Abstract
Nitric oxide is a gaseous free radical with a wide range of direct and indirect actions in plant cells. However, the enzymatic sources of NO and its subcellular localization in plants are still under debate. Among the different subcellular compartments where NO has been found to be produced, peroxisomes are the best characterized since in these organelles it has been demonstrated the presence of NO and it has been biochemically characterized a L-arginine-dependent nitric oxide synthase activity. This chapter summarizes the present knowledge of the NO metabolism and its derived reactive nitrogen species (RNS) in plant peroxisomes and how this gaseous free radical is involved in natural senescence, and is released to the cytosol under salinity stress conditions acting as a signal molecule.
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
Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: Change in S-nitrosylation of rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9:4368–4380
Airaki M, Sánchez-Moreno L, Leterrier M, Barroso JB, Palma JM, Corpas FJ (2011) Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. Plant Cell Physiol 52:2006–2015
Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615
Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupiáñez JA, del Río LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274: 36729–36733
Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río 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, Pieuchot L, Engler G, Pauly N, Puppo A (2006) Nitric oxide is formed in Medicago truncatula-Sinorhizobium meliloti functional nodules. Mol Plant Microbe Interact 19:970–975
Bethke PC, Libourel IG, Jones RL (2006) Nitric oxide reduces seed dormancy in Arabidopsis. J Exp Bot 57:517–526
Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199
Chaki M (2007) Function of reactive nitrogen species in sunflower (Helianthus annuus) in response to abiotic and biotic stresses. Ph.D. Thesis, University of Jaén, Spain
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 50:265–279
Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ 34:1803–1818
Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384
Corpas FJ, Barroso JB, del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150
Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004a) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733
Corpas FJ, Barroso JB, León AM, Carreras A, Quirós M, Palma JM, Sandalio LM, del Río LA (2004b) Peroxisomes as a source of nitric oxide. In: Magalhaes JR, Singh RP, Passos LP (eds) Nitric oxide signaling in plants. Studium Press, LLC, Houston, pp 111–129. ISBN 0-9761849-2-3
Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254
Corpas FJ, Carreras A, Esteban FJ, Chaki M, Valderrama R, del Río LA, Barroso JB (2008) Localization of S-nitrosothiols and assay of nitric oxide synthase and S-nitrosoglutathione reductase activity in plants. Methods Enzymol 437:559–572
Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009a) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2094
Corpas FJ, Palma JM, del Río LA, Barroso JB (2009b) Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14
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
De Bellis L, Picciarelli P, Pistelli L, Alpi A (1990) Localization of glyoxylate-cycle enzymes in peroxisomes of senescent leaves and green cotyledons. Planta 180:435–439
del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11
del Río LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200
del Río LA, Sandalio LM, Palma JM, Bueno P, Corpas FJ (1992) Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Rad Biol & Med 13:557–80
del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272
del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792
Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374
Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830
Foster MW, Stamler JS (2004) New insights into protein S-nitrosylation. Mitochondria as a model system. J Biol Chem 279:25891–25897
Ghosh DK, Salerno JC (2003) Nitric oxide synthases: domain structure and alignment in enzyme function and control. Front Biosci 8:193–209
Hancock JT (2012) NO synthase? Generation of nitric oxide in plants. Periodicum Biologorum 114:19–24
Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303
Hung KT, Kao CH (2003) Nitric oxide counteracts the senescence of rice leaves induced by abscisic acid. J Plant Physiol 160:871–879
Kissner R, Nauser T, Bugnon P, Lye PG, Koppenol WH (1997) Formation and properties of peroxynitrite as studied by laser flash photolysis, high pressure stopped flow technique, and pulse radiolysis. Chem Res Toxicol 10:1285–1292
Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351
Leach J, Keyster M, Du Plessis M, Ludidi N (2010) Nitric oxide synthase activity is required for development of functional nodules in soybean. J Plant Physiol 167:1584–1591
Leshem YY (2000) Nitric oxide in plants: occurrence, function and use. Kluwer Academic, Dordrecht
Leshem YY, Haramaty E (1996) The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. J Plant Physiol 148:258–263
Leshem YY, Wills RBH, Veng-Va Ku V (1998) Evidence for the function of the free radical gas-nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
Loughran PA, Stolz DB, Vodovotz Y, Watkins SC, Simmons RL, Billiar TR (2005) Monomeric inducible nitric oxide synthase localizes to peroxisomes in hepatocytes. Proc Natl Acad Sci USA 102:13837–13842
Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517
Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, Nishimura M (2002) Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol 43:331–341
Mano S, Nakamori C, Nito K, Kondo M, Nishimura M (2006) The Arabidopsis pex12 and pex13 mutants are defective in both PTS1- and PTS2-dependent protein transport to peroxisomes. Plant J 47:604–618
Moncada S, Palmer RMJ, Higgs EA (1991) Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol Rev 43:109–142
Mur LA, Carver TL, Prats E (2006) NO way to live; the various roles of nitric oxide in plant-pathogen interactions. J Exp Bot 57:489–505
Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35
Noble DR, Swift HR, Williams DLH (1999) Nitric oxide release from S-nitrosoglutathione (GSNO). Chem Commun 18:2317–2318
Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103
Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J (2010) Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiol 152:1514–1528
Pastori GM, del Río LA (1997) Natural senescence of pea leaves: an activated oxygen-mediated function for peroxisomes. Plant Physiol 113:411–418
Pracharoenwattana I, Smith SM (2008) When is a peroxisome not a peroxisome? Trends Plant Sci 13:522–525
Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714
Procházková D, Wilhelmová N (2011) Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. Nitric Oxide 24:61–65
Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci USA 101:4003–4008
Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber AP, Olsen LJ, Hu J (2009) In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150:125–143
Romero-Puertas MC, Campostrini N, Matte 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
Shapiro AD (2005) Nitric oxide signaling in plants. Vitam Horm 72:339–398
Šírová J, Sedlářová M, Piterková J, Luhová L, Petřivalský M (2011) The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci 181:560–572
Stamler JS, Lamas S, Fang FC (2001) Nitrosylation the prototypic redox based signaling mechanism. Cell 106:675–683
Stolz DB, Zamora R, Vodovotz Y, Loughran PA, Billiar TR, Kim YM, Simmons RL, Watkins SC (2002) Peroxisomal localization of inducible nitric oxide synthase in hepatocytes. Hepatology 36:81–93
Strother S (1988) The role of free radicals in leaf senescence. Gerontology 34:151–156
Szabó C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6:662–680
Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461
Wojtaszek P (2000) Nitric oxide in plants: to NO or not to NO. Phytochemistry 54:1–4
Yoshioka H, Mase K, Yoshioka M, Kobayashi M, Asai S (2011) Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide 25:216–221
Zafra A, Rodríguez-García MI, Alché JD (2010) Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol 10:36
Acknowledgements
Work in our laboratories was supported by ERDF-cofinanced grants from the Ministry of Science and Innovation (projects BIO2009-12003-C02-01 and BIO2009-12003-C02-02, and ACI2009-0860) and Junta de Andalucía (groups BIO-192 and BIO-286), Spain.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Corpas, F.J., Barroso, J.B., Palma, J.M., del Río, L.A. (2013). Peroxisomes as Cell Generators of Reactive Nitrogen Species (RNS) Signal Molecules. In: del Río, L. (eds) Peroxisomes and their Key Role in Cellular Signaling and Metabolism. Subcellular Biochemistry, vol 69. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6889-5_15
Download citation
DOI: https://doi.org/10.1007/978-94-007-6889-5_15
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-6888-8
Online ISBN: 978-94-007-6889-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)