Compartmentalization of Reactive Oxygen Species and Nitric Oxide Production in Plant Cells
Martina Janků
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorTereza Tichá
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorLenka Luhová
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorMarek Petřivalský
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorMartina Janků
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorTereza Tichá
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorLenka Luhová
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorMarek Petřivalský
Department of Biochemistry, Palacký University in Olomouc, Olomouc, Czech Republic
Search for more papers by this authorMirza Hasanuzzaman
Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
Search for more papers by this authorVasileios Fotopoulos
Cyprus University of Technology, Lemesos, Cyprus
Search for more papers by this authorKamrun Nahar
Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
Search for more papers by this authorSummary
h level of subcellular compartmentalization is as an evolutionary hallmark of eukaryotic cells. The existence of cellular compartment requires a complex system of regulations and signaling ensuring proper functioning of all biological processes in higher organisms. In plants, similarly to other organisms, reactive oxygen species (ROS) and nitrogen (RNS) species are known to be involved in controlling mechanisms of multiple molecular processes of growth, development and response to environmental stimuli. Production of individual ROS and RNS species is highly localized and controlled by compartment-specific enzymatic pathways regulated on transcriptional and post-translational control. Moreover, actual ROS and RNS levels in each compartment are influenced by their mutual chemical reactions and interactions with specific cellular antioxidants and scavengers. However, under specific condition, high induction of ROS- and RNS-producing cellular systems or their defective scavenging can result in oxidative or nitrosative stress conditions leading to irreversible damage to cellular components including nucleic acid, proteins and lipids. In this review current knowledge on molecular mechanisms involved in ROS and RNS production and homeostasis in different plant cell compartments will be summarized and future directions of ROS and RNS studies in higher plants presented.
References
- Asada, K. (1999). The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Reviews in Plant Physiology and Plant Molecular Biology 50: 601–639.
- Asai, S., Ichikawa, T., Nomura, H. et al. (2013). The variable domain of plant calcium-dependent protein kinase (CDPK) confers subcellular localization and substrate recognition for NADPH oxidase. The Journal of Biological Chemistry 288: 14332–14340.
- Bailly, C., El-Maarouf-Bouteau, H., and Corbineau, F. (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. Comptes Rendues Biologie 331: 806–814.
- Barroso, J.B., Corpas, F.J., Carreras, A. et al. (1999). Localization of nitric-oxide synthase in plant peroxisomes. Journal of Biological Chemistry 274: 36729–36733.
- Bartoli, C.G., Casalongué, C.A., Simontacchi, M. et al. (2013). Interaction between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environmental and Experimental Botany 94: 73–88.
- Baudouin, E. and Hancock, J.T. (2013). Nitric oxide signaling in plants. Frontiers in Plant Science 4: 553.
- Begara-Morales, J.C., Sánchez-Calvo, B., Chaki, M. et al. (2014). Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. Journal of Experimental Botany 65: 527–538.
- Bellin, D., Asai, S., Delledonne, M., and Yoshioka, H. (2013). Nitric oxide as a mediator for a defense responses. Molecular Plant-Microbe Interactions Journal 26: 271–277.
- Berglund, G.I., Carlsson, G.H., Smith, A.T. et al. (2002). The catalytic pathway of horseradish peroxidase at high resolution. Nature 417: 463–468.
- Berniers, F. and Berna, A. (2001). Germins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiology and Biochemistry 39: 545–554.
- Besson-Bard, A., Gravot, A., Richaud, P. et al. (2009). Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiology 149: 1302–1315.
- Bethke, P.C., Libourel, I.G., Aoyama, N. et al. (2007). The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiology 143: 1173–1188.
- Bethke, P.C., Badger, M.R., and Jones, R.L. (2008). Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16: 332–341.
- Bienert, G.P., Moller, A.L.B., Kristiansen, K.A. et al. (2007). Specific aquaporines facilitate the diffusion of hydrogen peroxide across membranes. The Journal of Biological Chemistry 282: 1183–1192.
- Bindschedler, L.V., Dewdney, J., Blee, K.A. et al. (2006). Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogene resistance. The Plant Journal 47: 851–863.
- Blokhina, O., Virolainen, E., and Fagerstedt, K.V. (2003). Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91: 179–194.
- Bolwell, G.P. and Wojtaszek, P. (1997). Mechanisms for the generation of reactive oxygen species in plant defence – a broad perspective. Physiological and Molecular Plant Pathology 51: 347–366.
- Borrell, A., Culianez-Macia, F.A., Altabella, T. et al. (1995). Arginine decarboxylase is localized in chloroplasts. Plant Physiology 109: 771–776.
- Bøller, T. and Felix, G. (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. The Annual Review of Plant Biology 60: 379–406.
- Braidot, E., Petrussa, E., Vianello, A., and Macri, F. (1999). Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I or complex II substrates. FEBS Letters 451: 347–350.
- Broniowska, K.A., Diers, A.R., and Hogg, N. (2013). S-nitrosoglutathione. Biochimica et Biophysica Acta 1830: 3173–3181.
- Brown, G.C. and Borutaite, V. (2002). Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radical Biology & Medicine 33: 1440–1450.
- Butt, Y., Lum, J., and Lo, S. (2003). Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies. Planta 216: 762–771.
- Clarke, A., Desikan, R., Hurst, R.D. et al. (2000). NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant Journal 24: 667–677.
- Cona, A., Rea, G., Angelini, R. et al. (2006). Functions of amine oxidases in plant development and defence. Trends in Plant Science 11: 80–88.
- Cooney, R.V., Harwood, P.J., Custer, L.J., and Franke, A.A. (1994). Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environmental Health Perspectives 102: 460–462.
- Corpas, F.J., Barroso, J.B., and del Río, L.A. (2001). Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends in Plant Science 6: 145–150.
- Corpas, F.J., Hayashi, M., Mano, S. et al. (2009). Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiology 151: 2083–2094.
- Corpas, F.J. and Barroso, J.B. (2014). Peroxisomal plant nitric oxide synthase (NOS) protein is imported by peroxisomal targeting signal type 2 (PTS2) in a process that depends on the cytosolic receptor PEX7 and calmodulin. FEBS Letters 588: 2049–2054.
-
Corpas, F.J., Palma, J.M., del Río, L.A., and Barroso, J.B. (2016). Nitric oxide emission and uptake from higher plants. In: Gasotransmitters in Plants: The Rise of a New Paradigm in Cell Signalling (ed. L. Lamattina), 79–94. Springer International Publishing 978-3-319-40713-5.
10.1007/978-3-319-40713-5_4 Google Scholar
- Corpas, F.J., Barroso, J.B., Palma, J.M., and Rodriguez-Ruiz, M. (2017). Plant peroxisomes: a nitro-oxidative cocktail. Redox Biology 11: 535–542.
- Courtois, C., Besson, A., Dahan, J. et al. (2008). Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. Journal of Experimental Botany 59: 155–163.
- Dat, J., Vandenabeele, S., Vranová, E. et al. (2000). Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57: 779–795.
- D'Autréaux, B. and Toledano, M.B. (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nature Review Molecular and Cell Biology 8: 813–824.
- Davidson, R.M., Reeves, P.A., Manosalva, P.M., and Leach, J.E. (2009). Germins: a diverse protein family important for crop improvement. Plant Science 177: 499–510.
- Del Río, L.A., Corpas, F.J., Sandalio, L.M. et al. (2002). Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53: 1255–1272.
- Delledonne, M., Xia, Y., Dixon, R.A., and Lamb, C. (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585–588.
- Dennes, L., McKenna, J.F., Segonzac, C. et al. (2011). Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis . Plant Physiology 156: 1364–1374.
- Domingos, P., Prado, A.M., Wong, A. et al. (2015). Nitric oxide: a multitasked signaling gas in plants. Molecular Plant 8: 506–520.
- Duan, Y1., Zhang, W., Li, B. et al. (2010). An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis . New Phytologist 186: 681–695.
- Dynowski, M., Schaaf, G., Loque, D. et al. (2008). Plant plasma membrane water channels conduct the signalling molecule H2O2 . The Biochemical Journal 414: 53–61.
- Flores-Pérez, U., Sauret-Güeto, S., Gas, E. et al. (2008). A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20: 1303–1315.
- Foresi, N., Correa-Aragunde, N., Parisi, G. et al. (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. The Plant Cell 22: 3816–3830.
- Foresi, N., Mayta, M.L., Lodeyro, A.F. et al. (2015). Expression of the tetrahydrofolate-dependent nitric oxide synthase from the green alga Ostreococcus tauri increases tolerance to abiotic stresses and influences stomatal development in Arabidopsis . The Plant Journal 82: 806–821.
- Foyer, C.H. and Halliwell, B. (1976). The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133: 21–25.
- Foyer, C.H., Lopez-Delgado, H., Dat, J.F., and Scott, I.M. (1997). Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum 100: 241–254.
- Foyer, C.H. and Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155: 2–18.
- Foyer, G. and Noctor, C.F. (2016). Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiology 171: 1581–1592.
- Freschi, L. (2013). Nitric oxide and phytohormone interactions: current status and perspectives. Frontiers in Plant Science 4: 398. https://doi.org/10.3389/fpls.2013.00398.
- Gabaldón, T. and Pittis, A.A. (2015). Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes. Biochimie 119: 262–268.
- Galatro, A., Puntarulo, S., Guiamet, J.J., and Simontacchi, M. (2013). Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiology and Biochemistry 66: 26–33.
- Gas, E., Flores-Pérez, U., Sauret-Güeto, S., and Rodríguez-Concepción, M. (2009). Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21: 18–23.
- Gaupels, F., Kuruthukulangarakoola, G.T., and Durner, J. (2012). Upstream and downstream signals of nitric oxide in pathogen defence. Current Opinion in Plant Biology 14: 707–714.
- Ghimire, K., Altmann, H.M., Straub, A.C., and Isenberg, J.S. (2017). Nitric oxide: what's new to NO? American Journal of Physiology-Cell Physiology 312: C254–C262.
- Gill, S.S. and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48: 909–930.
- Gleason, C., Huang, S., Thatcher, L.F. et al. (2011). Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proceedings of the National Academy of Sciences of the United States of America 108: 10768–10773.
- Go, Y.M. and Jones, D.P. (2008). Redox compartmentalization in eukaryotic cells. Biochimica et Biophysica Acta 1780: 1273–1290.
- Groß, F., Rudolf, E.E., Thiele, B. et al. (2017). Copper amine oxidase 8 regulates arginine-dependent nitric oxide production in Arabidopsis thaliana . Journal of Experimental Botany 68: 2149–2162.
- Guan, L. and Scandalios, J.G. (1996). Molecular evolution of maize catalases ant their relationship to the other eukaryotic and prokaryotic catalases. Journal of Molecular Evolution 42: 570–579.
- Gupta Kapuganti, J., Igamberdiev, U., and Kaiser, W.M. (2010). New insights into the mitochondrial nitric oxide production pathways. Plant Signaling and Behavior 5: 999–1001.
- Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is fundamental theme of aerobic life. Plant Physiology 141: 312–322.
- Hao, H., Fan, L., Chen, T. et al. (2014). Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis . The Plan Cell 26: 1729–1745.
- Hiraga, S., Sasaki, K., Ito, H. et al. (2001). A large family of class III plant peroxidases. Plant Cell Physiology 42: 462–468.
- Hossain, M.A., Bhattacharjee, S., Armin, S.M. et al. (2015). Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in Plant Science 6: 420.
- Igamberdiev, A.U., Bykova, N.V., Shah, J.K., and Hill, R.D. (2010). Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiologia Plantarum 138: 393–404.
- Jasid, S., Simontacchi, M., Bartoli, C.G., and Puntarulo, S. (2006). Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiology 142: 1246–1255.
- Jeandroz, S., Wipf, D., Stuehr, D.J. et al. (2016). Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Science Signaling 417: re2–re2.
- Kadota, Y., Shirasu, K., and Zipfel, C. (2015). Regulation of the NADPH oxidase RBOHD during plant immunity. Plant and Cell Physiology 56: 1472–1480.
- Kanno, T., Nakamura, K., Ikai, H. et al. (2012). Literature review of the role of hydroxyl radicals in chemically-induced mutagenicity and carcinogenicity for the risk assessment of a disinfection system utilizing photolysis of hydrogen peroxide. Journal of Clinical Biochemistry and Nutrition 51: 9–14.
- Kärkönen, A. and Kuchitsu, K. (2015). Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112: 22–32.
- Keegstra, K. (2010). Plant Cell Walls. Plant Physiology 154: 483–486.
- Keszler, A., Zhang, Y., and Hogg, N. (2010). Reaction between nitric oxide, glutathione, and oxygen in the presence and absence of protein: how are S-nitrosothiols formed? Free Radical Biology and Medicine 48: 55–64.
- Kim, N.H., Kim, B.S., and Hwang, B.K. (2013). Pepper arginine decarboxylase is required for polyamine and γ-aminobutyric acid signaling in cell death and defense response. Plant Physiology 162: 2067–2083.
- Kimura, S., Kaya, H., Kawarazaki, T. et al. (2012). Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidase and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochimica et Biophysica Acta 1823: 398–405.
- Knowles, R.G. and Moncada, S. (1994). Nitric oxide synthases in mammals. Biochemical Journal 298: 249–258.
- Kolbert, Z., Ortega, L., and Erdei, L. (2010). Involvement of nitrate reductase (NR) in osmotic stress-induced NO generation of Arabidopsis thaliana L. roots. Journal of Plant Physiology 167: 77–80.
- Krieger-Liszkay, A., Fufezan, C., and Trebst, A. (2008). Singlet oxygen production in photosystem II and related protection mechanism. Photosynthesis Research 98: 551–564.
- Kuzmin, A.N., Levchenko, S.M., Pliss, A. et al. (2017). Molecular profiling of single organelles for quantitative analysis of cellular heterogeneity. Scientific Reports 7: 6512.
- Jeevan Kumar, S.P., Rajendra Prasad, S., Banerjee, R., and Thammineni, C. (2015). Seed birth to death: dual functions of reactive oxygen species in seed physiology. Annals of Botany 116: 663–668.
- Kwak, J.M., Mori, I.C., Pei, Z.M. et al. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis . The EMBO Journal 22: 2623–2633.
- Limami, A.M., Diab, H., and Lothier, J. (2014). Nitrogen metabolism in plants under low oxygen stress. Planta 239: 531–541.
- López-Huertas, E., Corpas, F.J., Sandalio, L.M., and del Río, L.A. (1999). Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochemical Journal 337: 531–536.
- Ma, X., Wang, W., Bittner, F. et al. (2016). Dual and opposing roles of xanthine dehydrogenase in defense-associated reactive oxygen species metabolism in Arabidopsis . Plant Cell 28: 1108–1126.
- Marchi, S., Giorgi, C., Suski, J.M. et al. (2012). Mitochondria-ROS crosstalk in the control of cell death and aging. Journal of Signal Transduction 2012: 329635. https://doi.org/10.1155/2012/329635.
- Mathé, C., Barre, A., Jourda, C., and Dunand, C. (2010). Evolution and expression of class III peroxidases. Archives of Biochemistry and Biophysics 500: 58–65.
- Meng, Z., Meng, Z., Zhang, R. et al. (2015). Expression of the rice arginase gene OsARG in cotton influences the morphology and nitrogen transition of seedlings. PLoS One 10: e0141530.
- Mhamdi, A., Mauve, C., Gouia, H. et al. (2010). Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant, Cell and Environment 33: 1112–1123.
- Michels, P.A., Moyersoen, J., Krazy, H. et al. (2005). Peroxisomes, glyoxysomes and glycosomes. Molecular Membrane Biology 22: 133–145.
- Mignolet-Spruyt, L., Xu, E., Idänheimo, N. et al. (2016). Spreading the news: subcellular and organellar reactive oxygen species production and signalling. Journal of Experimental Botany 67: 3831–3844.
- Millar, T.M., Stevens, C.R., Benjamin, N. et al. (1998). Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Letters 427: 225–228.
- Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7: 405–410.
- Mittler, R. (2017). ROS are good. Trends in Plant Science 22: 11–19.
- Moche, M., Stremlau, S., Hecht, L. et al. (2010). Effect of nitrate supply and mycorrhizal inoculation on characteristics of tobacco root plasma membrane vesicles. Planta 23: 425–436.
- Modolo, L.V., Augusto, O., Almeida, I.M.G. et al. (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 Science 171: 34–40.
- Moller, I.M. (2001). Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52: 561–591.
-
Moucheshi, A.S., Pakniyat, H., Pirasteh-Anosheh, H., and Azooz, M.M. (2014). Role of ROS signaling molecule in plants. In: Oxidative Damage to Plants (ed. P. Ahmad), 585–620. The Netherland: Elsevier.
10.1016/B978-0-12-799963-0.00020-4 Google Scholar
- Murphy, M.P. (2009). How mitochondria produce reactive oxygen species. Biochemical Journal 47: 1–13.
- Navrot, N., Rouhier, N., Gelhaye, E., and Jacquot, J.P. (2007). Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiologia Plantarum 129: 185–195.
- Neve, E.P. and Ingelman-Sundberg, M. (2010). Cytochrome P450 proteins: retention and distribution from the endoplasmic reticulum. Current Opinion in Drug Discovery & Development 13: 78–85.
- Noctor, G., Arisi, A.C.M., Jouanin, L., and Foyer, C.H. (1999). Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. The Journal of Experimental Botany 50: 1157–1167.
- Noctor, G. and Foyer, C.H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49: 249–279.
- Noirot, E., Lherminier, J., Robert, F. et al. (2014). Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein. Journal of Experimental Botany 65: 5011–5022.
- Nühse, T.S., Bottrill, A.R., Jones, A.M.E., and Peck, S.C. (2007). Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanism of plant innate immune responses. The Plant Journal 51: 931–940.
- O'Brien, J.A., Daudi, A., Finch, P. et al. (2012). A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiology 158: 2013–2027.
- Ogasawara, Y., Kaya, H., Hiaroka, G. et al. (2008). Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. The Journal of Biological Chemistry 283: 8885–8892.
- Ozgur, R., Turkan, I., Uzilday, B., and Sekmen, A.H. (2014). Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana . Journal of Experimental Botany 65: 1377–1390.
- Palmieri, M.C., Lindermayr, C., Bauwe, H. et al. (2010). Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiology 152: 1514–1528.
- Passardi, F., Longet, D., Penel, C., and Dunand, C. (2004). The class III peroxidase multigenic family in rice ant its evolution in plants. Phytochemistry 65: 1879–1893.
- Pei, Z.M., Murata, Y., Benning, G., and Thomine, S. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734.
- Petřivalský M., Kubienová L., Tichá T., and Luhová L. (2015). S-nitrosoglutathione reductase: a key regulator of S-nitrosylation in plant development and stress responses. Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants, Series: Signaling and Communication in Plants, volume 23, 283–299, Springer International Publishing, ISBN 978–3–319-10078-4.
- Planchet, E., Jagadis Gupta, K., Sonoda, M., and Kaiser, W.M. (2005). Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant Journal 41: 732–743.
-
Planchet, E. and Kaiser, W.M. (2006). Nitric oxide production in plants. Plant Signaling & Behavior 2: 46–51.
10.4161/psb.1.2.2435 Google Scholar
- Prasad, A., Sedlářová, M., Kale, R.S., and Pospíšil, P. (2017). Lipoxygenase in singlet oxygen generation as a response to wounding: in vivo imaging in Arabidopsis thaliana . Scientific Reports 7: 9831. https://doi.org/10.1038/s41598-017-09758-1.
- Qi, J., Wang, J., Gong, Z., and Zhou, J.-M. (2017). Apoplastic ROS signaling in plant immunity. Current Opinion in Plant Biology 38: 92–100.
- Ramel, F., Birtic, S., Cuiné, S. et al. (2012). Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology 158: 1268–1287.
- Roach, T. and Krieger-Liszkay, A. (2014). Regulation of photosynthetic electron transport and photoinhibition. Current Protein and Peptide Science 15: 351–362.
- Rockel, P., Strube, F., Rockel, A. et al. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of Experimental Botany 53: 103–110.
- Romero-Puertas, M.C., Corpas, F.J., Sandalio, L.M. et al. (2006). Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytologist 170: 43–52.
- Sagi, M. and Fluhr, R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141: 336–340.
- Santolini, J., André, F., Jeandroz, S., and Wendehenne, D. (2017). Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63: 30–38.
- Schieber, M. and Chandel, N.S. (2014). ROS function in redox signaling and oxidative stress. Current Biology 24: R453–R462.
- Schopfer, P. (2001). Hydroxyl radical-induced cell wall loosening in vitro and in vivo: implications for control of elongation growth. The Plant Journal 28: 679–688.
- Schmitt, F.J., Renger, G., Friedrich, T. et al. (2014). Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochimica et Biophysica Acta 1837: 835–848.
- Schwarz, D.S. and Blower, M.D. (2016). The endoplasmic reticulum: structure, function and response to cellular signalling. Cellular and Molecular Life Sciences 73: 79–94.
- Shi, H., Ye, T., Chen, F. et al. (2013). Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation. Journal of Experimental Botany 64: 1367–1379.
- Shigeto, J. and Tsutsumi, Y. (2016). Diverse functions and reactions of class III peroxidases. New Phytologist 209: 1395–1402.
- Skovsen, E., Snyder, J.W., Lambert, J.D.C., and Ogilby, P.R. (2005). Lifetime and diffusion of singlet oxygen in a cell. The Journal of Physical Chemistry Letters 109: 8570–8573.
- Srivastava, S., Brychkova, G., Yarmolinsky, D. et al. (2017). Aldehyde oxidase 4 plays a critical role in delaying silique senescence by catalyzing aldehyde detoxification. Plant Physiology 173: 1977–1997.
- Stöhr, C., Strube, F., Marx, G. et al. (2001). A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212: 835–841.
- Stöhr, C. and Ullrich, W.R. (2002). Generation and possible roles of NO in plant roots and their apoplastic space. Journal of Experimental Botany 53: 2293–2303.
- Stöhr, C. and Stremlau, S. (2006). Formation and possible roles of nitric oxide in plant roots. Journal of Experimental Botany 57: 463–470.
- Suzuki, N., Miller, G., Morales, J. et al. (2001). Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14: 691–699.
- Suzuki, N., Koussevitzky, S., Mittler, R., and Miller, G. (2012). ROS and redox signaling in the response of plants to abiotic stress. Plant, Cell & Environment 35: 259–270.
- Šebela, M., Radová, A., Angelini, R. et al. (2001). FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Science 160: 197–207.
- Šírová, J., Sedlářová, M., Piterková, J. et al. (2011). The role of nitric oxide in the germination of plant seeds and pollen. Plant Science 181: 560–572.
- Thomas, D.D. (2015). Breathing new life into nitric oxide signaling: a brief overview of the interplay between oxygen and nitric oxide. Redox Biology 5: 225–233.
-
Tichá, T., Luhová, L., and Petřivalský, M. (2016). Functions and metabolism of S-nitrosothiols and S-nitrosylation of proteins in plants: the role of S-nitrosoglutathione reductase. In: Gasotransmitters in Plants: The Rise of a New Paradigm in Cell Signaling (ed. L. Lamattina), 175–200. Springer International Publishing 978-3-319-40713-5.
10.1007/978-3-319-40713-5_9 Google Scholar
- Tischner, R., Planchet, E., and Kaiser, W.M. (2004). Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana . FEBS Letters 576: 151–155.
- Tischner, R., Galli, M., Heimer, Y.M. et al. (2007). Interference with the citrulline-based nitric oxide synthase assay by argininosuccinate lyase activity in Arabidopsis extracts. The FEBS Journal 274: 4238–4245.
- Titus, D.E. and Becker, W.M. (1985). Investigation of glyoxysome-peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy. The Journal of Cell Biology 101: 1288–1299.
- Torres, M.A., Onouchi, H., Hamada, S. et al. (1998). Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). The Plant Journal 14: 365–370.
- Torres, M.A., Jones, J.D.G., and Dangl, J.L. (2006). Reactive oxygen species signalling in response to pathogens. Plant Physiology 141: 373–378.
- Tripathy, B.C. and Oelmüller, R. (2012). Reactive oxygen species generation and signaling in plants. Plant Signaling & Behavior 7: 1621–1633.
- Tun, N.N., Santa-Catarina, C., Begum, T. et al. (2006). Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiology 47: 346–354.
- Umbach, A.L., Fiorani, F., and Siedow, J.N. (2005). Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiology 139: 1806–1820.
- Vaahtera, L., Brosché, M., Wrzaczek, M., and Kangasjärvi, J. (2014). Specificity in ROS signalling and transcripts signatures. Antioxidants & Redox Signaling 21: 1422–1441.
- Van Breusegem, F., Bailey-Serres, J., and Mittler, R. (2008). Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiology 147: 978–984.
- Veitch, N.C. (2004). Structural determinants of plant peroxidase function. Phytochemistry Reviews 3: 3–18.
- Wang, B.L., Tang, X.Y., Cheng, L.Y. et al. (2010). Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytologist 7: 1112–1123.
- Werck-Reichhart, D. and Feyereisen, R. (2000). Cytochromes P450: a success story. Genome Biology 1: reviews3003.13003.9
- Wimalasekera, R., Tebartz, F., and Scherer, G.F.E. (2011). Polyamines, polyamine oxidases and nitricoxide in development, abiotic and biotic stresses. Plant Science 181: 593–603.
- Yamasaki, H. and Sakihama, Y. (2000). Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Letters 468: 89–92.
- Yergaliyev, T.M., Nurbekova, Z., Mukiyanova, G. et al. (2016). The involvement of ROS producing aldehyde oxidase in plant response to Tombusvirus infection. Plant Physiology and Biochemistry 109: 36–44.
- Yesbergenova, Z., Yang, G., Oron, E. et al. (2005). The plant Mo-hydroxylases aldehyde oxidase and xanthine dehydrogenase have distinct reactive oxygen species signatures and are induced by drought and abscisic acid. Plant Journal 42: 862–876.
- Yun, B.W., Feechan, A., Yin, M. et al. (2011). S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264–268.
- Zamocky, M., Furtmuller, P.G., and Obinger, C. (2008). Evolution of catalases from bacteria to humans. Antioxidants & Redox Signaling 10: 1527–1548.
- Zeeshan, H.M.A., Lee, G.H., Kim, H.-R., and Chae, H.-J. (2016). Endoplasmic reticulum stress and associated ROS. International Journal of Molecular Sciences 17: 327. https://doi.org/10.3390/ijms17030327.
- Zhou, F., Zhang, Z., Gregersen, P.L. et al. (1998). Molecular characterization of the oxalate oxidase involved in response of barley to the powdery mildew fungus. Plant Physiology 117: 33–41.
- Zhou, C., Liu, Z., Zhu, L. et al. (2016). Exogenous melatonin improves plant iron deficiency tolerance via increased accumulation of polyamine-mediated nitric oxide. International Journal of Molecular Sciences 17: pii: E1777.