closure: is there redundancy. Concerted Action, or Both? Front. Plant Sci. 7 277. 10.3389/fpls.2016.00277 PubMed DOI PMC

Shen Q., Zhan X., Yang P., Li J., Chen J., Tang B. (2019). Dual activities of plant cGMP-dependent protein kinase and its roles in gibberellin signaling and salt stress. Plant Cell 31 3073–3091. 10.1105/tpc.19.00510 PubMed DOI PMC

Sodum R. S., Fiala E. S. (2001). Analysis of peroxynitrite reactions with guanine, xanthine, and adenine nucleosides by high-pressure liquid chromatography with electrochemical detection: c8-nitration and –oxidation. Chem. Res. Toxicol. 14 438–450. 10.1021/tx000189s PubMed DOI

Spencer J. P., Wong J., Jenner A., Aruoma O. I., Cross C. E., Halliwell B. (1996). Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3-morpholinosydnonimine. Chem. Res. Toxicol. 9 1152–1158. 10.1021/tx960084i PubMed DOI

Sun L. R., Yue C. M., Hao F. S. (2019). Update on roles of nitric oxide in regulating stomatal closure. Plant Signal. Behav. 14:e1649569. 10.1080/15592324.2019.1649569 PubMed DOI PMC

Świeżawska B., Duszyn M., Jaworski K., Szmidt-Jaworska A. (2018). Downstream targets of cyclic nucleotides in plants. Front. Plant Sci. 9:1428. 10.3389/fpls.2018.01428 PubMed DOI PMC

Taguchi K., Fujikawa N., Komatsu M., Ishii T., Unno M., Akaike T., et al. (2012). Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc. Natl. Acad. Sci. U.S.A. 109 13561–13566. 10.1073/pnas.1121572109 PubMed DOI PMC

Takahashi D., Moriyama J., Nakamura T., Miki E., Takahashi E., Sato A., et al. (2019). AUTACs: cargo-specific degraders using selective autophagy. Mol Cell 76 797.e10–810.e10. 10.1016/j.molcel.2019.09.009 PubMed DOI

Terasaki Y., Akuta T., Terasaki M., Sawa T., Mori T., Okamoto T., et al. (2006). Guanine nitration in idiopathic pulmonary fibrosis and its implications for carcinogenesis. Am. J. Respir. Crit. Care Med. 174 665–673. 10.1164/rccm.200510-1580OC PubMed DOI

Terzič V., Padovani D., Balland V., Artaud I., Galardon E. (2014). Electrophilic sulfhydration of 8-nitro-cGMP involves sulfane sulfur. Org. Biomol. Chem. 12 5360–5364. 10.1039/c4ob00868e PubMed DOI

Umbreen S., Lubega J., Cui B., Pan Q., Jiang J., Loake G. J. (2018). Specificity in nitric oxide signalling. J. Exp. Bot. 69 3439–3448. 10.1093/jxb/ery184 PubMed DOI

Wang Y. F., Munemasa S., Nishimura N., Ren H. M., Robert N., Han M., et al. (2013). Identification of Cyclic GMP-activated nonselective Ca2+ -permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiol. 163 578–590. 10.1104/pp.113.225045 PubMed DOI PMC

Wheeler J. I., Freihat L., Irving H. R. (2013). A cyclic nucleotide sensitive promoter reporter system suitable for bacteria and plant cells. BMC Biotechnol. 13:97. 10.1186/1472-6750-13-97 PubMed DOI PMC

Ye W., Murata Y. (2016). Microbe associated molecular pattern signaling in guard cells. Front. Plant Sci. 7:583. 10.3389/fpls.2016.00583 PubMed DOI PMC

Yermilov V., Rubio J., Becchi M., Friesen M. D., Pignatelli B., Ohshima H. (1995a). Formation of 8-nitroguanine by the reaction of guanine with peroxynitrite in vitro. Carcinogenesis 16 2045–2050. 10.1093/carcin/16.9.2045 PubMed DOI

Yermilov V., Rubio J., Ohshima H. (1995b). Formation of 8-nitroguanine in DNA treated with peroxynitrite in vitro and its rapid removal from DNA by depurination. FEBS Lett. 376 207–210. 10.1016/0014-5793(95)01281-6 PubMed DOI

Yoshitake J., Akaike T., Akuta T., Tamura F., Ogura T., Esumi H., et al. (2004). Nitric oxide as an endogenous mutagen for sendai virus without antiviral activity. J. Virol. 78, 8709–8719. 10.1128/JVI.78.16.8709-8719.2004 PubMed DOI PMC

Yoshitake J., Soeda Y., Ida T., Sumioka A., Yoshikawa M., Matsushita K., et al. (2016). Modification of Tau by 8-Nitroguanosine 3′,5′-Cyclic Monophosphate (8-Nitro-cGMP): effects of nitric oxide-linked chemical modification on tau aggregation. J. Biol. Chem. 291 22714–22720. 10.1074/jbc.M116.734350 PubMed DOI PMC

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

Zaki M. H., Fujii S., Okamoto T., Islam S., Khan S., Ahmed K. A., et al. (2009). Cytoprotective function of heme oxygenase 1 Induced by a nitrated cyclic nucleotide formed during murine salmonellosis. J. Immunol. 182 3746–3756. 10.4049/jimmunol.0803363 PubMed DOI

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