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2013 | 35 | 08 |
Tytuł artykułu

Immunolocalization of S-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosine nitration in pea leaf organelles

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S-Nitrosoglutathione (GSNO) is a nitrosothiol which plays a major role in the metabolism of NO in higher plants mediating signaling processes. Protein tyrosine nitration (NO2–Tyr) is a post-translational modification which contributes to protein regulation. The subcellular localization of GSNO, S-nitrosoglutathione reductase (GSNOR), an enzyme which catalyzes its decomposition and protein tyrosine nitration was studied in pea (Pisum sativum L.) leaf plants with the aid of the electron microscopy immunogold-labeling technique. Our findings show that GSNO, GSNOR and nitrated proteins are present in the different subcellular compartments of leaf cells which include chloroplasts, cytosol, mitochondria, and peroxisomes. Given that pea peroxisomes are one of the cell compartments where nitric oxide (NO) has been thoroughly studied, our results provide additional insights into the metabolism of NO in this organelle where NO and GSNO could function as signal molecules in cross talk between the different cell compartments.
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Opis fizyczny
  • Grupo de Sen˜alizacio´n Molecular y Sistemas Antioxidantes en Plantas, Unidad Asociada al CSIC (EEZ), A ´ rea de Bioquı´mica y Biologı´a Molecular, Universidad de Jae´n, 23071 Jae´n, Spain
  • Grupo de Sen˜alizacio´n Molecular y Sistemas Antioxidantes en Plantas, Unidad Asociada al CSIC (EEZ), A ´ rea de Bioquı´mica y Biologı´a Molecular, Universidad de Jae´n, 23071 Jae´n, Spain
  • Departamento de Bioquı´mica, Biologı´a Celular y Molecular de Plantas, Estacio´n Experimental del Zaidı´n (EEZ), CSIC, Apartado 419, 18080 Granada, Spain
  • 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
  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Rıo LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295
  • Astier J, Kulik A, Koen E, Besson-Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D (2012) Protein S-nitrosylation: what’s going on in plants? Free Radic Biol Med 53:1101–1110
  • Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupiañez JA, del Rio LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274: 36729–36733
  • Barroso JB, Corpas FJ, Carreras A, Rodriguez-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 signalling. Plant Biol (Stuttg) 13:233–242
  • Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013a) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64:1121–1134
  • Begara-Morales JC, López-Jaramillo FJ, Sánchez-Calvo B, Carreras A, Ortega-Muñoz M, Santoyo-González F, Corpas FJ, Barroso JB (2013b) Vinyl sulfone silica: application of an open preactivated support to the study of transnitrosylation of plant proteins by S-nitrosoglutathione. BMC Plant Biol 3:61
  • Camejo D, Romero-Puertas MC, Rodrıguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteomics 79:87–99
  • Cecconi D, Orzetti S, Vandelle E, Rinalducci S, Zolla L, Delledonne M (2009) Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis 30:2460–2468
  • Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodrıguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009a) 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, López-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Gómez-Rodrıguez MV, Corpas FJ, Barroso JB (2009b) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60:4221–4234
  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodrıguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011a) 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
  • Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodrıguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011b) Mechanical wounding induces a nitrosative stress by downregulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813
  • Chaki M, Carreras A, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Valderrama R, Corpas FJ, Barroso JB (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (b-CA) activity under high temperature stress. Nitric Oxide 29:30–33
  • 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
  • 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, Bunkelmann J, Trelease RN (1994) Identification and immunochemical characterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. Eur J Cell Biol 65:280–290
  • Corpas FJ, Barroso JB, Carreras A, Quiro´s M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Rı´o LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733
  • Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Rıo LA (2006) Constitutive argininedependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254
  • Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Rı´o LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722
  • Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) 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, Alché JD, Barroso JB (2013a) Current overview of Snitrosoglutathione (GSNO) in higher plants. Front Plant Sci. doi: 10.3389/fpls.2013.00126
  • Corpas FJ, Palma JM, del Rıo LA, Barroso JB (2013b) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 4:29
  • Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39
  • del Rıo LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11
  • Espunya MC, Dıaz M, Moreno-Romero J, Martınez MC (2006) Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. Plant Cell Environ 29:1002–1011
  • Fahimi HD, Reich D, Völkl A, Baumgart E (1996) Contributions of the immunogold technique to investigation of the biology of peroxisomes. Histochem Cell Biol 106:105–114
  • Galatro A, Puntarulo S, Guiamet JJ, Simontacchi M (2013) Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiol Biochem 66:26–33
  • Ischiropoulos H (2009) Protein tyrosine nitration: an update. Arch Biochem Biophys 484:117–121
  • 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
  • Jensen DE, Belka GK, Du Bois GC (1998) S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331:659–668
  • 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 20:786–802
  • 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 6:789–793
  • 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
  • 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
  • Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517
  • Radi R (2013) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46:550–559
  • Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19:3170–3193
  • Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathionedependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24
  • Stec B (2012) Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. Proc Natl Acad Sci USA 109(46):18785–18790
  • Suss KH, Arkona C, Manteuffel R, Adler K (1993) Calvin cycle multienzyme complexes are bound to chloroplast thylakoid membranes of higher plants in situ. Proc Natl Acad Sci USA 90:5514–5518
  • Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599
  • Tewari RK, Prommer J, Watanabe M (2013) Endogenous nitric oxide generation in protoplast chloroplasts. Plant Cell Rep 32(1):31–44
  • Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodrıguez MV, Colmenero-Varea P, del Rıo LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461
  • Zechmann B, Müller M (2010) Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 246:15–24
  • Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027
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