Production Sites of Reactive Oxygen Species (ROS) in Organelles from Plant Cells

  • Francisco J. CorpasEmail author
  • Dharmendra K. Gupta
  • José M. PalmaEmail author


Reactive oxygen species (ROS) have been considered for a long time as undesirable by-product of the cellular metabolism, but recently the role of ROS in molecular signaling processes has been reported. Consequently, the cell must keep a fragile equilibrium between ROS production and the antioxidant defenses that protect cells in vivo against potential damages (oxidative stress) and, alternatively, allow the inter- and intra-cell communications. This equilibrium may become disturbed under different array of adverse conditions by an excessive generation of ROS or by an impaired antioxidant defenses. Plant cells have a compartmentalization of ROS production in the different organelles including chloroplasts, mitochondria, or peroxisomes, and they also have a complex battery of antioxidant enzymes usually close to the site of ROS production. Cell compartmentalization has been demonstrated to be an additional mechanism of cellular ROS modulation for signaling purposes. This chapter will provide a general overview of the main system of ROS production/regulation in plant cells.


Reactive oxygen species Chloroplasts Mitochondria Peroxisomes 



Work in our laboratories is supported by ERDF grants co-financed by the Ministry of Economy and Competitiveness (projects AGL2011-26044, BIO2012-33904) and the Junta de Andalucía (group BIO192) in Spain.


  1. Adams WW, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186:390–398PubMedCrossRefGoogle Scholar
  2. Arent S, Pye VE, Henriksen A (2008) Structure and function of plant acyl-CoA oxidases. Plant Physiol Biochem 46:292–301PubMedCrossRefGoogle Scholar
  3. Asada K, Kiso K, Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249:2175–2181PubMedGoogle Scholar
  4. Asada K (1992) Production and scavenging of active oxygen in chloroplasts. In: Scandalios JG (ed) Molecular biology of free radical scavenging system. Cold Spring Harbor Laboratory Press, Plainview, NY, pp 173–192Google Scholar
  5. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedCentralPubMedCrossRefGoogle Scholar
  6. Baker A, Paudyal R (2014) The life of the peroxisome: from birth to death. Curr Opin Plant Biol 22:39–47PubMedCrossRefGoogle Scholar
  7. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341PubMedCentralPubMedCrossRefGoogle Scholar
  9. Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598PubMedCentralPubMedCrossRefGoogle Scholar
  10. Corpas FJ, Barroso JB (2014) NADPH-generating dehydrogenases: their role in the mechanism of protection against nitro-oxidative stress induced by adverse environmental conditions. Front Environ Sci 2:55CrossRefGoogle Scholar
  11. Corpas FJ, Trelease RN (1998) Differential expression of ascorbate peroxidase and a putative molecular chaperone in the boundary membrane of differentiating cucumber seedling peroxisomes. J Plant Physiol 153:332–338CrossRefGoogle Scholar
  12. 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 6:145–50PubMedCrossRefGoogle Scholar
  13. Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, del Río LA (2008) peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165:1319–1330PubMedCrossRefGoogle Scholar
  14. Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126PubMedCentralPubMedGoogle Scholar
  15. Corpas FJ, Begara-Morales JC, Sánchez-Calvo B, Chaki M, Barroso JB (2015) Nitration and S-nitrosylation: two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) which participate in signaling processes of plant cells. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signalling and communication in plants. Springer, BerlinGoogle Scholar
  16. Daudi A, Cheng Z, O’Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287PubMedCentralPubMedCrossRefGoogle Scholar
  17. Demmig-Adams B, Adams W (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21PubMedCrossRefGoogle Scholar
  18. del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11PubMedCrossRefGoogle Scholar
  19. del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837Google Scholar
  20. del Río LA, Lyon DS, Olah I, Glick B, Salin ML (1983) Immunocytochemical evidence for a peroxisomal localization of manganese superoxide dismutase in leaf protoplasts from a higher plant. Planta 158:216–224PubMedCrossRefGoogle Scholar
  21. del Río LA, Fernández VM, Rupérez FL, Sandalio LM, Palma JM (1989) NADH induces the generation of superoxide radicals in leaf peroxisomes. Plant Physiol 89:728–31PubMedCentralPubMedCrossRefGoogle Scholar
  22. 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 53:1255–1272PubMedCrossRefGoogle Scholar
  23. Delker C, Zolman BK, Miersch O, Wasternack C (2007) Jasmonate biosynthesis in Arabidopsis thaliana requires peroxisomal β-oxidation enzymes-additional proof by properties of pex6 and aim1. Phytochemistry 68:1642–1650PubMedCrossRefGoogle Scholar
  24. Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Physiol Plant Mol Biol 54:93–107CrossRefGoogle Scholar
  25. Droillard MJ, Paulin A (1990) Isozymes of superoxide dismutase in mitochondria and peroxisomes isolated from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiol 94:1187–1192PubMedCentralPubMedCrossRefGoogle Scholar
  26. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  27. Foyer CH, Lelandais M, Edwards EA, Mullineaux PM (1991) The role of ascorbate in plants, interaction with photosynthesis, and regulatory significance. In: Pell E, Steffen K (eds) Active oxygen/oxidative stress and plant metabolism. American Society of Plant Physiologists, Rockville, pp 131–143Google Scholar
  28. Foyer CH, Lescure JC, Lefebvre C, Morot-Gaudry JF, Vincentz M, Vaucheret H (1994) Adaptations of photosynthetic electron transport, carbon assimilation, and carbon partitioning in transgenic Nicotiana plumbaginifolia plants to changes in nitrate reductase activity. Plant Physiol 104:171–178Google Scholar
  29. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  30. Goyer A, Johnson TL, Olsen LJ, Collakova E, Shachar-Hill Y, Rhodes D, Hanson AD (2004) Characterization and metabolic function of a peroxisomal sarcosine and pipecolate oxidase from Arabidopsis. J Biol Chem 279:16947PubMedCrossRefGoogle Scholar
  31. Grace SC (1990) Phylogenetic distribution of superoxide dismutase supports an endosymbiotic origin for chloroplasts and mitochondria. Life Sci 47:1875–86PubMedCrossRefGoogle Scholar
  32. Gupta KJ, Igamberdiev AU (2015) Compartmentalization of reactive oxygen species and nitric oxide production in plant cells: an overview. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. Springer International Publishing, Switzerland, pp 1–14Google Scholar
  33. Hänsch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR (2006) Plant sulfite oxidase as novel producer of H2O2: combination of enzyme catalysis with a subsequent non-enzymatic reaction step. J Biol Chem 281:6884–6888PubMedCrossRefGoogle Scholar
  34. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedCentralPubMedCrossRefGoogle Scholar
  35. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, Oxford, UKGoogle Scholar
  36. Harrison R (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33:774–797PubMedCrossRefGoogle Scholar
  37. Hayakawa T, Kanematsu S, Asada K (1984) Occurrence of CuZn-superoxide dismutase in the intrathylakoid space of spinach chloroplasts. Plant Cell Physiol 25:883–889Google Scholar
  38. Hebelstrup KH, Møller I (2015) Mitochondrial signaling in plants under hypoxia: use of reactive oxygen species (ROS) and reactive nitrogen species (RNS). In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. Springer International Publishing, Switzerland, pp 63–77Google Scholar
  39. Hideg E, Kalai T, Hideg K, Vass I (1998) Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37:11405–11411PubMedCrossRefGoogle Scholar
  40. Hinkle PC, Butow RA, Rackers E (1967) Partial resolution of the enzymes catalyzing oxidative phosphorylation. XV Reverse electron transfer in the flavin-cytochrome b region of the respiratory chain of beef heart submitochondrial particles. J Biol Chem 242:5169–5173PubMedGoogle Scholar
  41. Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303PubMedCentralPubMedCrossRefGoogle Scholar
  42. Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284PubMedCentralPubMedGoogle Scholar
  43. Jiménez A, Hernández JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335PubMedCentralPubMedCrossRefGoogle Scholar
  44. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JD, Shirasu K, Menke F, Jones A, Zipfel C (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55PubMedCrossRefGoogle Scholar
  45. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282PubMedCrossRefGoogle Scholar
  46. Kaur G, Sharma A, Guruprasad K, Pati PK (2014) Versatile roles of plant NADPH oxidases and emerging concepts. Biotechnol Adv 32:551–563PubMedCrossRefGoogle Scholar
  47. Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080PubMedCentralPubMedCrossRefGoogle Scholar
  48. Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080PubMedCentralPubMedCrossRefGoogle Scholar
  49. Kukavica B, Vucinić Z, Vuletić M (2005) Superoxide dismutase, peroxidase, and germin-like protein activity in plasma membranes and apoplast of maize roots. Protoplasma 226:191–197PubMedCrossRefGoogle Scholar
  50. Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, del Río LA (2005) Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123PubMedCentralPubMedCrossRefGoogle Scholar
  51. Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914PubMedCrossRefGoogle Scholar
  52. López-Huertas E, Corpas FJ, Sandalio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536PubMedCentralPubMedCrossRefGoogle Scholar
  53. Loschen G, Azzi A (1975) On the formation of hydrogen peroxide and oxygen radicals in heart mitochondria. Recent Adv Stud Cardiac Struct Metab 7:3–12Google Scholar
  54. Mano S, Nishimura M (2005) Plant peroxisomes. Vitam Horm 72:111–154PubMedCrossRefGoogle Scholar
  55. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15PubMedCrossRefGoogle Scholar
  56. Martí MC, Camejo D, Olmos E, Sandalio LM, Fernández-García N, Jiménez A, Sevilla F (2009) Characterisation and changes in the antioxidant system of chloroplasts and chromoplasts isolated from green and mature pepper fruits. Plant Biol 11:613–624PubMedCrossRefGoogle Scholar
  57. Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51:190–200PubMedCrossRefGoogle Scholar
  58. Mateos RM, León AM, Sandalio LM, Gómez M, del Río LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterisation and antioxidant activity. J Plant Physiol 160:1507–1516PubMedCrossRefGoogle Scholar
  59. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276PubMedCentralPubMedCrossRefGoogle Scholar
  60. Mehler AH (1951) Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. Arch Biochem Biophys 34(2):339–351PubMedCrossRefGoogle Scholar
  61. Mittova V, Volokita M, Guy M (2015) Antioxidative systems and stress tolerance: insights from wild and cultivated tomato species. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. Springer International Publishing, Switzerland, pp 89–131Google Scholar
  62. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591PubMedCrossRefGoogle Scholar
  63. Muller M, Hernández I, Alegre L, Munné-Bosch S (2006) Enhanced alpha-tocopherol quinone levels and xanthophyll cycle de-epoxidation in rosemary plants exposed to water deficit during a Mediterranean winter. J Plant Physiol 163:601–606PubMedCrossRefGoogle Scholar
  64. Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042PubMedCrossRefGoogle Scholar
  65. Nikkanen L, Rintamäki E (2014) Thioredoxin-dependent regulatory networks in chloroplasts under fluctuating light conditions. Phil Trans R Soc B 369:20130224Google Scholar
  66. O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779PubMedCrossRefGoogle Scholar
  67. Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río LA (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57:1747–58PubMedCrossRefGoogle Scholar
  68. Palma JM, Corpas FJ, del Río LA (2009) Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9:2301–2312PubMedCrossRefGoogle Scholar
  69. Palma JM, Gupta DK, Corpas FJ (2013) Metalloenzymes involved in the metabolism of reactive oxygen species and heavy metal stress. In: Gupta DK, Corpas FJ, Palma JM (eds) Heavy metal stress in plants. Springer, BerlinGoogle Scholar
  70. Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–344PubMedCentralPubMedCrossRefGoogle Scholar
  71. Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6:379–389PubMedCrossRefGoogle Scholar
  72. Planas-Portell J, Gallart M, Tiburcio AF, Altabella T (2013) Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol 13:109PubMedCentralPubMedCrossRefGoogle Scholar
  73. Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK (2006) Peroxisomal β-oxidation-a metabolic pathway with multiple functions. Biochim Biophys Acta 1763:1413–1426PubMedCrossRefGoogle Scholar
  74. Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462PubMedCentralPubMedCrossRefGoogle Scholar
  75. Popov VN (2015) Feedback loop of non-coupled respiration and reactive oxygen species production in plant mitochondria. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communications in plants. Springer International Publishing, Switzerland, pp 79–88Google Scholar
  76. Pruzinska A, Tanner G, Aubry S, Anders I, Moser S, Muller T, Ongania K-H, Krautler B, Youn J-Y, Liljegren SL et al (2005) Chlorophyll breakdown in senescent Arabidopsis leaves: characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139:52–63PubMedCentralPubMedCrossRefGoogle Scholar
  77. Puerto-Galán L, Pérez-Ruiz JM, Ferrández J, Cano B, Naranjo B, Nájera VA, González M, Lindahl AM, Cejudo FJ (2013) Overoxidation of chloroplast 2-Cys peroxiredoxins: balancing toxic and signaling activities of hydrogen peroxide. Front Plant Sci 4:310PubMedCentralPubMedCrossRefGoogle Scholar
  78. Raha S, Robinson BH (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25:502–508PubMedCrossRefGoogle Scholar
  79. Reumann S, Corpas FJ (2010) The peroxisomal ascorbate-glutathione pathway: molecular identification and insights into its essential role under environmental stress conditions. In: Anjum NA, Umar S, Chan MT (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, BerlinGoogle Scholar
  80. Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366PubMedCentralPubMedCrossRefGoogle Scholar
  81. Rodríguez-Serrano M, Romero-Puertas MC, Pastori GM, Corpas FJ, Sandalio LM, del Río LA, Palma JM (2007) Peroxisomal membrane manganese superoxide dismutase: characterization of the isozyme from watermelon cotyledons. J Exp Bot 58:2417–2427PubMedCrossRefGoogle Scholar
  82. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodríguez-Serrano M, del Río LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52PubMedCrossRefGoogle Scholar
  83. Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340PubMedCentralPubMedCrossRefGoogle Scholar
  84. Sandalio LM, Fernández VM, Rupérez FL, del Río LA (1988) Superoxide free radicals are produced in glyoxysomes. Plant Physiol 87:1–4PubMedCentralPubMedCrossRefGoogle Scholar
  85. Schürman P, Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51:371–400CrossRefGoogle Scholar
  86. Schwarz G, Mendel RR (2006) Molybdenum cofactor biosynthesis and molybdenum enzymes. Annu Rev Plant Biol 57:623–647PubMedCrossRefGoogle Scholar
  87. Shi YC, Fu YP, Liu WQ (2012) NADPH oxidase in plasma membrane is involved in stomatal closure induced by dehydroascorbate. Plant Physiol Biochem 51:26–30PubMedCrossRefGoogle Scholar
  88. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319PubMedCrossRefGoogle Scholar
  89. Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FM (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci Signal 7(320):ra33PubMedCrossRefGoogle Scholar
  90. Skelly MJ, Loake GJ (2013) Synthesis of redox-active molecules and their signaling functions during the expression of plant disease resistance. Antioxid Redox Signal 19:990–997PubMedCentralPubMedCrossRefGoogle Scholar
  91. Smirnoff N (2001) L-ascorbic acid biosynthesis. Vitam Horm 61:241–266PubMedCrossRefGoogle Scholar
  92. Stöhr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293–2303PubMedCrossRefGoogle Scholar
  93. Streller S, Schinkel H, Wingsle G (1997) Apoplasmic CuZn-superoxide dismutase in Pinus sylvestris. Phyton Ann Rei Bot 37:271–276Google Scholar
  94. Sweetlove LJ, Foyer CH (2004) Roles for reactive oxygen species and antioxidants in plant mitochondria. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function, vol 1, Advances in photosynthesis and respiration. Kluwer Academic, DordrechtGoogle Scholar
  95. Telfer A, Dhami S, Bishop SM, Phillips D, Barber J (1994) Beta-carotene quenches singlet oxygen formed by isolated Photosystem-II reaction centers. Biochemistry 33:14469–14474PubMedCrossRefGoogle Scholar
  96. Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522PubMedCentralPubMedCrossRefGoogle Scholar
  97. Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633PubMedCentralPubMedCrossRefGoogle Scholar
  98. Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577PubMedCrossRefGoogle Scholar
  99. Vanacker H, Carver TL, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114PubMedCentralPubMedCrossRefGoogle Scholar
  100. Vanacker H, Foyer CH, Carver TLW (1999) Changes in apoplastic antioxidants induced by powdery mildew attack in oat genotypes with race non-specific resistance. Planta 208:444–452CrossRefGoogle Scholar
  101. Veljovic-Jovanovic S, Oniki T, Takaham U (1998) Detection of Monodehydroascorbic acid radical in sulfite-treated leaves and mechanism of its formation. Plant Cell Physiol 39:1203–1208CrossRefGoogle Scholar
  102. Wagner DE, Przybyla D, op den Camp RG, Kim C, Landgraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185PubMedCrossRefGoogle Scholar
  103. Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692PubMedCentralPubMedCrossRefGoogle Scholar
  104. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–4034PubMedCentralPubMedCrossRefGoogle Scholar
  105. Yoshie Y, Goto K, Takai R, Iwano M, Takayama S, Isogai A, Che FS (2005) Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses. Plant Biotechnol 22:127–135CrossRefGoogle Scholar
  106. Yoshimura K, Yabuta Y, Tamoi M, Ishikawa T, Shigeoka S (1999) Alternatively spliced mRNA variants of chloroplast ascorbate peroxidase isoenzymes in spinach leaves. Biochem J 338(Pt 1):41–48PubMedCentralPubMedCrossRefGoogle Scholar
  107. Yun BW, Feechan A, Yin M, Saidi NB, 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 478:264–268PubMedCrossRefGoogle Scholar
  108. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Department of Biochemistry, Cell and Molecular Biology of PlantsEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Institut für Radioökologie und Strahlenschutz (IRS)Gottfried Wilhelm Leibniz Universität HannoverHannoverGermany

Personalised recommendations