Regulating the regulator: nitric oxide control of post-translational modifications

. 2020 Sep ; 227 (5) : 1319-1325. [epub] 20200523

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid32339293

Grantová podpora
BB/H000984/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/DO11809/1 Biotechnology and Biological Sciences Research Council - United Kingdom

Nitric oxide (NO) is perfectly suited for the role of a redox signalling molecule. A key route for NO bioactivity occurs via protein S-nitrosation, and involves the addition of a NO moiety to a protein cysteine (Cys) thiol (-SH) to form an S-nitrosothiol (SNO). This process is thought to underpin a myriad of cellular processes in plants that are linked to development, environmental responses and immune function. Here we collate emerging evidence showing that NO bioactivity regulates a growing number of diverse post-translational modifications including SUMOylation, phosphorylation, persulfidation and acetylation. We provide examples of how NO orchestrates these processes to mediate plant adaptation to a variety of cellular cues.

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Ahmad A, Cao X. 2012. Plant PRMTs Broaden the scope of arginine methylation. Journal of Genetics and Genomics 39: 195-208.

Aroca Á, Serna A, Gotor C, Romero LC. 2015. S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiology 168: 334 LP-342.

Arruebarrena A, Palma D, Di LM, Salvatore SR, Martín J, Ambrosio D, García-mata C, Schopfer FJ, Laxalt AM. 2020. Nitro-oleic acid triggers ROS production via NADPH oxidase activation in plants: a pharmacological approach. Journal of Plant Physiology 246-247: 153128.

Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Research 21: 381-395.

Begara-Morales JC, Sánchez-Calvo Beatriz, 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.

Begara-Morales JC, Sánchez-Calvo Beatriz, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB. 2014. Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. Journal of Experimental Botany 65: 527-538.

Besson-Bard A, Courtois C, Gauthier A, Dahan J, Dobrowolska G, Jeandroz S, Pugin A, Wendehenne D. 2008a. Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Molecular Plant 1: 218-228.

Besson-Bard A, Pugin A, Wendehenne D. 2008b. New insights into nitric oxide signaling in plants. Annual Review of Plant Biology 59: 21-39.

Blanc RS, Richard S. 2017. Arginine methylation: the coming of age. Molecular Cell 65: 8-24.

Bossis G, Melchior F. 2006. SUMO: regulating the regulator. Cell Division 1: 13.

van den Burg HA, Kini RK, Schuurink RC, Takken FLW. 2010. Arabidopsis small ubiquitin-like modifier Paralogs have distinct functions in development and defense. Plant Cell 22: doi: 10.1105/tpc.109.070961

Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J et al. 2009. The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Research 19: 1377-1387.

Corpas FJ, González-Gordo S, Cañas A, Palma JM. 2019. Nitric oxide and hydrogen sulfide in plants: which comes first? Journal of Experimental Botany 70: 4391-4404.

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

Del Castello F, Nejamkin A, Cassia R, Correa-Aragunde N, Fernández B, Foresi N, Lombardo C, Ramirez L, Lamattina L. 2019. The era of nitric oxide in plant biology: twenty years tying up loose ends. Nitric Oxide 85: 17-27.

Dissmeyer N, Rivas S, Graciet E. 2018. Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway. New Phytologist 218: 929-935.

Feechan A, Kwon E, Yun B-W, Wang Y, Pallas JA, Loake GJ. 2005. A central role for S-nitrosothiols in plant disease resistance. Proceedings of the National Academy of Sciences, USA 102: 8054-8059.

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

Frederickson Matika DE, Loake GJ. 2014. Redox regulation in plant immune function. Antioxidants & Redox Signaling 21: 1373-1388.

Frungillo L, Spoel SH. 2017. Preview modulating the modulator: regulation of protein methylation by nitric oxide. Molecular Cell 67: 535-537.

Gibbs DJ, Bacardit J, Bachmair A, Holdsworth MJ. 2014. The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends in Cell Biology 24: 603-611.

Gibbs DJ, Bailey M, Tedds HM, Holdsworth MJ. 2016. From start to finish: amino-terminal protein modifications as degradation signals in plants. New Phytologist 211: 1188-1194.

Gupta KJ, Stoimenova M, Kaiser WM. 2005. In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. Journal of Experimental Botany 56: 2601-2609.

Hancock JT. 2019. Considerations of the importance of redox state for reactive nitrogen species action. Journal of Experimental Botany 70: 4323-4331.

Hartman S, Liu Z, van Veen H, Vicente J, Reinen E, Martopawiro S, Zhang H, van Dongen N, Bosman F, Bassel GW et al. 2019. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nature Communications 10: 4020.

Hong S, Song H-R, Lutz K, Kerstetter RA, Michael TP, McClung CR. 2010. Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 107: 21211-21216.

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.

Huang J, Willems P, Wei B, Tian C, Ferreira RB, Bodra N, Martínez Gache SA, Wahni K, Liu K, Vertommen D et al. 2019. Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites. Proceedings of the National Academy of Sciences, USA 116: 21256-21261.

Hussain A, Mun B, Imran QM, Lee S, Adamu TA, Kim K, Yun B-W. 2016. Nitric oxide mediated transcriptome profiling reveals activation of multiple regulatory pathways in Arabidopsis thaliana. Frontiers in Plant Science 7: 975.

Kelley EE, Batthyany CI, Hundley NJ, Woodcock SR, Bonacci G, Del Rio JM, Schopfer FJ, Lancaster JR, Freeman BA, Tarpey MM. 2008. Nitro-oleic acid, a novel and irreversible inhibitor of xanthine oxidoreductase. Journal of Biologcal Chemistry 283: 36176-36184.

Kolbert Z, Feigl G. 2017. Cross-talk of reactive oxygen species and nitric oxide in various processes of plant development. In: Singh VP, Singh S, Tripathi DK, Prasad SM, Chauhan D, eds. Reactive oxygen species in plants. New Jersey, USA: John Wiley & Sons, 261-289.

Kovacs I, Holzmeister C, Wirtz M, Geerlof A, Fröhlich T, Römling G, Kuruthukulangarakoola GT, Linster E, Hell R, Arnold GJ et al. 2016. ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms. Frontiers in Plant Science 7: 1-17.

Lee J, Lee Y, Lee MJ, Park E, Kang SH, Chung CH, Lee KH, Kim K. 2008a. Dual modification of BMAL1 by SUMO2/3 and ubiquitin promotes circadian activation of the CLOCK/BMAL1 complex. Molecular and Cellular Biology 28: 6056-6065.

Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E. 2008b. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20: 786-802.

Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso JB, Corpas FJ. 2011. Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signaling & Behavior 6: 789-793.

Lindermayr C, Saalbach G, Durner J. 2005. Proteomic identification of S-nitrosylated proteins. Plant Physiology 137: 921-930.

Ling T, Vandelle E, Bellin D, Kleinfelder-Fontanesi K, Huang JJ, Chen J, Digby AM, Delledonne M. 2012. Nitric oxide produced during the hypersensitive response modulates the plant signaling network and inhibits the pathogen’s virulence machinery. Nitric Oxide 27: S9.

Lozano-Juste J, Colom-Moreno R, León J. 2011. In vivo protein tyrosine nitration in Arabidopsis thaliana. Journal of Experimental Botany 62: 3501-3517.

Mengel A, Ageeva A, Georgii E, Bernhardt J, Wu K, Durner J, Lindermayr C. 2017. Nitric oxide modulates histone acetylation at stress genes by inhibition of histone deacetylases. Plant Physiology 173: 1434-1452.

Minguez P, Parca L, Diella F, Mende DR, Kumar R, Helmer-Citterich M, Gavin A-C, van Noort V, Bork P. 2012. Deciphering a global network of functionally associated post-translational modifications. Molecular Systems Biology 8: 599.

Nakamura T, Lipton SA. 2019. Nitric oxide-dependent protein post-translational modifications impair mitochondrial function and metabolism to contribute to neurodegenerative diseases. Antioxidants & Redox Signaling. 32: 7916.

Ortega-Galisteo AP, Gupta DK, Pazmiño DM, Sandalio LM, Rodríguez-Serrano M, 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.

Ou X, Zhuang T, Yin W, Miao Y, Wang B, Zhang Y, Lin X, Xu C, von Wettstein D, Rustgi S et al. 2015. DNA methylation changes induced in rice by exposure to high concentrations of the nitric oxide modulator, sodium nitroprusside. Plant Molecular Biology Reporter 33: 1428-1440.

Saleh A, Withers J, Mohan R, Marqués J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X. 2015. Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host & Microbe 18: 169-182.

Servet C, Conde N, Zhou D. 2010. Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Molecular Plant 3: 670-677.

Shen J, Zhang J, Zhou M, Zhou H, Cui B, Gotor C, Romero LC, Fu L, Yang J, Foyer CH et al. 2020. Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell 32: 1000-1017.

Shen Y, Wei W, Zhou D-X. 2015. Histone acetylation enzymes coordinate metabolism and gene expression. Trends in Plant Science 20: 614-621.

Shi H, Ye T, Zhu J-K, Chan Z. 2014. Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. Journal of Experimental Botany 65: 4119-4131.

Skelly MJ, Malik SI, Le Bihan T, Bo Y, Jiang J, Spoel SH, Loake GJ. 2019. A role for S-nitrosylation of the SUMO-conjugating enzyme SCE1 in plant immunity. Proceedings of the National Academy of Sciences, USA 116: 17090-17095.

Tompa P, Davey NE, Gibson TJ, Babu MM. 2014. A million peptide motifs for the molecular biologist. Molecular Cell 55: 161-169.

Varshavsky A. 2011. The N-end rule pathway and regulation by proteolysis. Protein Science 20: 1298-1345.

Wawer I, Bucholc M, Astier J, Anielska-Mazur A, Dahan J, Kulik A, Wysłouch-Cieszynska A, Zaręba-Kozioł M, Krzywinska E, Dadlez M et al. 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.

Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou J-M, Zuo J. 2015. S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiology 167: 1604-1615.

Yun B, Skelly MJ, Yin M, Yu M, Mun B, Lee S, Hussain A, Spoel SH, Loake GJ. 2016. Nitric oxide and S -nitrosoglutathione function additively during plant immunity. New Phytologist 211: 516-526.

Yun B-W, Feechan A, Yin M, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang J-G, Kwon E, Spoel SH et al. 2011. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264-268.

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