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Nitric Oxide Synthesis in Leaf Peroxisomes and in Plant-Type Mitochondria

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The Biology of Subcellular Nitric Oxide

Abstract

Peroxisomes are single-membrane bound organelles that are present in almost all types of eukaryote cells (Vitam Horm 72:111–154, 2005). Plant peroxisomes may be specialized to perform certain functions, such as the glyoxysomes of oilseeds, root nodule peroxisomes of tropical legumes or the leaf peroxisomes of photosynthesizing cells (Vitam Horm 72:111–154, 2005; Biochimica et Biophysica Acta (BBA)—Mol Cell Res 1763:1478–1495, 2006). Glyoxysomes are responsible for the b-oxidation of fatty acids and also contain the glyoxalate cycle enzymes which convert lipids to carbohydrates, representing a plant-specific metabolite transition. Root nodule peroxisomes are sites of allantoin (the major transportable nitrogen form) biosynthesis (Vitam Horm 72:111–154, 2005). The leaf peroxisomes are organelles of photorespiration and are usually present in close vicinity of the chloroplasts and the mitochondria since photorespiration establishes a metabolic interlace between these three plant organelles (Plant Cell Physiol 43:689–696, 2002). Peroxisomes are also sites of hydrogen peroxide (H2O2) generation, reactive oxygen species (ROS) detoxification and involved in the biosynthesis of vitamins and plant hormones (Vitam Horm 72:111–154, 2005; Biochimica et Biophysica Acta (BBA)—Mol Cell Res 1763:1478–1495, 2006; J Exp Bot 61:1441–1453, 2010).

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Bibliography

  • Babujee L, Wurtz V, Ma C, Lueder F, Soni P, van Dorsselaer A, Reumann S (2010) The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. J Exp Bot 61:1441–1453

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupianez JA, del Rio LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274:36729–36733

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Rodriguez-Serrano M, Esteban FJ, Fernandez-Ocana 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

    Article  PubMed  CAS  Google Scholar 

  • Basset G, Quinlivan EP, Ziemak MJ, Diaz De La Garza R, Fischer M, Schiffmann S, Bacher A, Gregory JF 3rd, Hanson AD (2002) Folate synthesis in plants: the first step of the pterin branch is mediated by a unique bimodular GTP cyclohydrolase I. Proc Natl Acad Sci USA 99:12489–12494

    Article  PubMed  CAS  Google Scholar 

  • Botrel A, Kaiser WM (1997) Nitrate reductase activation state in barley roots in relation to the energy and carbohydrate status. Planta 201:496–501

    Article  PubMed  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  PubMed  CAS  Google Scholar 

  • Castello PR, David PS, McClure T, Crook Z, Poyton RO (2006) Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 3:277–287

    Article  PubMed  CAS  Google Scholar 

  • Cooper CE (2002) Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 27:33–39

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, del Rio LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150

    Article  PubMed  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, Carreras A, Quiros M, Leon AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gomez M, del Rio LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733

    Article  PubMed  CAS  Google Scholar 

  • Corpas F, Barroso J, Carreras A, Valderrama R, Palma J, León A, Sandalio L, del Río L (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200

    Article  PubMed  CAS  Google Scholar 

  • Del Rio LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11

    Article  PubMed  Google Scholar 

  • Del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81

    Article  PubMed  Google Scholar 

  • Del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405–417

    Article  PubMed  Google Scholar 

  • Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652

    Article  PubMed  CAS  Google Scholar 

  • Floryszak-Wieczorek J, Milczarek G, Arasimowicz M, Ciszewski A (2006) Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224:1363–1372

    Article  PubMed  CAS  Google Scholar 

  • Foissner I, Wendehenne D, Langebartles C, Durner J (2000) In vivo imaging of an elicitor induced nitric oxide burst in tobacco. Plant J 23:7

    Article  Google Scholar 

  • Foresi N, Correa-Aragunde N, Parisi G, Calo 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

    Article  PubMed  CAS  Google Scholar 

  • Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43:689–696

    Article  PubMed  CAS  Google Scholar 

  • Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R (2010) The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta 232:999–1005

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103

    Article  PubMed  CAS  Google Scholar 

  • Gupta KJ, Igamberdiev AU (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion 11:537–543

    Article  PubMed  CAS  Google Scholar 

  • Gupta KJ, Kaiser WM (2010) Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol 51:576–584

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hachiya T, Noguchi K (2011) Integrative response of plant mitochondrial electron transport chain to nitrogen source. Plant Cell Rep 30:195–204

    Article  PubMed  CAS  Google Scholar 

  • Holzmeister C, Frohlich A, Sarioglu H, Bauer N, Durner J, Lindermayr C (2011) Proteomic analysis of defense response of wildtype Arabidopsis thaliana and plants with impaired NO- homeostasis. Proteomics 11:1664–1683

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Kerschbaum HH, Engel E, Hermann A (1997) Biochemical characterization and histochemical localization of nitric oxide synthase in the nervous system of the snail, Helix pomatia. J Neurochem 69:2516–2528

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ (2007) Ostreococcus tauri: seeing through the genes to the genome. Trends Genet 23:151–154

    Article  PubMed  CAS  Google Scholar 

  • Klessig DF, Martin GB, Ekengren SK (2004a) Suppression of pathogen-inducible NO synthase (iNOS) activity in tomato increases susceptibility to Pseudomonas syringae (retraction). Proc Natl Acad Sci USA 101:16081

    Article  Google Scholar 

  • Klessig DF, Ytterberg AJ, van Wijk KJ (2004b) The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex (retraction). Cell 119:445

    Article  CAS  Google Scholar 

  • Lee JS (1998) The mechanism of stomatal closing by salicylic acid in Commelina communis L. J Plant Biol 41:97–102

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zhang J (2009) Rapid accumulation of NO regulates ABA catabolism and seed dormancy during imbibition in Arabidopsis. Plant Signal Behav 4:905–907

    Article  PubMed  CAS  Google Scholar 

  • Majlath I, Szalai G, Papp I, Vankova R, Janda T (2011) Atnoa1 mutant Arabidopsis plants induce compensation mechanisms to reduce the negative effects of the mutation. J Plant Physiol 168:1184–1190

    Article  PubMed  CAS  Google Scholar 

  • Mano S, Nishimura M (2005) Plant peroxisomes. Vitam Horm 72:111–154

    Article  PubMed  CAS  Google Scholar 

  • Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem 283:32957–32967

    Article  PubMed  CAS  Google Scholar 

  • Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants—where do we stand? Physiol Plant 138:372–383

    Article  PubMed  CAS  Google Scholar 

  • Moro MA, Darley-Usmar VM, Goodwin DA, Read NG, Zamora-Pino R, Feelisch M, Radomski MW, Moncada S (1994) Paradoxical fate and biological action of peroxynitrite on human platelets. Proc Natl Acad Sci USA 91:6702–6706

    Article  PubMed  CAS  Google Scholar 

  • Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochimica et Biophysica Acta (BBA)—Mol Cell Res 1763:1478–1495

    Article  CAS  Google Scholar 

  • Pauly N, Ferrari C, Andrio E, Marino D, Piardi S, Brouquisse R, Baudouin E, Puppo A (2011) MtNOA1/RIF1 modulates Medicago truncatula-Sinorhizobium meliloti nodule development without affecting its nitric oxide content. J Exp Bot 62:939–948

    Article  PubMed  CAS  Google Scholar 

  • Pedroso MC, Magalhaes JR, Durzan D (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. J Exp Bot 51:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Planchet E, Kaiser WM (2006) Nitric oxide production in plants: facts and fictions. Plant Signal Behav 1:46–51

    Article  PubMed  Google Scholar 

  • Planchet E, Jagadis Gupta K, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743

    Article  PubMed  CAS  Google Scholar 

  • Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714

    Article  PubMed  CAS  Google Scholar 

  • Robbens S, Derelle E, Ferraz C, Wuyts J, Moreau H, Van de Peer Y (2007) The complete chloroplast and mitochondrial DNA sequence of Ostreococcus tauri: organelle genomes of the smallest eukaryote are examples of compaction. Mol Biol Evol 24:956–968

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rőszer T, Kiss-Tóth E, Rózsa D, Józsa T, Szentmiklósi AJ, Bánfalvi G (2010) Hypothermia translocates nitric oxide synthase from cytosol to membrane in snail neurons. Cell Tissue Res 342:191–203

    Article  PubMed  Google Scholar 

  • Sakuma S, Fujimoto Y, Sakamoto Y, Uchiyama T, Yoshioka K, Nishida H, Fujita T (1997) Peroxynitrite induces the conversion of xanthine dehydrogenase to oxidase in rabbit liver. Biochem Biophys Res Commun 230:476–479

    Article  PubMed  CAS  Google Scholar 

  • Salanoubat M, Lemcke K, Rieger M, Ansorge W, Unseld M, Fartmann B, Valle G, Blocker H, Perez-Alonso M, Obermaier B, Delseny M, Boutry M, Grivell LA, Mache R, Puigdomenech P, De Simone V, Choisne N, Artiguenave F, Robert C, Brottier P, Wincker P, Cattolico L, Weissenbach J, Saurin W, Quetier F, Schafer M, Muller-Auer S, Gabel C, Fuchs M, Benes V, Wurmbach E, Drzonek H, Erfle H, Jordan N, Bangert S, Wiedelmann R, Kranz H, Voss H, Holland R, Brandt P, Nyakatura G, Vezzi A, D’Angelo M, Pallavicini A, Toppo S, Simionati B, Conrad A, Hornischer K, Kauer G, Lohnert TH, Nordsiek G, Reichelt J, Scharfe M, Schon O, Bargues M, Terol J, Climent J, Navarro P, Collado C, Perez-Perez A, Ottenwalder B, Duchemin D, Cooke R, Laudie M, Berger-Llauro C, Purnelle B, Masuy D, de Haan M, Maarse AC, Alcaraz JP, Cottet A, Casacuberta E, Monfort A, Argiriou A, flores M, Liguori R, Vitale D, Mannhaupt G, Haase D, Schoof H, Rudd S, Zaccaria P, Mewes HW, Mayer KF, Kaul S, Town CD, Koo HL, Tallon LJ, Jenkins J, Rooney T, Rizzo M, Walts A, Utterback T, Fujii CY, Shea TP, Creasy TH, Haas B, Maiti R, Wu D, Peterson J, Van Aken S, Pai G, Militscher J, Sellers P, Gill JE, Feldblyum TV, Preuss D, Lin X, Nierman WC, Salzberg SL, White O, Venter JC, Fraser CM, Kaneko T, Nakamura Y, Sato S, Kato T, Asamizu E, Sasamoto S, Kimura T, Idesawa K, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakayama S, Nakazaki N, Shinpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (2000) Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. Nature 408:820–822

    Article  PubMed  CAS  Google Scholar 

  • Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. J Integr Plant Biol 50:231–243

    Article  PubMed  CAS  Google Scholar 

  • Shapiro AD (2005) Nitric oxide signaling in plants. Vitam Horm 72:339–398

    Article  PubMed  CAS  Google Scholar 

  • Shiva S, Rassaf T, Patel RP, Gladwin MT (2011) The detection of the nitrite reductase and NO-generating properties of haemoglobin by mitochondrial inhibition. Cardiovasc Res 89:566–573

    Article  PubMed  CAS  Google Scholar 

  • Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474

    Article  PubMed  CAS  Google Scholar 

  • Sturms R, Dispirito AA, Hargrove MS (2011) Plant and Cyanobacterial Hemoglobins Reduce Nitrite to Nitric Oxide under Anoxic Conditions. Biochemistry 50:3873–3878

    Article  PubMed  CAS  Google Scholar 

  • Sudhamsu J, Lee GI, Klessig DF, Crane BR (2008) The structure of YqeH. An AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition. J Biol Chem 283:32968–32976

    Article  PubMed  CAS  Google Scholar 

  • Sun LR, Hao FS, Lu BS, Ma LY (2010) AtNOA1 modulates nitric oxide accumulation and stomatal closure induced by salicylic acid in Arabidopsis. Plant Signal Behav 5:1022–1024

    Article  PubMed  Google Scholar 

  • Tischner R, Planchet E, Kaiser WM (2004) Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett 576:151–155

    Article  PubMed  CAS  Google Scholar 

  • Tiso M, Tejero J, Basu S, Azarov I, Wang X, Simplaceanu V, Frizzell S, Jayaraman T, Geary L, Shapiro C, Ho C, Shiva S, Kim-Shapiro DB, Gladwin MT (2011) Human Neuroglobin Functions as a Redox-regulated Nitrite Reductase. J Biol Chem 286:18277–18289

    Article  PubMed  CAS  Google Scholar 

  • Travis J (2004) Plant biology. NO-making enzyme no more: Cell, PNAS papers retracted. Science 306:960

    Article  PubMed  CAS  Google Scholar 

  • Vitecek J, Reinohl V, Jones RL (2008) Measuring NO production by plant tissues and suspension cultured cells. Mol Plant 1:270–284

    Article  PubMed  CAS  Google Scholar 

  • Wink DA, Hanbauer I, Grisham MB, Laval F, Nims RW, Laval J, Cook J, Pacelli R, Liebmann J, Krishna M, Ford PC, Mitchell JB (1996) Chemical biology of nitric oxide: regulation and protective and toxic mechanisms. Curr Top Cell Regul 34:159–187

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki H (2000) Nitrite-dependent nitric oxide production pathway: implications for involvement of active nitrogen species in photoinhibition in vivo. Philos Trans R Soc Lond B Biol Sci 355:1477–1488

    Article  PubMed  CAS  Google Scholar 

  • Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA 101:15811–15816

    Article  PubMed  CAS  Google Scholar 

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Rőszer, T. (2012). Nitric Oxide Synthesis in Leaf Peroxisomes and in Plant-Type Mitochondria. In: The Biology of Subcellular Nitric Oxide. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2819-6_4

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