Skip to main content

Redox State in Plant Mitochondria and its Role in Stress Tolerance

  • Chapter
  • First Online:
Redox State as a Central Regulator of Plant-Cell Stress Responses

Abstract

Redox state in plant mitochondria is a key factor regulating metabolism of the plant cell and generating signalling cascades in response to abiotic and biotic stress, light regime, and cell differentiation. While the NAD pool plays primarily role in energy production, the internal mitochondrial NADP pool, which represents 20–25 % of the NAD pool, is important for the regulation of metabolic processes associated with mitochondria. The reduction level of NADP is the main factor regulating via thioredoxin the activities of several enzymes of the tricarboxylic acid cycle, the alternative oxidase, and other proteins. The NADPH/NADP+ ratio in the matrix is controlled by NADP-dependent isocitrate dehydrogenase, by the non-proton-translocating transhydrogenase reaction, and by the oxidation via Ca2+-dependent NADPH dehydrogenase. The mitochondrial redox state regulates the transport in and out of the organelle, balancing redox reactions in other compartments. This is achieved, in particular, via the operation of malate and citrate valves. The efflux of citrate provides the carbon skeletons for transamination and for ammonia refixation during photorespiration. The consequence of an increased redox state of NAD(H) and NADP(H) pools in mitochondria is the formation of reactive oxygen species, via leakage of electrons from the electron transport chain, and of NO, by using nitrite as an alternative electron acceptor under oxygen deficiency. It is concluded that the mitochondrial redox state is a central regulator of plant metabolism and a trigger of signalling cascades in response to stress and during plant development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radic Res 50:291–303

    Article  CAS  PubMed  Google Scholar 

  • Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909–9918

    Article  CAS  PubMed  Google Scholar 

  • Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schürmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Nat Acad Sci U S A 101:2642–2647

    Article  CAS  Google Scholar 

  • Bardel J, Louwagie M, Jaquinod M, Jourdain A, Luche S, Rabilloud T, Macherel D, Garin J, Bourguignon J (2002) A survey of the plant mitochondrial proteome in relation to development. Proteomics 2:880–898

    Article  CAS  PubMed  Google Scholar 

  • 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 123:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basu S, Azarova NA, Font MD, King SB, Hogg N, Gladwin MT, Shiva S, Kim-Shapiro DB (2008) Nitrite reductase activity of cytochrome c. J Biol Chem 283:32590–32597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beeckmans S, Van Driessche E, Kanarek L (1990) Clustering of sequential enzymes in the glycolytic pathway and the citric acid cycle. J Cell Biochem 43:297–306

    Article  CAS  PubMed  Google Scholar 

  • Blair JM (1969) Magnesium and the aconitase equilibrium: determination of apparent stability constants of magnesium substrate complexes from equilibrium data. Eur J Biochem 8:287–291

    Google Scholar 

  • Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Planta 138:447–462

    Article  CAS  Google Scholar 

  • Bölter B, Soll J (2001) Ion channels in the outer membranes of chloroplasts and mitochondria: open doors or regulated gates? EMBO J 20:935–940

    Article  PubMed  PubMed Central  Google Scholar 

  • Borisjuk L, Macherel D, Benamar A, Wobus U, Rolletschek H (2007) Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol 176:813–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botrel A, Magne C, Kaiser WM (1996) Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34:645–652

    CAS  Google Scholar 

  • Brouwer KS, van Valen T, Day DA, Lambers H (1986) Hydroxamate-stimulated O2 uptake in roots of Pisum sativum and Zea mays, mediated by a peroxidase: its consequences for respiration measurements. Plant Physiol 82:236–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bucher M, Brändle R, Kuhlemeier C (1994) Ethanolic fermentation in transgenic tobacco expressing Zymomonas mobilis pyruvate decarboxylase. EMBO J 13:2755–2763

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bykova NV, Rasmusson AG, Igamberdiev AU, Gardeström P, Møller IM (1999) Two separate transhydrogenase activities are present in plant mitochondria. Biochem Biophys Res Commun 265:106–111

    Article  CAS  PubMed  Google Scholar 

  • Bykova NV, Møller IM (2001) Involvement of matrix NADP turnover in the oxidation of NAD-linked substrates by pea leaf mitochondria. Physiol Planta 111:448–456

    Article  CAS  Google Scholar 

  • Bykova NV, Stensballe A, Egsgaard H, Jensen ON, Møller IM (2003a) Phosphorylation of formate dehydrogenase in potato tuber mitochondria. J Biol Chem 278:26021–26030

    Article  CAS  PubMed  Google Scholar 

  • Bykova NV, Egsgaard H, Møller IM (2003b) Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 540:141–146

    Article  CAS  PubMed  Google Scholar 

  • Bykova NV, Hoehn B, Rampitsch C, Banks T, Stebbing JA, Fan T, Knox R (2011a) Redox-sensitive proteome and antioxidant strategies in wheat seed dormancy control. Proteomics 11:865–882

    Article  CAS  PubMed  Google Scholar 

  • Bykova NV, Hoehn B, Rampitsch C, Hu J, Stebbing J-A, Knox R (2011b) Thiol redox-sensitive seed proteome in dormant and non-dormant hybrid genotypes of wheat. Phytochemistry 72:1162–1172

    Article  CAS  PubMed  Google Scholar 

  • Bykova NV, Møller IM, Gardeström P, Igamberdiev AU (2014) The function of glycine decarboxylase complex is optimized to maintain high photorespiratory flux via buffering of its reaction products. Mitochondrion 19:357–364

    Article  CAS  PubMed  Google Scholar 

  • Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Nat Acad Sci U S A 95:11715–11720

    Article  CAS  Google Scholar 

  • Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027–36031

    Article  CAS  PubMed  Google Scholar 

  • 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 278:46869–46877

    Article  CAS  PubMed  Google Scholar 

  • du Choi S, Kim NH, Hwang BK (2014) Pepper mitochondrial FORMATE DEHYDROGENASE1 regulates cell death and defense responses against bacterial pathogens. Plant Physiol 166:1298–1311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Considine MJ, Sandalio LM, Foyer CH (2015) Unravelling how plants benefit from ROS and NO reactions, while resisting oxidative stress. Ann Bot 116:469–473

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB, Sandalio LM, Palma JM, Lupiáñez JA, del Río LA (1999) Peroxisomal NADP-dependent isocitrate dehydrogenase. Characterization and activity regulation during natural senescence. Plant Physiol 121:921–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas FJ, Palma JM, del Río LA, Barroso JB (2009) Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14

    Article  CAS  PubMed  Google Scholar 

  • Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39

    Article  CAS  PubMed  Google Scholar 

  • Cvetkovska M, Vanlerberghe GC (2013) Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ 36:721–732

    Article  CAS  Google Scholar 

  • Dahal K, Wang J, Martyn GD, Rahimy F, Vanlerberghe GC (2014) Mitochondrial alternative oxidase maintains respiration and preserves photosynthetic capacity during moderate drought in Nicotiana tabacum. Plant Physiol 166:1560–1574

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daloso DM, Müller K, Obata T, Florian A, Tohge T, Bottcher A, Riondet C, Bariat L, Carrari F, Nunes-Nesi A, Buchanan BB, Reichheld JP, Araújo WL, Fernie AR (2015) Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Nat Acad Sci U S A 112:E1392–E1400

    Article  CAS  Google Scholar 

  • Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espey MG, Thomas DD, Miranda KM, Wink DA (2002) Focusing of nitric oxide mediated nitrosation and oxidative nitrosylation as a consequence of reaction with superoxide. Proc Nat Acad Sci U S A 99:11127–11132

    Article  CAS  Google Scholar 

  • Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Carreras A, Valderrama R, Begara-Morales JC, Hernández LE, Corpas FJ, Barroso JB (2011) Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions. Identification of two new genes of mitochondrial Mn-SOD. J Plant Physiol 168:1303–1308

    Article  PubMed  CAS  Google Scholar 

  • Finkemeier I, König AC, Heard W, Nunes-Nesi A, Pham PA, Leister D, Fernie AR, Sweetlove LJ (2013) Transcriptomic analysis of the role of carboxylic acids in metabolite signaling in Arabidopsis leaves. Plant Physiol 162:239–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florez-Sarasa I, Flexas J, Rasmusson AG, Umbach AL, Siedow JN, Ribas-Carbo M (2011) In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant Cell Environ 34:1373–1383

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P, Fernie AR (2011) Metabolic control of redox and redox control of metabolism in plants. Antiox Redox Signal 21:1389–1421

    Article  CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot JP (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Nat Acad Sci U S A 101:14545–14550

    Article  CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35

    Article  CAS  PubMed  Google Scholar 

  • Giegé P, Heazlewood JL, Roessner-Tunali U, Millar AH, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15:2140–2151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Graham JW, Williams TC, Morgan M, Fernie AR, Ratcliffe RG, Sweetlove LJ (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19:3723–3738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta KJ, Stoimenova M, Kaiser WM (2005) In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J Exp Bot 56:2601–2609

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Shah JK, Brotman Y, Jahnke K, Willmitzer L, Kaiser WM, Bauwe H, Igamberdiev AU (2012) Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot 63:1773–1784

    Article  CAS  PubMed  Google Scholar 

  • Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91:807–819

    Article  CAS  PubMed  Google Scholar 

  • Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I, Mulo P, Kangasjärvi S, Aro EM, Oelze ML, Dietz KJ, Nunes-Nesi A, Do PT, Fernie AR, Talla SK, Raghavendra AS, Linke V, Scheibe R (2012) Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J Exp Bot 63:1445–1459

    Article  CAS  PubMed  Google Scholar 

  • Hebelstrup KH, Jensen EO (2008) Expression of NO scavenging hemoglobin is involved in the timing of bolting in Arabidopsis thaliana. Planta 227:917–927

    Article  CAS  PubMed  Google Scholar 

  • Heineke D, Riens B, Grosse H, Hoferichter P, Peter U, Flügge UI, Heldt HW (1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95:1131–1137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoek JB, Rydström J (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem J 254:1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horchani F, Prevot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, Brouquisse R (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155:1023–1036

    Article  CAS  PubMed  Google Scholar 

  • Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, Davy de Virville J, Rémy R, Francs-Small CC (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol 116:627–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Taylor NL, Narsai R, Eubel H, Whelan J, Millar AH (2009) Experimental analysis of the rice mitochondrial proteome, its biogenesis, and heterogeneity. Plant Physiol 149:719–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Hill RD, Wally OS, Dionisio G, Ayele BT, Jami SK, Stasolla C (2014) Hemoglobin control of cell survival/death decision regulates in vitro plant embryogenesis. Plant Physiol 165:810–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igamberdiev AU, Hurry V, Krömer S, Gardeström P (1998) The role of mitochondrial electron transport during photosynthetic induction. A study with barley (Hordeum vulgare) protoplasts incubated with rotenone and oligomycin. Physiol Planta 104:431–439

    Article  CAS  Google Scholar 

  • Igamberdiev AU, Bykova NV, Lea PJ, Gardeström P (2001) The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol Planta 111:427–438

    Article  CAS  Google Scholar 

  • Igamberdiev AU, Gardeström P (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim Biophys Acta 1606:117–125

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Shen T, Gardeström P (2006) Function of mitochondria during the transition of barley protoplasts from low light to high light. Planta 224:196–204

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Lernmark U, Gardeström P (2014a) Activity of the mitochondrial pyruvate dehydrogenase complex in plants is stimulated in the presence of malate. Mitochondrion 19:184–190

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Ratcliffe RG, Gupta KJ (2014b) Plant mitochondria: source and target for nitric oxide. Mitochondrion 19:329–333

    Article  CAS  PubMed  Google Scholar 

  • Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M, Galina A (2015) Succinate dehydrogenase (mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. New Phytol 208:776–789

    Article  CAS  PubMed  Google Scholar 

  • Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GK, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci Signal 9:re2

    Google Scholar 

  • Jia L (2011) Is reactive oxygen species (ROS) the underlying factor for inhibited root growth in Osspr1? Plant Signal Behav 6:1024–1025

    Article  CAS  PubMed  Google Scholar 

  • Jimenez A, Hernandez JA, Del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kasimova MR, Grigiene J, Krab K, Hagedorn PH, Flyvbjerg H, Andersen PE, Møller IM (2006) The free NADH concentration is kept constant in plant mitochondria under different metabolic conditions. Plant Cell 18:688–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozlov AV, Staniek K, Nohl H (1999) Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 454:127–130

    Article  CAS  PubMed  Google Scholar 

  • Krömer S, Scheibe R (1996) Function of the chloroplastic malate valve for respiration during photosynthesis. Biochem Soc Trans 24:761–766

    Article  PubMed  Google Scholar 

  • Kurtz DM (2007) Flavo-diiron enzymes: nitric oxide or dioxygen reductases? Dalton Trans 37:4115–4121

    Article  CAS  Google Scholar 

  • Laloi C, Rayapuram N, Chartier Y, Grienenberger JM, Bonnard G, Meyer Y (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Nat Acad Sci U S A 98:14144–14149

    Article  CAS  Google Scholar 

  • Leterrier M, Del Río LA, Corpas FJ (2007) Cytosolic NADP-isocitrate dehydrogenase of pea plants: genomic clone characterization and functional analysis under abiotic stress conditions. Free Radic Res 41:191–199

    Article  CAS  PubMed  Google Scholar 

  • Leterrier M, Barroso JB, Valderrama R, Begara-Morales JC, Sánchez-Calvo B, Chaki M, Luque F, Viñegla B, Palma JM, Corpas FJ (2016) Peroxisomal NADP-isocitrate dehydrogenase is required for Arabidopsis stomatal movement. Protoplasma 253:403–415

    Article  CAS  PubMed  Google Scholar 

  • Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice ALTERNATIVE OXIDASE 1 genes. Plant Cell Environ 36:775–788

    Article  CAS  Google Scholar 

  • 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 150:646–657

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T, Jarvis R, Haas F, Nieuwland J, Lim B, Müller C, Salcedo-Sora E, Kruse C, Orsel M, Hell R, Miller AJ, Bray P, Foyer CH, Murray JA, Meyer AJ, Cobbett CS (2010) Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc Nat Acad Sci U S A 107:2331–2336

    Article  CAS  Google Scholar 

  • Maurino VG, Engqvist MK (2015) 2-Hydroxy acids in plant metabolism. Arabidopsis Book 13:e0182

    Article  PubMed  PubMed Central  Google Scholar 

  • McKinnon DJ, Brzezowski P, Wilson KE, Gray GR (2009) Mitochondrial and chloroplastic targeting signals of NADP+-dependent isocitrate dehydrogenase. Biochem Cell Biol 87:963–974

    Article  CAS  PubMed  Google Scholar 

  • Millar AH, Sweetlove LJ, Giegé P, Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127:1711–1727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A, Sugimoto E, Omote H, Ma JF, Shinozaki K, Moriyama Y (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat Comm 6:5928

    Article  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annl Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  Google Scholar 

  • Møller IM (2015) Mitochondrial metabolism is regulated by thioredoxin. Proc Nat Acad Sci U S A 112:3180–3181

    Article  CAS  Google Scholar 

  • Møller IM, Rasmusson AG (1998) The role of NADP in the mitochondrial matrix. Trend Plant Sci 3:21–27

    Article  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13

    Article  CAS  PubMed  Google Scholar 

  • Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122:573–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol. doi:10.1104/pp.16.00346

    Google Scholar 

  • O’Brien KM, Dirmeier R, Engle M, Poyton RO (2004) Mitochondrial protein oxidation in yeast mutants lacking manganese-(MnSOD) or copper- and zinc-containing superoxide dismutase (CuZnSOD): evidence that MnSOD and CuZnSOD have both unique and overlapping functions in protecting mitochondrial proteins from oxidative damage. J Biol Chem 279:51817–51827

    Article  PubMed  CAS  Google Scholar 

  • Pearce LL, Kanai AJ, Birder LA, Pitt BR, Peterson J (2002) The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J Biol Chem 277:13556–13562

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Poyton RO, Ball KA, Castello PR (2009) Mitochondrial generation of free radicals and hypoxic signaling. Trend Endocrinol Metab 20:332–340

    Article  CAS  Google Scholar 

  • Radi R, Turrens JF, Chang LY, Bush KM, Crapo JD, Freeman BA (1991) Detection of catalase in rat heart mitochondria. J Biol Chem 266:22028–22034

    CAS  PubMed  Google Scholar 

  • Rasmusson AG, Møller IM (1991) NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial membrane studied using inside-out submitochondrial particles. Physiol Planta 83:357–365

    Article  CAS  Google Scholar 

  • Reichheld JP, Meyer E, Khafif M, Bonnard G, Meyer Y (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 579:337–342

    Article  CAS  PubMed  Google Scholar 

  • Rhoads DM, Umbach AL, Sweet CR, Lennon AM, Rauch GS, Siedow JN (1998) Regulation of the cyanide-resistant alternative oxidase of plant mitochondria. Identification of the cysteine residue involved in alpha-keto acid stimulation and intersubunit disulfide bond formation. J Biol Chem 273:30750–30756

    Article  CAS  PubMed  Google Scholar 

  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141:357–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H, Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33:841–851

    Article  CAS  PubMed  Google Scholar 

  • Salvato F, Havelund JF, Chen M, Rao RS, Rogowska-Wrzesinska A, Jensen ON, Gang DR, Thelen JJ, Møller IM (2014) The potato tuber mitochondrial proteome. Plant Physiol 164:637–653

    Article  CAS  PubMed  Google Scholar 

  • Salvi M, Battaglia V, Brunati AM, La Rocca N, Tibaldi E, Pietrangeli P, Marcocci L, Mondovì B, Rossi CA, Toninello A (2007) Catalase takes part in rat liver mitochondria oxidative stress defense. J Biol Chem 282:24407–24415

    Article  CAS  PubMed  Google Scholar 

  • Sazanov LA, Jackson JB (1994) Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett 344:109–116

    Article  CAS  PubMed  Google Scholar 

  • Schimmeyer J, Bock R, Meyer EH (2016) l-Galactono-1,4-lactone dehydrogenase is an assembly factor of the membrane arm of mitochondrial complex I in Arabidopsis. Plant Mol Biol 90:117–126

    Article  CAS  PubMed  Google Scholar 

  • Schmidtmann E, König AC, Orwat A, Leister D, Hartl M, Finkemeier I (2014) Redox regulation of Arabidopsis mitochondrial citrate synthase. Mol Plant 7:156–169

    Article  CAS  PubMed  Google Scholar 

  • Selles B, Hugo M, Trujillo M, Srivastava V, Wingsle G, Jacquot JP, Radi R, Rouhier N (2012) Hydroperoxide and peroxynitrite reductase activity of poplar thioredoxin-dependent glutathione peroxidase 5: kinetics, catalytic mechanism and oxidative inactivation. Biochem J 442:369–380

    Article  CAS  PubMed  Google Scholar 

  • Shabnam N, Sharmila P, Sharma A, Strasser RJ, Govindjee Pardha-Saradhi P (2015) Mitochondrial electron transport protects floating leaves of long leaf pondweed (Potamogeton nodosus Poir) against photoinhibition: comparison with submerged leaves. Photosynth Res 125:305–319

    Article  CAS  PubMed  Google Scholar 

  • Shah JK, Cochrane DW, De Paepe R, Igamberdiev AU (2013) Respiratory complex I deficiency results in low nitric oxide levels, induction of hemoglobin and upregulation of fermentation pathways. Plant Physiol Biochem 63:185–190

    Article  CAS  PubMed  Google Scholar 

  • Stöhr C, Strube F, Marx G, Ullrich WR, Rockel P (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212:835–841

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Struglics A, Fredlund KM, Rasmusson AG, Møller IM (1993) The presence of a short redox chain in the membrane of intact potato tuber peroxisomes and the association of malate dehydrogenase with the peroxisomal membrane. Physiol Planta 88:19–28

    Article  CAS  Google Scholar 

  • Subbaiah CC, Bush DS, Sachs MM (1998) Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells. Plant Physiol 118:759–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundaravelpandian K, Chandrika NN, Schmidt W (2013) PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol 197:151–161

    Article  CAS  PubMed  Google Scholar 

  • Sweetlove LJ, Beard KF, Nunes-Nesi A, Fernie AR, Ratcliffe RG (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15:462–470

    Article  CAS  PubMed  Google Scholar 

  • Szarka A, Bánhegyi G, Asard H (2013) The inter-relationship of ascorbate transport, metabolism and mitochondrial, plastidic respiration. Antioxid Redox Signal 19:1036–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 36:163–173

    Article  CAS  PubMed  Google Scholar 

  • Tcherkez G, Mahé A, Gauthier P, Mauve C, Gout E, Bligny R, Cornic G, Hodges M (2009) In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the noncyclic nature of the tricarboxylic acid “cycle” in illuminated leaves. Plant Physiol 151:620–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tielens AG, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don’t know them. Trend Biochem Sci 27:564–572

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tovar-Méndez A, Matamoros MA, Bustos-Sanmamed P, Dietz KJ, Cejudo FJ, Rouhier N, Sato S, Tabata S, Becana M (2011) Peroxiredoxins and NADPH-dependent thioredoxin systems in the model legume Lotus japonicus. Plant Physiol 156:1535–1547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Trujillo M, Ferrer-Sueta G, Radi R (2008) Kinetic studies on peroxynitrite reduction by peroxiredoxins. Method Enzymol 441:173–196

    Article  CAS  Google Scholar 

  • Vanlerberghe GC, Day DA, Wiskich JT, Vanlerberghe AE, McIntosh L (1995) Alternative oxidase activity in tobacco leaf mitochondria—dependence on tricarboxylic acid cycle-mediated redox regulation and pyruvate activation. Plant Physiol 109:353–361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J 276:643–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Rajakulendran N, Amirsadeghi S, Vanlerberghe GC (2011) Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol Plant 142:339–351

    Article  CAS  PubMed  Google Scholar 

  • Wigge B, Krömer S, Gardeström P (1993) The redox levels and subcellular distribution of pyridine nucleotides in illuminated barley leaf protoplasts studied by rapid fractionation. Physiol Planta 88:10–18

    Article  CAS  Google Scholar 

  • Wulff A, Oliveira HC, Saviani EE, Salgado I (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21:132–139

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, 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 Lett 468:89–92

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54:875–892

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Hisabori T (2016) Adenine nucleotide-dependent and redox-independent control of mitochondrial malate dehydrogenase activity in Arabidopsis thaliana. Biochim Biophys Acta 1857:810–818

    Article  CAS  PubMed  Google Scholar 

  • Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Planta 143:396–407

    Article  CAS  Google Scholar 

  • Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. U. Igamberdiev .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Bykova, N.V., Igamberdiev, A.U. (2016). Redox State in Plant Mitochondria and its Role in Stress Tolerance. In: Gupta, D., Palma, J., Corpas, F. (eds) Redox State as a Central Regulator of Plant-Cell Stress Responses. Springer, Cham. https://doi.org/10.1007/978-3-319-44081-1_5

Download citation

Publish with us

Policies and ethics