Abstract
Studies in the last two decades have firmly established that the gaseous free radical nitric oxide (NO) is an intracellular and intercellular mediator of signal transduction pathways controlling plant growth and development, as well as plant responses to biotic and abiotic stresses. The underlying mechanisms of NO action may rely on its reactivity with different kinds of biomolecules, leading to modulation of enzymatic activities, and of gene transcription, with profound impact on metabolism and signal transduction pathways. NO homeostasis depends on the appropriate coordination of NO synthesis and degradation under different physiological conditions. The mechanisms by which NO is synthesized de novo in plants are still a matter of controversy, although in the last years, the key role of the enzyme nitrate reductase (NR) in plants NO production has been widely accepted. In addition, S-nitrosoglutathione (GSNO), which forms by spontaneous reaction of NO with glutathione, is likely a major NO reservoir and NO donor in plant cells. GSNO levels are controlled by the enzyme GSNO reductase that has emerged as the main enzyme responsible for the modulation of S-nitrosothiol pools. The number of plant processes influenced/modulated by NO has dramatically increased in the last years. This review particularly emphasizes the roles of NR and GSNOR enzymes in NO homeostasis and NO-mediated plant responses to environmental challenges.
Similar content being viewed by others
References
Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615
Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS ONE 6:e20714
Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Rio LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793
Baudouin E (2011) The language of nitric oxide signaling. Plant Biol 13:233–242
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39
Besson-Bard A, Astier J, Rasul S, Wawer I, Dubreuil-Maurizi C, Jeandroz S, Wendehenne D (2009) Current view of nitric oxide-responsive genes in plants. Plant Sci 177:302–309
Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341
Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytol 182:17–30
Brown GC (2007) Nitric oxide and mitochondria. Frontiers Biosci 12:1024–1033
Castello P, David P, McClure T, Crook Z, Poyton R (2006) Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxia signaling in eukaryotes. Cell Metab 3:277–287
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J, Zuo J (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S- nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387
Cooper CE, Giulivi C (2007) Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am J Physiol—Cell Physiol 292:1993–2003
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 49:1711–1722
Corpas FJ, Chaki M, Leterrier M, Barroso JB (2009) Protein tyrosine nitration: a new challenge in plants. Plant Signal Behav 4:920–923
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 181:604–611
Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D (2008) Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J Exp Bot 59:155–163
de Oliveira HC, Wulff A, Saviani EE, Salgado I (2008) Nitric oxide degradation by potato tuber mitochondria: evidence for the involvement of external NAD(P)H dehydrogenases. Biochim Biophys Acta 1777:470–476
del Rio LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792
Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588
Díaz M, Achkor H, Titarenko E, Martínez MC (2003) The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett 543:136–139
Durner J, Wendehenne D, Klessing DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Elstner EF, Osswald W (1991) Air pollution: involvement of oxygen radicals (a mini review). Free Radical Res Commun 12–13:795–807
Espunya MC, Michele R, Gómez-Cadenas A, Martínez MC (2012) S-nitrosoglutathione is a componente of wound- and salicylic acid-induced systemic responses in Arabidopsis thaliana. J Exp Bot 63:3219–3227
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 USA 102:8054–8059
Ferrarini A, De Stefano M, Baudouin E, Pucciariello C, Polverari A, Puppo A, Delledonne M (2008) Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol Plant Microbe Interact 21:781–790
Flores T, Todd CD, Tovar-Mendez A, Dhanoa PK, Correa-Aragunde N (2008) Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiol 147:1936–1946
Freschi L, Rodrigues MA, Domingues DS, Purgatto E, Van Sluys MA, Magalhaes JR, Kaiser WM, Mercier H (2010) Nitric oxide mediates the hormonal control of crassulacean acid metabolism expression in young pineapple plants. Plant Physiol 152:1971–1985
Friebe A, Koesling D (2009) The function of NO-sensitive guanylyl cyclase: what we can learn from genetic mouse models. Nitric Oxide 21:149–156
Frungillo L, de Oliveira JF, Saviani EE, Oliveira HC, Martínez MC, Salgado I (2013) Modulation of mitochondrial activity by S-nitrosoglutathione reductase in Arabidopsis thaliana transgenic cell lines. Biochim Biophys Acta 1827:239–247
Gao Y (2010) The multiple actions of NO. Pflügers Arch Eur J Physiol 459:829–839
Gouvêa CMPC, Souza FJ, Magalhães ACN, Martins IS (1997) NO releasing substances that induce growth elongation in maize root segments. Plant Growth Regul 21:183–187
Grünn S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516
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. J Exp Bot 56:2601–2609
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168
He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971
Hebelstrup KH, Jensen EO (2008) Expression of NO scavenging hemoglobin is involved in the timing of bolting in Arabidopsis thaliana. Planta 227:917–927
Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923
Igamberdiev AU, Baron K, Manac’h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557–564
Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255
Klepper L (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ 13:537–542
Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Lea PJ (1993) Nitrogen Metabolism. In: Lea PJ, Leegood RC (eds) Plant biochemistry and molecular biology. Wiley, New York, pp 155–180
Lee U, Wie C, Fernandez BO, Feelish M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 20:786–802
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signaling in plant defence. Curr Opin Plant Biol 12:451–458
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 6:789–793
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907
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 410:490–494
Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M, Gao Q, Tian LL, Xu ZH, Bao F, Hu Y, Ye NS, Pei ZM, He YK (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci USA 110:1548–1553
Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517
Melo PM, Silva LS, Ribeiro I, Seabra AR, Carvalho HG (2011) Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiol 157:1505–1517
Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398:155–158
Modolo LV, Augusto O, Almeida IMG, Magalhaes JR, Salgado I (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820
Modolo LV, Augusto O, Almeida IMG, Pinto-Maglio CAF, Oliveira HC, Seligman K, Salgado I (2006) Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae. Plant Sci 171:34–40
Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants—where do we stand? Physiol Plant 138:372–383
Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Oliveira HC, Justino GC, Sodek L, Salgado I (2009) Amino acid recovery does not prevent susceptibility to Pseudomonas syringae in nitrate reductase double-deficient Arabidopsis thaliana plants. Plant Sci 176:105–111
Oliveira HC, Saviani EE, Oliveira JFP, Salgado I (2010) Nitrate reductase-dependent nitric oxide synthesis in the defense response of Arabidopsis thaliana against Pseudomonas syringae. Tropical Plant Pathol 35:104–107
Oliveira HC, Salgado I, Sodek L (2013) Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia. Planta 237:255–264
Palmer RM, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526
Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186
Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant Microbe Interact 23:846–860
Qiao W, Fan LM (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246
Radi R (2013) Protein tyrosine nitration: Biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46:550–559
Radi R, Cassina A, Hodara R (2002) Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem 383:401–409
Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ 35:1483–1499
Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110
Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signalling functions in plant–pathogen interactions. Cell Microbiol 6:795–803
Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-Nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130
Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469
Rumer S, Gupta KJ, Kaiser WM (2009) Plant cells oxidize hydroxylamines to NO. J Exp Bot 60:2065–2072
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 143:1282–1292
Sánchez C, Cabrera JJ, Gates AJ, Bedmar EJ, Richardson DJ, Delgado MJ (2011) Nitric oxide detoxification in the rhizobia-legume symbiosis. Biochem Soc Trans 39:184–188
Saviani EE, Orsi CH, Oliveira JFP, Pinto-Maglio CAF, Salgado I (2002) Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett 510:136–140
Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CAF, Salgado I (2008) Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol 49:1112–1121
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455
Spoel SH, Loake GJ (2011) Redox-based protein modifications: the missing link in plant immune signalling. Curr Opin Plant Biol 14:358–364
Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902
Stamler JS, Lamas S, Fang FC (2001) Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106:675–683
Stohr C, Strube F, Marx G, Ullrich WR, Rockel P (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212:835–841
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956
Terrile MC, París R, Calderón-Villalobos LI, 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 70:492–500
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A, Taylor P, Xue P, Yang FQ, Xie ZS, Pallas JA, Chu CC, Loake GJ (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284:2131–2137
Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signaling and defence responses. Curr Opin Plant Biol 7:449–455
Wulff A, Oliveira HC, Saviani EE, Salgado I (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21:132–139
Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129
Yun BW, Feechan A, Yin MH, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268
Acknowledgments
We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Grant 473090/2011-2) and Spanish Ministry of Science and Innovation (Grant BFU2010-15090) for financial support. LF is supported by a student fellowship from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Salgado, I., Carmen Martínez, M., Oliveira, H.C. et al. Nitric oxide signaling and homeostasis in plants: a focus on nitrate reductase and S-nitrosoglutathione reductase in stress-related responses. Braz. J. Bot 36, 89–98 (2013). https://doi.org/10.1007/s40415-013-0013-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-013-0013-6