What Do the Plant Mitochondrial Antioxidant and Redox Systems Have to Say Under Salinity, Drought, and Extreme Temperature?

  • F. SevillaEmail author
  • A. Jiménez
  • J. J. Lázaro


Mitochondria are ubiquitous organelles with a notable oxidative metabolism. They are a significant site of reactive oxygen species (ROS) production in plant cells, including superoxide (O2 •−) and H2O2. In addition to ROS, there are compelling indications that nitric oxide (NO) can be generated in this organelle by both reductive and oxidative pathways. ROS and reactive nitrogen species (RNS) play a key role in signaling but they can also be deleterious via oxidation of cell components when overproduced as a consequence of adverse conditions. The high production of ROS obligates mitochondria to be provided with a set of ROS-scavenging mechanisms. The first line of plant mitochondrial antioxidants is composed of superoxide dismutase and the enzymes of the ascorbate–glutathione cycle, which are not only able to scavenge ROS but also to repair cell damage and possibly serve as redox sensors. Besides direct control by antioxidants, mitochondrial ROS production is tightly controlled by multiple redundant systems affecting inner membrane potential such as NADPH-dependent dehydrogenases, alternative oxidase (AOX), and uncoupling proteins. In addition, the presence of specific protein families responsible for dithiol/disulfide exchange reactions such as the thioredoxin (Trx), peroxiredoxin (Prx), and sulfiredoxin (Srx) families in the mitochondria has been recently reported. These proteins are critically important under some abiotic stress conditions by controlling the cellular redox status of thiol groups of cysteinyl residues as well as acting as antioxidant defense mechanisms. Here, we summarize the insights of the involvement of this Trx–Prx–Srx system and the ASC–GSH cycle components in plant tolerance to abiotic stress, more specifically in salinity, drought, and extreme temperatures, as some of the most important unfavorable environmental conditions for plant yield and growth. In the plant response to stress, it seems that not only the antioxidant but also the redox systems are emerging as key components functioning in both redox sensing and signal transduction pathways.


Abiotic stress Antioxidants Drought Extreme temperatures Mitochondria Redox proteins RNS ROS Salinity Signaling 



This work was supported by MICINN (BFU2014-52452-P) and Séneca Foundation, Murcia, Spain (04553/GERM/06). The authors apologize to the scientists that are not cited because of space limitation and thank Phillip Thomas for correction of the written English in the manuscript.


  1. Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374PubMedCentralPubMedCrossRefGoogle Scholar
  2. Agrawal GK, Bourguignon J, Rolland N, Ephritikhine G, Ferro M, Jaquinod M, Alexiou KG, Chardot T, Chakraborty N, Jolivet P, Doonan JH, Rakwal R (2011) Plant organelle proteomics: collaborating for optimal cell function. Mass Spectrom Rev 30:772–853PubMedGoogle Scholar
  3. Andronis EA, Roubelakis-Angelakis KA (2010) Short-term salinity stress in tobacco leads to the onset of animal-like PCD hallmarks in planta in contrast to long-term stress. Planta 231:437–448PubMedCrossRefGoogle Scholar
  4. Armstrong AF, Badger MR, Day DA, Barthet MM, Smith PMC, Millar AH, Whelan J, Atkin OK (2008) Dynamic changes in the mitochondrial electron transport chain underpinning cold acclimation of leaf respiration. Plant Cell Environ 31:1156–1169PubMedCrossRefGoogle Scholar
  5. Arrigoni O, Dipierro S, Borranccino G (1981) Ascorbate free radical reductase: a key enzyme of the ascorbic acid system. FEBS Lett 125:242–244CrossRefGoogle Scholar
  6. Asada K (1999) The water-water cycle in chloroplast: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639PubMedCrossRefGoogle Scholar
  7. Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv 27:84–93PubMedCrossRefGoogle Scholar
  8. Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597PubMedCentralPubMedCrossRefGoogle Scholar
  9. Bachhawat AK, Thakur A, Kaur J, Zulkifli M (2013) Glutathione transporters. Biochim Biophys Acta 1830:3154–3164PubMedCrossRefGoogle Scholar
  10. Barranco-Medina S, López-Jaramillo FJ, Bernier-Villamor L, Sevilla F, Lázaro JJ (2006) Cloning, overexpression, purification and preliminary crystallographic studies of a mitochondrial type II peroxiredoxin from Pisum sativum. Acta Crystallogr F 62:696–698CrossRefGoogle Scholar
  11. Barranco-Medina S, Krell T, Finkemeier I, Sevilla F, Lazaro JJ, Dietz KJ (2007) Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxII F from Pisum sativum. Plant Physiol Biochem 45:729–739PubMedCrossRefGoogle Scholar
  12. Barranco-Medina S, Krell T, Bernier-Villamor L, Sevilla F, Lázaro JJ, Dietz KJ (2008a) Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF and formation of an ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J Exp Bot 59:3259–3269PubMedCentralPubMedCrossRefGoogle Scholar
  13. Barranco-Medina S, Kakorin S, Lázaro JJ, Dietz KJ (2008b) Thermodynamics of the dimmer-decamer transition of reduced human and plant 2-Cys peroxiredoxin. Biochemistry 47:7196–7204PubMedCrossRefGoogle Scholar
  14. 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
  15. Bartoli CG, Gómez F, Martínez DE, Guiamet JJ (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). J Exp Bot 55:1663–1669PubMedCrossRefGoogle Scholar
  16. Bartoli CG, Guiamet JJ, Kiddle G, Pastori GM, Cagno R, Theodoulou FL, Foyer CH (2005) Ascorbate content of wheat leaves is not determined by maximal L-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress. Plant Cell Environ 28:1073–1081CrossRefGoogle Scholar
  17. Beer SM, Taylor ER, Brown SE, Dahm CC, Costa NJ, Runswick MJ, Murphy MP (2004) Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant defense. J Biol Chem 279:47939–47951PubMedCrossRefGoogle Scholar
  18. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984PubMedCrossRefGoogle Scholar
  19. Boyer JS (1982) Plant productivity and environment. Science 218:443–448PubMedCrossRefGoogle Scholar
  20. Camejo D, Jiménez A, Alarcón JJ, Torres W, Gómez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities during heat shock treatment in tomato plants. Funct Plant Biol 33:177–187CrossRefGoogle Scholar
  21. Camejo D, Martí MC, Nicolás E, Alarcón JJ, Jiménez A, Sevilla F (2007) Response of superoxide dismutase isoenzymes in tomato plants (Lycopersicon esculentum) during thermo-acclimation of the photosynthetic apparatus. Physiol Planta 131:367–2007CrossRefGoogle Scholar
  22. Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteom 79:87–99CrossRefGoogle Scholar
  23. Camejo D, Ortiz-Espín A, Lázaro JJ, Romero-Puertas MC, Lázaro-Payo A, Sevilla F, Jiménez A (2015) Functional and structural changes in plant mitochondrial PrxIIF caused by NO. J Proteom 119:112–125CrossRefGoogle Scholar
  24. Campbell C, Atkinson L, Zaragoza-Castells J, Lundmark M, Atkin O, Hurry V (2007) Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group. New Phytol 176:375–389PubMedCrossRefGoogle Scholar
  25. Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulphur assimilation conundrum. Trends Plant Sci 18:18–29PubMedCrossRefGoogle Scholar
  26. Chang-Quan W, Rui-Chang L (2008) Enhancement of superoxide dismutase activity in the leaves of white clover (Trifolium repens L.) in response to polyethylene glycol-induced water stress. Acta Physiol Planta 30:841–847CrossRefGoogle Scholar
  27. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877PubMedCrossRefGoogle Scholar
  28. Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biophys Biochem Acta 1757:730–741Google Scholar
  29. Collins Y, Chouchani ET, James AM, Menger KE, Cochemé HM, Murphy MP (2012) Mitochondrial redox signaling at a glance. J Cell Sci 125:801–806PubMedCrossRefGoogle Scholar
  30. Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4Google Scholar
  31. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163PubMedCentralPubMedCrossRefGoogle Scholar
  32. Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39PubMedCrossRefGoogle Scholar
  33. Dat J, Foyer C, Scott I (1998) Change in salicylic acid and antioxidants during induced thermo tolerance in mustard seedlings. Plant Physiol 118:1455–1461PubMedCentralPubMedCrossRefGoogle Scholar
  34. Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM, Wiskich JT (1996) The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiol 110:1–2PubMedCentralPubMedGoogle Scholar
  35. del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11PubMedCrossRefGoogle Scholar
  36. 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 116:1195–1200PubMedCentralPubMedCrossRefGoogle Scholar
  37. 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
  38. Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159PubMedCentralPubMedCrossRefGoogle Scholar
  39. Edwards EA, Rawsthorne S, Mullineux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284PubMedCrossRefGoogle Scholar
  40. Edwards E, Enard C, Creissen GP, Mullineaux PM (1994) Synthesis and properties of glutathione reductase in stressed peas. Planta 192:137–143Google Scholar
  41. Elhafez D, Murcha MW, Clifton R, Soole KL, Day DA, Whelan J (2005) Characterisation of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant Cell Physiol 47:43–54PubMedCrossRefGoogle Scholar
  42. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Morishima I, Shibahara T, Inanaga S, Tanaka K (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Planta 127:57–65CrossRefGoogle Scholar
  43. Eyidogan F, Oz MT (2005) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29:485–493CrossRefGoogle Scholar
  44. Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336PubMedCrossRefGoogle Scholar
  45. Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450PubMedCrossRefGoogle Scholar
  46. Fernández-García N, Martí MC, Jiménez A, Sevilla F, Olmos E (2009) Sub-cellular distribution of glutathione in an Arabidopsis mutant (vtc1) deficient in ascorbate. J Plant Physiol 166:2004–2012PubMedCrossRefGoogle Scholar
  47. Filipovic MR, Stanic D, Raicevic S, Spasic M, Niketic V (2007) Consequences of MnSOD interactions with nitric oxide: nitric oxide dismutation and the generation of peroxynitrite and hydrogen peroxide. Free Radic Res 4:62–72CrossRefGoogle Scholar
  48. Filippou P, Antoniou C, Fotopoulos V (2011) Effect of drought and rewatering on the cellular status and antioxidant response of Medicago truncatula plants. Plant Signal Behav 6:270–277PubMedCentralPubMedCrossRefGoogle Scholar
  49. Finkemeier I, Goodman M, Lankemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180PubMedCrossRefGoogle Scholar
  50. Fiorani F, Umbach AL, Siedow JN (2005) The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 139:1795–1805PubMedCentralPubMedCrossRefGoogle Scholar
  51. Flexas J, Galmes J, Ribas-Carbo M, Medrano H (2005) The effects of water stress on plant respiration. In: Lambers H, Ribas-Carbó M (eds) Plant respiration: from cell to ecosystem. Springer, BerlinGoogle Scholar
  52. Flexas J, Bota J, Galmes J, Medrano H, Ribas-Carbo M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Planta 127:343–352CrossRefGoogle Scholar
  53. Florez-Sarasa ID, Bouma TJ, Medrano H, Azcon-Bieto J, Ribas-Carbó M (2007) Contribution of the cytochrome and alternative pathways to growth respiration and maintenance respiration in Arabidopsis thaliana. Physiol Planta 129:143–151CrossRefGoogle Scholar
  54. Foyer CH, Halliwell B (1976) Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25PubMedCrossRefGoogle Scholar
  55. Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905PubMedCrossRefGoogle Scholar
  56. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedCentralPubMedCrossRefGoogle Scholar
  57. Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18:2087–2090PubMedCrossRefGoogle Scholar
  58. Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 181:401–440PubMedCrossRefGoogle Scholar
  59. Galle A, Florez-Sarasa I, Thameur A, de Paepe R, Flexas J, Ribas-Carbó M (2010) Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant. J Exp Bot 61:765–775PubMedCentralPubMedCrossRefGoogle Scholar
  60. Gama O, Keech F, Eymery F, Finkemeier I, Gelhaye E, Gardeström P, Dietz KJ, Rey P, Jacquot JP, Rouhier N (2007) The mitochondrial type II peroxiredoxin from poplar. Physiol Plant 129:196–206CrossRefGoogle Scholar
  61. Gelhaye E, Rouhier N, Gerard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson P, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremei P, Meyer Y, Jacquot JP (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101:14545–14550PubMedCentralPubMedCrossRefGoogle Scholar
  62. Gelhaye E, Rouhier N, Navrot N, Jaquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35PubMedCrossRefGoogle Scholar
  63. Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol 147:595–610PubMedCentralPubMedCrossRefGoogle Scholar
  64. Gómez JM, Hernández JA, Jiménez A, del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Radic Res 31:S11–S18PubMedCrossRefGoogle Scholar
  65. Gómez JM, Jiménez A, Olmos E, Sevilla F (2004) Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. J Exp Bot 55:119–130PubMedCrossRefGoogle Scholar
  66. González-Meler MA, Ribas-Carbó M, Giles L, Siedow JN (1999) The effect of growth and measurement temperature on the activity of the alternative respiratory pathway. Plant Physiol 120:765–772PubMedCentralPubMedCrossRefGoogle Scholar
  67. Greetham D, Kritsiligkou P, Watkins RH, Carter Z, Parkin J, Grant CM (2013) Oxidation of the yeast mitochondrial thioredoxin promotes cell death. Antioxid Redox Sign 18:376–385CrossRefGoogle Scholar
  68. Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim G (1997) Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus. Planta 203:460–469PubMedCrossRefGoogle Scholar
  69. Gupta KJ, Igamberdiev AU, Manjunatha G, Segu S, Moran JF, Neelawarne B, Bauwe H, Kaiser WM (2011) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526PubMedCrossRefGoogle Scholar
  70. Guy RD, Vanlerberghe GC (2005) Partitioning of respiratory electrons in the dark in leaves of transgenic tobacco with modified levels of alternative oxidase. Physiol Planta 125:171–180CrossRefGoogle Scholar
  71. Hasanuzzaman M, Vahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684PubMedCentralPubMedCrossRefGoogle Scholar
  72. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499CrossRefGoogle Scholar
  73. Hernández JA, Corpas FJ, Gómez M, del Río LA, Sevilla F (1993) Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Planta 89:103–110CrossRefGoogle Scholar
  74. Hernández JA, Jiménez A, Mullineaux PM, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  75. Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2 ·−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831PubMedCentralPubMedCrossRefGoogle Scholar
  76. Hernández I, Cela J, Alegre L (2013) Antioxidant defenses against drought stress. In: Aroca R (ed) Plant responses to drought stress. Springer, BerlinGoogle Scholar
  77. Horling F, König J, Dietz KJ (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40:491–499CrossRefGoogle Scholar
  78. Horling F, Lamkemeyer P, König J, Finkemeier I, Kandlbinder A, Baier M, Dietz KJ (2003) Divergent light, ascorbate, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325PubMedCentralPubMedCrossRefGoogle Scholar
  79. Huerta-Ocampo JA, Briones-Cerecero EP, Mendoza-Hernández G, De León-Rodríguez A, Barba de la Rosa AP (2009) Proteomic analysis of Amaranth (Amaranthus hypochondriacus L.) leaves under drought stress. Int J Plant Sci 170:990–998CrossRefGoogle Scholar
  80. Igamberdiev AU, Ratcliffe RG, Gupta KJ (2014) Plant mitochondria: source and target for nitric oxide. Mitochondrion 19:329–333PubMedCrossRefGoogle Scholar
  81. Iglesias-Baena I, Barranco-Medina S, Lázaro-Payo A, López-Jaramillo FJ, Sevilla F, Lázaro JJ (2010) Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin. J Exp Bot 6:1509–1521CrossRefGoogle Scholar
  82. Iglesias-Baena I, Barranco-Medina S, Sevilla F, Lázaro JJ (2011) The dual targeted plant sulfiredoxin retroreduces the sulfinic form of atypical mitochondrial peroxiredoxin. Plant Physiol 155:944–955PubMedCentralPubMedCrossRefGoogle Scholar
  83. Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J Proteom Res 9:6595–6604CrossRefGoogle Scholar
  84. Jensen PK (1966) Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-transport particles. I. pH dependency and hydrogen peroxide formation. Biochim Biophys Acta 122:157–166PubMedCrossRefGoogle Scholar
  85. Jha UC, Bohra A, Singh NP (2014) Heat stress in crop plants: its nature, impacts and integrated breeding strategies to improve heat tolerance. Plant Breed 133:679–701CrossRefGoogle Scholar
  86. Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607PubMedCrossRefGoogle Scholar
  87. 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
  88. Jiménez A, Hernández JA, Ros Barceló A, Sandalio LM, Del Río LA, Sevilla F (1998a) Characterization of mitochondrial and peroxisomal ascorbate peroxidase of pea leaves. Physiol Planta 104:687–692CrossRefGoogle Scholar
  89. Jiménez A, Hernández JA, Pastori G, del Río LA, Sevilla F (1998b) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335PubMedCentralPubMedCrossRefGoogle Scholar
  90. Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P, Driscoll S, Vanacker H, Verrier P, Hancock RD, Foyer CH (2011) The transcription factor ABI4 Is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23:3319–3334PubMedCentralPubMedCrossRefGoogle Scholar
  91. Kido Y, Shiba T, Inaoka DK, Sakamoto K, Nara T, Aoki T, Honma T, Inoue M, Matsuoka S, Moore A, Harada S, Kita K (2010) Crystallization and preliminary crystallographic analysis of cyanide-insensitive alternative oxidase from Trypanosoma brucei. Acta Crystallogr F Struct Biol Cryst Commun 66:275–278CrossRefGoogle Scholar
  92. Kocsy G, Tari I, Vankova R, Zechmann B, Gulyas Z, Poor P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77–91PubMedCrossRefGoogle Scholar
  93. Koffler BE, Luschin-Ebengreuth N, Stabentheiner E, Müller M, Zechman B (2014) Compartment specific response of antioxidants to drought stress in Arabidopsis. Plant Sci 227:133–144PubMedCentralPubMedCrossRefGoogle Scholar
  94. Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167PubMedCrossRefGoogle Scholar
  95. Kubo A, Sano A, Saji H, Tanaka K, Kondo N, Tanaka K (1993) Primary structure and properties of glutathione reductase from Arabidopsis thaliana. Plant Cell Physiol 34:1259–1266Google Scholar
  96. Laloi C, Rayapuram N, Chartier Y, Grienenberger JM, Bonnard G, Meyer Y (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci USA 98:14144–14149PubMedCentralPubMedCrossRefGoogle Scholar
  97. Lambers H, Robinson SA, Ribas-Carbo M (2005) Regulation of respiration in vivo. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem, vol 18, Advances in photosynthesis and respiration series. Springer, AmsterdamCrossRefGoogle Scholar
  98. Lázaro JJ, Jiménez A, Camejo D, Iglesias-Baena I, Martí MC, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460PubMedCentralPubMedCrossRefGoogle Scholar
  99. Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159:75–85PubMedCrossRefGoogle Scholar
  100. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze. Nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458PubMedCrossRefGoogle Scholar
  101. Li W, Qi L, Lin X, Chen H, Ma Z, Wu K, Huang S (2009) The expression of manganese superoxide dismutase gene from Nelumbo nucifera responds strongly to chilling and oxidative stresses. J Integr Plant Biol 51:279–286PubMedCrossRefGoogle Scholar
  102. Lin KH, Pu SF (2010) Tissue- and genotype-specific ascorbate peroxidase expression in sweet potato in response to salt stress. Biol Plant 54:664–670CrossRefGoogle Scholar
  103. Liu XP, Liu XY, Zhang J, Xia ZL, Liu X, Qin HJ, Wang DW (2006) Molecular and functional characterization of sulfiredoxin homologs from higher plants. Cell Res 16:287–296PubMedCrossRefGoogle Scholar
  104. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620PubMedCrossRefGoogle Scholar
  105. Lopert P, Day BJ, Patel M (2012) Thioredoxin reductase deficiency potentiates oxidative stress, mitochondrial dysfunction and cell death in dopaminergic cells. PLOS One 7:e50683PubMedCentralPubMedCrossRefGoogle Scholar
  106. Maathuis FJM, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 5:467PubMedCentralPubMedCrossRefGoogle Scholar
  107. MacFarlane C, Hansen LD, Florez-Sarasa I, Ribas-Carbo M (2009) Plant mitochondria electron partitioning is independent of short-term temperature changes. Plant Cell Environ 32:585–591PubMedCrossRefGoogle Scholar
  108. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  109. Malone M (1993) Rapid inhibition of leaf growth by root cooling in wheat: kinetics and mechanism. J Exp Bot 44:1663–1669CrossRefGoogle Scholar
  110. Marques AT, Santos SP, Rosa MG, Rodrigues MAA, Abreu JA, Frazao C, Romao CV (2014) Expression, purification and crystallization of MnSOD from Arabidopsis thaliana. Acta Crystallogr 70:669–672Google Scholar
  111. Martí MC, Olmos E, Calvete JJ, Díaz I, Barranco-Medina S, Whelan J, Lázaro JJ, Sevilla F, Jiménez A (2009) Mitochondrial and nuclear localization of a novel pea thioredoxin: identification of its mitochondrial target proteins. Plant Physiol 150:646–657PubMedCentralPubMedCrossRefGoogle Scholar
  112. Martí MC, Florez-Sarasa, Camejo D, Ribas-Carbó M, Lázaro JJ, Sevilla F, Jiménez A (2011) Response of the mitochondrial antioxidant redox system and respiration to salinity in pea plants. J Exp Bot 62:3863–3874PubMedCentralPubMedCrossRefGoogle Scholar
  113. Martí MC, Florez-Sarasa I, Camejo D, Pallol B, Ortiz A, Ribas-Carbó M, Jiménez A, Sevilla F (2012) Response of mitochondrial antioxidant system and respiratory pathways to reactive nitrogen species in pea leaves. Physiol Planta 147:194–206CrossRefGoogle Scholar
  114. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276PubMedCentralPubMedCrossRefGoogle Scholar
  115. McDonald AE, Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Physiol Part D1:357–364Google Scholar
  116. McDonald AE, Vanlerberghe GC, Staples JF (2009) Alternative oxidase in animals: unique characteristics and taxonomic distribution. J Exp Biol 212:2627–2634PubMedCrossRefGoogle Scholar
  117. McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic Alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181PubMedCentralPubMedGoogle Scholar
  118. Metwally A, Safronova VI, Belimov AA, Dietz KJ (2005) Genotypic variation of the response to cadmium toxicity in Pisum sativum L. J Exp Bot 56:167–178PubMedGoogle Scholar
  119. Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C, Meyer Y (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160PubMedCrossRefGoogle Scholar
  120. Millar AH, Mittova V, Kiddle G, Heazlewood JL, Bartoli CG, Theodoulou FL, Foyer CH (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447PubMedCentralPubMedCrossRefGoogle Scholar
  121. Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104PubMedCrossRefGoogle Scholar
  122. Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5:2–15CrossRefGoogle Scholar
  123. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  124. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van BF (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309PubMedCrossRefGoogle Scholar
  125. Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856PubMedCrossRefGoogle Scholar
  126. Moller 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
  127. Moore AL, Shiba T, Young L, Harada S, Kita K, Ito K (2013) Unraveling the heater: new insights into the structure of the alternative oxidase. Annu Rev Plant Biol 64:637–663PubMedCrossRefGoogle Scholar
  128. Moran JF, Becana M, Iturbe-Ormaetxe I, Frechillam S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352CrossRefGoogle Scholar
  129. Morgan MJ, Lehmann M, Schwarzländer M, Baxter CJ, Sienkiewicz-Porzucek A, Williams TCR, Schauer N, Fernie AR, Fricker MD, Ratcliffe RG, Sweetlove LJ, Finkemeier I (2008) Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricarboxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol 147:101–114PubMedCentralPubMedCrossRefGoogle Scholar
  130. Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474PubMedCrossRefGoogle Scholar
  131. Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19PubMedCentralPubMedCrossRefGoogle Scholar
  132. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  133. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13PubMedCentralPubMedCrossRefGoogle Scholar
  134. Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134PubMedCrossRefGoogle Scholar
  135. Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484PubMedCrossRefGoogle Scholar
  136. Olmos E, Hernández JA, Sevilla F, Hellín E (1994) Induction of several antioxidant enzymes in the selection of a salt-tolerant cell-line of Pisum sativum. J Plant Physiol 144:594–598CrossRefGoogle Scholar
  137. Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 49:157–165CrossRefGoogle Scholar
  138. Preuss ML, Cameron JC, Berg RH, Jez JM (2014) Immunolocalization of glutathione biosynthesis enzymes in Arabidopsis thaliana. Plant Physiol Biochem 75:9–13PubMedCrossRefGoogle Scholar
  139. Pulido P, Cazalis R, Cejudo FJ (2009) An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. Plant J 57:132–145PubMedCrossRefGoogle Scholar
  140. Rasmusson AG, Moller IM (1991) NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial membrane studied using inside out submitochondrial particles. Physiol Planta 83:357–365CrossRefGoogle Scholar
  141. Rasmusson AG, Wallström SV (2010) Involvement of mitochondria in the control of plant cell NAD(P)H reduction levels. Biochem Soc Trans 38:661–666PubMedCrossRefGoogle Scholar
  142. Rasmusson AG, Fernie AR, van Dongen JT (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiol Planta 137:371–382CrossRefGoogle Scholar
  143. Rautenkranz A, Li L, Machler F, Martinoia E, Oertli JJ (1994) Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare L. cv Gerbel) leaves. Plant Physiol 106:187–193PubMedCentralPubMedGoogle Scholar
  144. Rey P, Becuwe N, Barrault MB, Rumeau D, Havaux M, Biteau B, Toledano MB (2007) The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505–514PubMedCrossRefGoogle Scholar
  145. Rhoads DM, Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7:177–194PubMedCrossRefGoogle Scholar
  146. Ribas-Carbó M, Berry JA, Yakir D, Giles L, Robinson SA, Lennon AM, Siedow JN (1995) Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiol 109:829–837PubMedCentralPubMedGoogle Scholar
  147. Ribas-Carbó M, Lennon AM, Robinson SA, Giles L, Berry J, Siedow JN (1997) The regulation of the electron partitioning between the cytochrome and alternative pathways in soybean cotyledon and root mitochondria. Plant Physiol 113:903–911PubMedCentralPubMedGoogle Scholar
  148. Ribas-Carbó M, Aroca R, Gonzàlez-Meler MA, Irigoyen JJ, Sánchez-Díaz M (2000) The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol 122:199–204PubMedCentralPubMedCrossRefGoogle Scholar
  149. Ribas-Carbó M, Robinson SA, Giles L (2005a) The application of the oxygen-isotope technique to assess respiratory pathway partitioning. In: Lambers H, Ribas-Carbó M (eds) Advances in photosynthesis and respiration. Plant respiration: from cell to ecosystem. Springer, AmsterdamGoogle Scholar
  150. Ribas-Carbó M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J (2005b) Effects of water stress on respiration in soybean leaves. Plant Physiol 139:466–473PubMedCentralPubMedCrossRefGoogle Scholar
  151. Rich PR, Bonner WD Jr (1978) The sites of superoxide anion generation in higher plant mitochondria. Arch Biochem Biophys 188:206–213PubMedCrossRefGoogle Scholar
  152. Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, Del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243PubMedCentralPubMedCrossRefGoogle Scholar
  153. Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM (2013) Protein S-nitrosylation in plants under abiotic stress: an overview. Front Plant Sci 20:373Google Scholar
  154. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126PubMedGoogle Scholar
  155. Sanz-Barrio R, Fernández-San Millán A, Carballeda J, Corral-Martínez P, Seguí-Simarro JM, Farran I (2012) Chaperone-like properties of tobacco plastid thioredoxins f and m. J Exp Bot 63:365–379PubMedCentralPubMedCrossRefGoogle Scholar
  156. Schmitt FJ, Renger G, Friedrich T, Kreslavksi VD, Zharmukhadmedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837:385–848CrossRefGoogle Scholar
  157. Schnaubelt D, Schulz P, Hannah MA, Yocgo RE, Foyer CH (2013) A phenomics approach to the analysis of the influence of glutathione on leaf area and abiotic stress tolerance in Arabidopsis thaliana. Front Plant Sci 4:416PubMedCentralPubMedCrossRefGoogle Scholar
  158. Searle SY, Turnbull MH (2011) Seasonal variation of leaf respiration and the alternative pathway in field-grown Populus × canadensis. Physiol Planta 141:332–342CrossRefGoogle Scholar
  159. Selote DS, Khanna-Chopra R (2010) Antioxidant response of wheat roots to drought acclimation. Protoplasma 245:153–163PubMedCrossRefGoogle Scholar
  160. Serrato AJ, Pérez-Ruiz JM, Spínola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279:43821–43827PubMedCrossRefGoogle Scholar
  161. Sevilla F, López-Gorgé J, del Río LA (1982) Characterization of a manganese superoxide dismutase from the higher plant Pisum sativum. Plant Physiol 70:1321–1326PubMedCentralPubMedCrossRefGoogle Scholar
  162. Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) Thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by ROS and RNS. J Exp Bot. doi: 10.1093/jxb/erv146 PubMedGoogle Scholar
  163. Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864PubMedCrossRefGoogle Scholar
  164. Shiriga K, Sharma R, Kumar K, Yadav SK, Hossain F, Thirunavukkarasu N (2014) Expression pattern of superoxide dismutase under drought stress in maize. Int J Innov Res Sci Eng Technol 3:11333–11337Google Scholar
  165. Song XS, Hu WH, Mao WH, Ogweno JO, Zhou YH, Yu JQ (2005) Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. Plant Physiol Biochem 43:1082–1088PubMedCrossRefGoogle Scholar
  166. Stevens RG, Creissen GP, Mullineaux PM (1997) Cloning and characterisation of a cytosolic glutathione reductase cDNA from pea (Pisum sativum L.) and its expression in response to stress. Plant Mol Biol 35:641–654PubMedCrossRefGoogle Scholar
  167. Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31:1086–1096PubMedCrossRefGoogle Scholar
  168. Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474PubMedCrossRefGoogle Scholar
  169. Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904PubMedCrossRefGoogle Scholar
  170. Szarka A, Horemans N, Kovacs Z, Gróf P, Mayer M, Bánhegyi G (2007) Dehydroascorbate reduction in plant mitochondria is coupled to the respiratory electron transfer chain. Physiol Planta 129:225–232CrossRefGoogle Scholar
  171. Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3:207–219CrossRefGoogle Scholar
  172. Talla S, Riazunnisa K, Padmavathi L, Sunil B, Rajsheel P, Raghavendra AS (2011) Ascorbic acid is a key participant during the interactions between chloroplasts and mitochondria to optimize photosynthesis and protect against photoinhibition. J Biosci 36:163–173PubMedCrossRefGoogle Scholar
  173. Tan YF, O’Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol 152:747–761PubMedCentralPubMedCrossRefGoogle Scholar
  174. Tan M, Lu J, Zhang A, Hu B, Zhu X, Li W (2011) The distribution and cooperation of antioxidant (iso)enzymes and antioxidants in different subcellular compartments in maize leaves during water stress. J Plant Grow Regul 30:255–271CrossRefGoogle Scholar
  175. Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteom 72:367–378CrossRefGoogle Scholar
  176. Trono D, Flagella Z, Laus MN, Di Fonzo N, Pastore D (2004) The uncoupling protein and the potassium channel are activated by hyperosmotic stress in mitochondria from durum wheat seedlings. Plant Cell Environ 27:437–448CrossRefGoogle Scholar
  177. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol (Lond) 552:335–344CrossRefGoogle Scholar
  178. Umbach AL, Fiorani F, Siedow JN (2005) Characterization of transformed Arabidopsis with altered alternative oxidase levels and analysis of effects on reactive oxygen species in tissue. Plant Physiol 139:1806–1820PubMedCentralPubMedCrossRefGoogle Scholar
  179. Umbach AL, Lacey EP, Richter SJ (2009) Temperature-sensitive alternative oxidase protein content and its relationship to floral reflectance in natural Plantago lanceolata populations. New Phytol 181:662–671PubMedCrossRefGoogle Scholar
  180. Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184PubMedCrossRefGoogle Scholar
  181. Van Breusegem F, Slooten L, Stassart JM, Botterman J, Monees T, Van Montagu M, Inze D (1999) Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. J Exp Bot 50:71–78CrossRefGoogle Scholar
  182. Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847PubMedCentralPubMedCrossRefGoogle Scholar
  183. Vassileva V, Simova-Stoilova L, Demirevska K, Feller U (2009) Variety-specific response of wheat (Triticum aestivum L.) leaf mitochondria to drought stress. J Plant Res 122:445–454PubMedCrossRefGoogle Scholar
  184. Vidal G, Ribas-Carbó M, Garmier M, Dubertret G, Rasmusson AG, Mathieu C, Foyer CH, De Paepe R (2007) Lack of respiratory chain complex I impairs alternative oxidase engagement and modulates redox signalling during elicitor-induced cell death in tobacco. Plant Cell 19:640–655PubMedCentralPubMedCrossRefGoogle Scholar
  185. Vidigal P, Carvalho R, Amancio S, Carvalho L (2013) Peroxiredoxins are involved in two independent signalling pathways in the abiotic stress protection in Vitis vinifera. Biol Planta 57:675–683CrossRefGoogle Scholar
  186. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223CrossRefGoogle Scholar
  187. Wang YH, Ying Y, Vhen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677CrossRefGoogle Scholar
  188. Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472PubMedCrossRefGoogle Scholar
  189. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631PubMedCrossRefGoogle Scholar
  190. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395PubMedCrossRefGoogle Scholar
  191. Wu G, Wilen RW, Robertson AJ, Gusta LV (1999) Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120:513–520PubMedCentralPubMedCrossRefGoogle Scholar
  192. Xie G, Kato H, Sasaki K, Imai R (2009) A cold-induced thioredoxin h of rice, OsTrx23, negatively regulates kinase activities of OsMPK3 and OsMPK6 in vitro. FEBS Lett 583:2734–2738PubMedCrossRefGoogle Scholar
  193. Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285CrossRefGoogle Scholar
  194. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156PubMedCrossRefGoogle Scholar
  195. Zaffagnini M, Bedhomme M, Marchand CH, Morisse S, Trost P, Lemaire SD (2012) Redox regulation in photosynthetic organisms: focus on glutathionylation. Antioxid Redox Signal 16:567–586PubMedCrossRefGoogle Scholar
  196. Zechmann B (2014) Compartment-specific importance of glutathione during abiotic and biotic stress. Front Plant Sci 5:566PubMedCentralPubMedCrossRefGoogle Scholar
  197. Zechmann B, Müller M (2010) Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 246:15–24PubMedCentralPubMedCrossRefGoogle Scholar
  198. Zechmann B, Stumpe M, Mauch F (2011) Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta 233:1–12PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Stress Biology and Plant PathologyCEBAS-CSICMurciaSpain
  2. 2.Department of Biochemistry, Cellular and Molecular Biology of PlantsEEZ-CSICGranadaSpain

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