Abstract
Nitric oxide (NO) is a key signalling molecule involved in fundamental processes in animals and plants. NO mainly transmits its action through post-translational modifications (NO-PTMs), among which S-nitrosylation, the covalent attachment of an NO group to a rare, highly reactive cysteine (Cys) thiol to form an S-nitrosothiol (SNO), is preeminent. In the last decade, the numbers of proteins identified that undergo S-nitrosylation have significantly increased. This analysis has revealed that a wide range of both physiological and stress response processes are regulated by this post-translational modification. To function effectively as a molecular cue, S-nitrosylation must be specific and reversible. Denitrosylation, the removal of an NO group from an SNO, has emerged as a key regulatory process. While the role of S-nitrosylation in plant biology has garnered significant attention, denitrosylation, a pivotal counterpoint, remains relatively unexplored. In plants, S-nitrosoglutathione reductase (GSNOR) and thioredoxin reductase (Trx)-mediated denitrosylation have emerged as key mechanisms for denitrosylation.
This chapter describes the current state of the art with respect to the role of denitrosylation in plant biology.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Achkor H, Díaz M, Fernández MR, Biosca JA, Parés X, Martínez MC (2003) Enhanced formaldehyde detoxification by overexpression of glutathione-dependent formaldehyde dehydrogenase from Arabidopsis. Plant Physiol 132(4):2248–2255
Alderton WK, Cooper CH, Knowles R (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615
Anand P, Stamler JS (2012) Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J Mol Med 90(3):233–244
Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181(5):527–533
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014a) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65(2):527–538
Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014b) Differential transcriptomic analysis by RNA-seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55(6):1080–1095
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. J Exp Bot 66(19):5983–5996
Beigi F, Gonzalez DR, Minhas KM, Sun Q-A, Foster MW, Khan SA, Treuer AV, Dulce RA, Harrison RW, Saraiva RM (2012) Dynamic denitrosylation via S-nitrosoglutathione reductase regulates cardiovascular function. Proc Natl Acad Sci 109(11):4314–4319
Beligni MV, Laxalt AM, Lamattina L (1997) Putative role of nitric oxide in plant-pathogen interactions. In: Moncada S, Toda N, Higgs EA (eds) The biology of nitric oxide, Part 6. Portland Press, London, 250p
Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320(5879):1050–1054
Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10(10):721–732
Cao Y, Gomes SA, Rangel EB, Paulino EC, Fonseca TL, Li J, Teixeira MB, Gouveia CH, Bianco AC, Kapiloff MS (2015) S-nitrosoglutathione reductase-dependent PPARγ denitrosylation participates in MSC-derived adipogenesis and osteogenesis. J Clin Invest 125(4):1679–1691
Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol 50(2):265–279
Chaki M, Kovacs I, Spannagl M, Lindermayr C (2014) Computational prediction of candidate proteins for S-nitrosylation in Arabidopsis thaliana. PLoS One 9(10):e110232
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19(12):1377–1387
Corpas FJ, Chaki M, Fernández-Ocaña 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 Physiol 49(11):1711–1722
Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181(5):604–611
Corrales FJ, Ruiz F, Mato JM (1999) In vivo regulation by glutathione of methionine adenosyltransferase S-nitrosylation in rat liver. J Hepatol 31(5):887–894
Correa-Aragunde N, Cejudo FJ, Lamattina L (2015) Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in Arabidopsis. Ann Bot 116(4):695–702
Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394(6693):585–588
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci 98(23):13454–13459
Dubreuil-Maurizi C, Poinssot B (2012) Role of glutathione in plant signaling under biotic stress. Plant Signal Behav 7(2):210–212
Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci 95(17):10328–10333
Feechan A, Kwon E, Yun B-W, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci 102(22):8054–8059
Foster MW, Hess DT, Stamler JS (2009) Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med 15(9):391–404
Frendo P, Baldacci-Cresp F, Benyamina SM, Puppo A (2013) Glutathione and plant response to the biotic environment. Free Radic Biol Med 65:724–730
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2012) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212
Gong B, Wen D, Wang X, Wei M, Yang F, Li Y, Shi Q (2015) S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L. Plant Cell Physiol 56(4):790–802
Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124(1):21–30
Greco TM, Hodara R, Parastatidis I, Heijnen HFG, Dennehy MK, Liebler DC, Ischiropoulos H (2006) Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci 103(19):7420–7425
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16(3):160–168
Hogg N (2002) The biochemistry and physiology of S-nitrosothiols. Annu Rev Pharmacol Toxicol 42(1):585–600
Holmes AJ, Williams DLH (2000) Reaction of ascorbic acid with S-nitrosothiols: clear evidence for two distinct reaction pathways. J Chem Soc Perkin Trans 2(8):1639–1644
Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci 84(24):9265–9269
Jensen D, Belka G, Du Bois G (1998) S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331:659–668
Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12(12):2339–2350
Klepper L (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ (1967) 13(4):537–542
Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56(1):153–162
Kovacs I, Lindermayr C (2013) Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Front Plant Sci 4:137
Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. doi:10.1111/nph.13502
Kronenfeld G, Engelman R, Weisman-Shomer P, Atlas D, Benhar M (2015) Thioredoxin-mimetic peptides as catalysts of S-denitrosylation and anti-nitrosative stress agents. Free Radic Biol Med 79:138–146
Kubienová L, Tichá T, Jahnová J, Luhová L, Mieslerovái B, Petrivalský M (2014) Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants. Planta 239(1):139–146
Kwon E, Feechan A, Yun B-W, Hwang B-H, Pallas JA, Kang J-G, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236(3):887–900
Laxalt A, Beligni MV, Lamattina L (1997) Nitric oxide preserves the level of chlorophyll in potato leaves infected by Phytophthora infestans. Eur J Plant Pathol 103(7):643–651
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. Plant Cell 20(3):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 Signal Behav 6(6):789–793
Lindermayr C, Sell S, Muller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22(8):2894–2907
Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410(6827):490–494
Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Ahearn G, McMahon TJ, Dickfeld T, Marshall HE, Que LG (2004) Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116(4):617–628
Malik SI, Hussain A, Yun B-W, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181(5):540–544
Marino SM, Gladyshev VN (2010) Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation. J Mol Biol 395(4):844–859
Meng T-C, Fukada T, Tonks NK (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9(2):387–399
Mitchell DA, Marletta MA (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 1(3):154–158
Moore JW, Loake GJ, Spoel SH (2011) Transcription dynamics in plant immunity. Plant Cell 23(8):2809–2820
Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113(7):935–944
Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35(2):454–484
Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37(1):113–116
Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013) Tell me more: roles of NPRs in plant immunity. Trends Plant Sci 18(7):402–411
Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327(6122):524–526
Qian J, Chen F, Kovalenkov Y, Pandey D, Moseley MA, Foster MW, Black SM, Venema RC, Stepp DW, Fulton DJR (2012) Nitric oxide reduces NADPH oxidase 5 (Nox5) activity by reversible S-nitrosylation. Free Radic Biol Med 52(9):1806–1819
Romero JM, Bizzozero OA (2009) Intracellular glutathione mediates the denitrosylation of protein nitrosothiols in the rat spinal cord. J Neurosci Res 87(3):701–709
Rustérucci C, Espunya MC, Díaz M, Chabannes M, Martínez MC (2007) S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143(3):1282–1292
Sengupta R, Holmgren A (2012) The role of thioredoxin in the regulation of cellular processes by S-nitrosylation. Biochim Biophys Acta Gen Sub 1820(6):689–700
Shi Y-F, Wang D-l, Wang C, Culler AH, Kreiser MA, Suresh J, Cohen JD, Pan J, Baker B, Liu J-Z (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8(9):1350–1365
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248(3):447–455
Smith BC, Marletta MA (2012) Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling. Curr Opin Chem Biol 16(5):498–506
Spadaro D, Yun B-W, Spoel SH, Chu C, Wang Y-Q, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Plant 138(4):360–371
Staab CA, Hellgren M, Höög JO (2008) Medium-and short-chain dehydrogenase/reductase gene and protein families: dual functions of alcohol dehydrogenase 3: implications with focus on formaldehyde dehydrogenase and S-nitrosoglutathione reductase activities. Cell Mol Life Sci 65(24):3950–3960
Stamler JS, Toone EJ, Lipton SA, Sucher NJ (1997) (S) NO signals: translocation, regulation, and a consensus motif. Neuron 18(5):691–696
Strittmatter P, Ball EG (1955) Formaldehyde dehydrogenase, a glutathione-dependent enzyme system. J Biol Chem 213(1):445–461
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321(5891):952–956
Terrile MC, París R, Calderón-Villalobos LIA, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70(3):492–500
Wang Y-Q, Feechan A, Yun B-W, Shafiei R, Hofmann A, Taylor P, Xue P, Yang F-Q, Xie Z-S, Pallas JA (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284(4):2131–2137
Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, Li H (2011) Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. J Proteomics 74(11):2498–2509
Xu S, Guerra D, Lee U, Vierling E (2013) S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front Plant Sci 4:430
Yu M, Yun B-W, Spoel SH, Loake GJ (2012) A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. Curr Opin Plant Biol 15(4):424–430
Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202(4):1142–1156
Yun B-W, Spoel SH, Loake GJ (2011) Synthesis of and signalling by small, redox active molecules in the plant immune response. Biochim Biophys Acta Gen Sub 1820(6):770–776
Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288(31):22777–22789
Acknowledgements
JBM would like to thank Alfonso Martín Escudero Foundation for funding his postdoctoral fellowship.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Begara-Morales, J.C., Loake, G.J. (2016). Protein Denitrosylation in Plant Biology. In: Lamattina, L., García-Mata, C. (eds) Gasotransmitters in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-40713-5_10
Download citation
DOI: https://doi.org/10.1007/978-3-319-40713-5_10
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-40711-1
Online ISBN: 978-3-319-40713-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)