Skip to main content

Oxygen Deprivation, Metabolic Adaptations and Oxidative Stress

  • Chapter
  • First Online:
Waterlogging Signalling and Tolerance in Plants

Abstract

In this chapter, we discuss the metabolic changes relevant for the production of reactive oxygen and nitrogen species (ROS and RNS) in plant tissues during oxygen deprivation. It is notable too, that at times the oxidative damage does not take place during the oxygen deficiency period but only after the restoration of normal oxygen supply to the tissues. This is mainly due to the fact that ROS may be formed immediately after oxygen re-enters the tissues. The level of oxygen in the tissues naturally depends on the outside concentration and diffusion rate but is also under metabolic control. Two hypotheses on the regulation of internal O2 concentration in the cells through the control of respiration rely on a regulation of glycolytic pathway and pyruvate availability and mitochondrial electron transport chain by NO and ROS balance. Both adaptive strategies aim to decrease the respiratory capacity and to postpone complete anoxia. This chapter also describes the interaction of the many antioxidants found in plant tissues and oxidative stress and oxidative damage caused by waterlogging and oxygen deprivation. If the antioxidative protection is still capable of detoxifying the ROS formed, damage is minimal, but if not, then considerable damage can take place very suddenly. Many of the ROS and RNS species act as signalling agents acting in the regulation of metabolic events leading to tolerance or, e.g. in the case of aerenchyma development, into programmed cell death. The balance between O2 transport to hypoxic tissues, regulatory adaptations, anoxic metabolites, ROS–RNS chemistry and signalling, determines the survival of plants under waterlogging and oxygen deprivation.

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 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

Abbreviations

ADH:

Alcohol dehydrogenase

AOX:

Alternative oxidase

COX:

Cytochrome oxidase

ETC:

Electron transport chain

FFA:

Free fatty acids

LP:

Lipid peroxidation

NO:

Nitric oxide

1O2 :

Singlet oxygen

O −•2 :

Superoxide anion

ONOO :

Peroxynitrite

PFK-PPi:

PPi-dependent phosphofructokinase

PLD:

Phospholipase D

PEPC:

Phosphoenolpyruvate carboxylase

PPDK:

Pyruvate phosphate dikinase

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

UCP:

Mitochondrial uncoupling protein

References

  • Ahsan N, Lee D, Lee S, Lee K, Bahk J, Lee B (2007) A proteomic screen and identification of waterlogging-regulated proteins in tomato roots. Plant Soil 295:37–51

    Article  CAS  Google Scholar 

  • Alscher RG (1989) Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant 77:457–464

    Article  CAS  Google Scholar 

  • Amor Y, Chevion M, Levine A (2000) Anoxia pretreatment protects soybean cells against H2O2-induced cell death: possible involvement of peroxidases and of alternative oxidase. FEBS Lett 477:175–180

    Article  CAS  Google Scholar 

  • Andreyev A, Kushnareva Y, Starkov A (2005) Mitochondrial metabolism of reactive oxygen species. Biochem (Moscow) 70:200–214

    Article  CAS  Google Scholar 

  • Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466

    Article  CAS  PubMed  Google Scholar 

  • Arcisio-Miranda M, Abdulkader F, Brunaldi K, Curi R, Procopio J (2009) Proton flux induced by free fatty acids across phospholipid bilayers: new evidences based on short-circuit measurements in planar lipid membranes. Arch Biochem Biophys 484:63–69

    Article  CAS  PubMed  Google Scholar 

  • Armstrong W, Webb T, Darwent M, Beckett PM (2009) Measuring and interpreting respiratory critical oxygen pressures in roots. Ann Bot 103:281–293

    Article  PubMed  Google Scholar 

  • Arora A, Byrem TM, Nair MG, Strasburg GM (2000) Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Arch Biochem Biophys 373:102–109

    Article  CAS  PubMed  Google Scholar 

  • Arrigoni O, de Tullio MC (2000) The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions. J Plant Physiol 157:481–488

    CAS  Google Scholar 

  • Attia H, Arnaud N, Karray N, Lachaal M (2008) Long-term effects of mild salt stress on growth, ion accumulation and superoxide dismutase expression of Arabidopsis rosette leaves. Physiol Plant 132:293–305

    Article  CAS  PubMed  Google Scholar 

  • Avsian-Kretchmer O, Eshdat Y, Gueta-Dahan Y, Ben-Hayyim G (1999) Regulation of stress-induced phospholipid hydroperoxide glutathione peroxidase expression in citrus. Planta 209:469–477

    Article  CAS  PubMed  Google Scholar 

  • Baier M, Dietz KJ (1999) Alkyl hydroperoxide reductases: the way out of the oxidative breakdown of lipids in chloroplasts. Trends Plant Sci 4:166–168

    Article  PubMed  Google Scholar 

  • Bailey-Serres J, Chang R (2005) Sensing and signalling in response to oxygen deprivation in plants and other organisms. Ann Bot 96:507–518

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    Article  CAS  PubMed  Google Scholar 

  • Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028

    Article  CAS  PubMed  Google Scholar 

  • Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel M, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite–nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta Bioenergetics 1777:1268–1275

    Article  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  CAS  PubMed  Google Scholar 

  • Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341

    Article  CAS  PubMed  Google Scholar 

  • Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658

    Article  CAS  PubMed  Google Scholar 

  • Biemelt S, Keetman U, Mock H, Grimm B (2000) Expression and activity of isoenzymes of superoxide dismutase in wheat roots in response to hypoxia and anoxia. Plant Cell Environ 23:135–144

    Article  CAS  Google Scholar 

  • Blokhina O, Chirkova TV, Fagerstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Fagerstedt KV (2006) Oxidative stress and antioxidant defences in plants. In: Quek (ed) Oxidative stress, disease and cancer, pp 151–199

    Google Scholar 

  • Blokhina OB, Fagerstedt KV, Chirkova TV (1999) Relationships between lipid peroxidation and anoxia tolerance in a range of species during post-anoxic reaeration. Physiol Plant 105:625–632

    Article  CAS  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV, Hoikkala A, Wähälä K, Chirkova TV (2000) Antioxidant status of anoxia-tolerant and -intolerant plant species under anoxia and reaeration. Physiol Plant 109:396–403

    Article  CAS  Google Scholar 

  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53:1367–1376

    Article  CAS  PubMed  Google Scholar 

  • Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence – a broad perspective. Physiol Mol Plant Pathol 51:347–366

    Article  CAS  Google Scholar 

  • Boo YC, Jung J (1999) Water deficit-induced oxidative stress and antioxidative defenses in rice plants. J Plant Physiol 155:255–261

    CAS  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  Google Scholar 

  • Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytol 182:17–30

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Braidot E, Petrussa E, Vianello A, Macri F (1999) Hydrogen peroxide generation by higher plant mitochondria oxidizing complex I or complex II substrates. FEBS Lett 451:347–350

    Article  CAS  PubMed  Google Scholar 

  • Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755

    Article  CAS  PubMed  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660

    Article  CAS  PubMed  Google Scholar 

  • Brandalise M, Maia IG, Borecký J, AbE V, Arruda P (2003) Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress. J Bioenerg Biomembr 35:203–209

    Article  CAS  PubMed  Google Scholar 

  • Buettner GR (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch Biochem Biophys 300:535–543

    Article  CAS  PubMed  Google Scholar 

  • Cela J, Falk J, Munné-Bosch S (2009) Ethylene signaling may be involved in the regulation of tocopherol biosynthesis in Arabidopsis thaliana. FEBS Lett 583:992–996

    Article  CAS  PubMed  Google Scholar 

  • Chakraborti T, Das S, Mondal M, Roychoudhury S, Chakraborti S (1999) Oxidant, mitochondria and calcium: an overview. Cell Signal 11:77–85

    Article  CAS  PubMed  Google Scholar 

  • Chirkova TV, Sinyutina NF, Blyudzin YA, Barsky IE, Smetannikova SV (1989) Phospholipid fatty acids of root mitochondria and microsomes from rice and wheat seedlings exposed to aeration or anaerobiosis. Plant Physiol (Russian) 36:126–134

    CAS  Google Scholar 

  • Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309

    Article  CAS  PubMed  Google Scholar 

  • Cooper CE, Davies NA, Psychoulis M, Canevari L, Bates TE, Dobbie MS, Casley CS, Sharpe MA (2003) Nitric oxide and peroxynitrite cause irreversible increases in the K-m for oxygen of mitochondrial cytochrome oxidase: in vitro and in vivo studies. Biochim Biophys Acta Bioenergetics 1607:27–34

    Article  CAS  Google Scholar 

  • de Oliveira HC, Wulff A, Saviani EE, Salgado I (2008) Nitric oxide degradation by potato tuber mitochondria: evidence for the involvement of external NAD(P)H dehydrogenases. Biochim Biophys Acta Bioenergetics 1777:470–476

    Article  CAS  Google Scholar 

  • del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335

    Article  PubMed  CAS  Google Scholar 

  • Della Penna D (2005) Progress in the dissection and manipulation of vitamin E synthesis. Trends Plant Sci 10:574–579

    Article  CAS  Google Scholar 

  • Dordas C, Hasinoff B, Rivoal J, Hill R (2004) Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219:66–72

    Article  CAS  PubMed  Google Scholar 

  • Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot (Lond) 91:173–178

    Article  CAS  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Article  CAS  PubMed  Google Scholar 

  • Elstner EF, Osswald W (1994) Mechanisms of oxygen activation during plant stress. Proc Royal Soc Edinb 102B:31–154

    Google Scholar 

  • Freeman BA, Baker PRS, Schopfer FJ, Woodcock SR, Napolitano A, d'Ischia M (2008) Nitro-fatty acid formation and signaling. J Biol Chem 283:15515–15519

    Article  CAS  PubMed  Google Scholar 

  • Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggests a role for dehydroascorbate signalling. J Exp Bot 59:729–737

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Foyer CH, Lelandais MA (1996) A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaves mesophyll cells. J Plant Physiol 148:391–398

    CAS  Google Scholar 

  • Fryer MJ (1992) The antioxidant effects of thylakoid vitamin E (α-tocopherol). Plant Cell Environ 15:381–392

    Article  CAS  Google Scholar 

  • Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia – is survival a balancing act? Trends Plant Sci 9:449–456

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256

    Article  CAS  PubMed  Google Scholar 

  • Generosova IP, Vartapetian BB (2005) On the physiological role of anaerobically synthesized lipids in Oryza sativa seedlings. Russ J Plant Physiol 52:481–488

    Article  CAS  Google Scholar 

  • Gibbs J, Greenway H (2003) Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Gille L, Nohl H (2001) The ubiquinol/bc1 redox couple regulates mitochondrial oxygen radical formation. Arch Biochem Biophys 388:34–38

    Article  CAS  PubMed  Google Scholar 

  • Godber BL, Doel JJ, Sapkota GP, Blake DR, Stevens CR, Eisenthal R, Harrison R (2000) Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J Biol Chem 275:7757–7763

    Article  CAS  PubMed  Google Scholar 

  • Goglia F, Skulachev VP (2003) A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet. FASEB J 17:1585–1591

    Article  CAS  PubMed  Google Scholar 

  • Grabel'nykh OI, Kolesnichenko AV, Pobezhimova TP, Zykova VV, Voinikov VK (2006) Mechanisms and functions of nonphosphorylating electron transport in respiratory chain of plant mitochondria. Russ J Plant Physiol 53:418–429

    Article  CAS  Google Scholar 

  • Grace S, Logan BA (2000) Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Trans R Soc Lond B 355:1499–1510

    Article  CAS  Google Scholar 

  • Graham JWA, Williams TCR, 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  Google Scholar 

  • Greenway H, Gibbs J (2003) Review: mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct Plant Biol 30:999–1036

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B (2009) The wanderings of a free radical. Free Radic Biol Med 46:531–542

    Article  CAS  PubMed  Google Scholar 

  • Hamberg M, Fahlstadius P (1992) On the specificity of a fatty acid epoxygenase in broad bean (Vicia faba L.). Plant Physiol 99:987–995

    Article  CAS  PubMed  Google Scholar 

  • Harrison R (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33:774–797

    Article  CAS  PubMed  Google Scholar 

  • Hassan W, Ibrahim M, Deobald AM, Braga AL, Nogueira CW, Rocha JBT (2009) pH-Dependent Fe (II) pathophysiology and protective effect of an organoselenium compound. FEBS Lett 583:1011–1016

    Article  CAS  PubMed  Google Scholar 

  • Hebelstrup KH, Igamberdiev AU, Hill RD (2007) Metabolic effects of hemoglobin gene expression in plants. Gene 398:86–93

    Article  CAS  PubMed  Google Scholar 

  • Hernandez I, Alegre L, Van Breusegem F, Sergi Munne-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132

    Article  CAS  PubMed  Google Scholar 

  • Horemans N, Foyer CH, Potters G, Asard H (2000) Ascorbate function and associated transport systems in plants. Plant Physiol Biochem 38:531–540

    Article  CAS  Google Scholar 

  • Huang S, Colmer TD, Millar AH (2008) Does anoxia tolerance involve altering the energy currency towards PPi? Trends Plant Sci 13:221–227

    Article  CAS  PubMed  Google Scholar 

  • Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Baron K, Manac'h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: Involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557–564

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103:259–268

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot 101:229–248

    Article  CAS  PubMed  Google Scholar 

  • Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255

    Article  CAS  PubMed  Google Scholar 

  • Jimenez A, Hernandez JA, Pastori G, del Río LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335

    Article  CAS  PubMed  Google Scholar 

  • Kagan VE (1989) Tocopherol stabilizes membrane against phospholipase A, free fatty acids, and lysophospholipids. In: Diplock AT, Machlin J, Packer L, Pryor WA (Eds) Vitamin E: biochemistry and health implications. Ann New York Acad Sci 570:121–135

    Google Scholar 

  • Kagan VE, Fabisiak JP, Quinn PJ (2000) Coenzyme Q and vitamin E need each other as antioxidants. Lipids 214:11–18

    CAS  Google Scholar 

  • Kalashnikov JUE, Balakhnina TI, Zakrzhevsky DA (1994) Effect of soil hypoxia on activation of oxygen and the system of protection from oxidative destruction in roots and leaves of Hordeum vulgare. Russ J Plant Physiol 41:583–588

    CAS  Google Scholar 

  • Kamal-Eldin A, Appelqvist L-Å (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701

    Article  CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant physiol 118:637–650

    Article  CAS  PubMed  Google Scholar 

  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494

    Article  CAS  PubMed  Google Scholar 

  • Kondo N, Kawashima M (2000) Enhancement of tolerance to oxidative stress in cucumber (Cucumis sativus L.) seedlings by UV-B irradiation: possible involvement of phenolic compounds and antioxidant enzymes. J Plant Res 113:311–317

    Article  CAS  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  CAS  PubMed  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  CAS  PubMed  Google Scholar 

  • Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–198

    Article  CAS  PubMed  Google Scholar 

  • Larson RA (1988) The antioxidants of higher plants. Phytochem 27:969–978

    Article  CAS  Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    Article  CAS  PubMed  Google Scholar 

  • Lavola A, Julkunen-Tiitto R, DeE La Rosa TM, Lehto T, Aphalo PJ (2000) Allocation of carbon to growth and secondary metabolites in birch seedlings under UV-B radiation and CO2 exposure. Physiol Plant 109:260–267

    Article  CAS  Google Scholar 

  • Lee SH, Ahsan N, Lee KW, Lee DG, Kwark SS, Kwon SY, Kim TH, Lee BH (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Lee TM, Lin YN (1995) Changes in soluble and cell wall-bound peroxidase activities with growth in anoxia-treated rice (Oryza sativa L.) coleoptiles and roots. Plant Sci 106:1–7

    Article  CAS  Google Scholar 

  • Libourel IG, van Bodegom PM, Fricker MD, Ratcliffe RG (2006) Nitrite reduces cytoplasmic acidosis under anoxia. Plant Physiol 142:1710–1717

    Article  CAS  PubMed  Google Scholar 

  • Liso R, Innocenti AM, Bitonti MB, Arrigoni O (1988) Ascorbic acid-induced progression of quiescent centre cells from G1 to S phase. New Phytol 110:469–471

    Article  CAS  Google Scholar 

  • Liu F, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    Article  CAS  PubMed  Google Scholar 

  • Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138

    Article  CAS  PubMed  Google Scholar 

  • 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 96:8271–8276

    Article  CAS  PubMed  Google Scholar 

  • May MJ, Vernoux T, Leaver C, Van Montagu M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    Article  CAS  Google Scholar 

  • McDonald AE, Vanlerberghe GC (2007) The organization and control of plant mitochondrial metabolism. In: Plaxton WC, McManus MT (eds) Control of primary metabolism in plants. Blackwell, Oxford, pp 290–324

    Google Scholar 

  • Millenaar FF, Lambers H (2003) The alternative oxidase: in vivo regulation and function. Plant Biol 5:2–15

    Article  CAS  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  PubMed  Google Scholar 

  • Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566:1–5

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • 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 52:561–591

    Article  CAS  PubMed  Google Scholar 

  • Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  CAS  Google Scholar 

  • Moller M, Botti H, Batthyany C, Rubbo H, Radi R, Denicola A (2005) Direct measurement of nitric oxide and oxygen partitioning into liposomes and low density lipoprotein. J Biol Chem 280:8850–8854

    Article  PubMed  CAS  Google Scholar 

  • Monk LS, Fagerstedt KV, Crawford RMM (1989) Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiol Plant 76:456–459

    CAS  Google Scholar 

  • 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 147:101–114

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux PM, Karpinski S, Jiménez A, Cleary SP, Robinson C, Creissen GP (1998) Identification of cDNAS encoding plastid-targeted glutathione peroxidase. Plant J 13:375–379

    Article  CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Weiler E, Alegre L, Müller M, Düchting P, Falk J (2007) α-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants. Planta 225:681–691

    Article  PubMed  CAS  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–17

    Article  CAS  PubMed  Google Scholar 

  • Mustroph A, Albrecht G, Hajirezaei M, Grimm B, Biemelt S (2005) Low levels of pyrophosphate in transgenic potato plants expressing E. coli pyrophosphatase lead to decreased vitality under oxygen deficiency. Ann Bot 96:717–726

    Article  CAS  PubMed  Google Scholar 

  • Nakazono M, Imamura T, Tsutsumi N, Sasaki T, Hirai A (2000) Characterization of two cDNA clones encoding isozymes of the F1F0-ATPase inhibitor protein of rice mitochondria. Planta 210:188–194

    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  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • Nowak G, Grant DF, Moran JH (2004) Linoleic acid epoxide promotes the maintenance of mitochondrial function and active Na+ transport following hypoxia. Toxicol Lett 147:161–175

    Article  CAS  PubMed  Google Scholar 

  • O'Donnell VB, Freeman BA (2001) Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circ Res 88:12–21

    PubMed  Google Scholar 

  • Ohyashiki T, Nunomura M (2000) A marked stimulation of Fe3+-dependent lipid peroxidation in phospholipid liposomes under acidic conditions. Biochim Biophys Acta Mol Cell Biol Lipids 1484:241–250

    CAS  Google Scholar 

  • Pastore D, Trono D, Laus MN, Di Fonzo N, Flagella Z (2007) Possible plant mitochondria involvement in cell adaptation to drought stress: a case study: durum wheat mitochondria. J Exp Bot 58:195–210

    Article  CAS  PubMed  Google Scholar 

  • Pavelic D, Arpagaus S, Rawyler A, Brandle R (2000) Impact of post-anoxia stress on membrane lipids of anoxia-pretreated potato cells. A re-appraisal. Plant Physiol 124:1285–1292

    Article  CAS  PubMed  Google Scholar 

  • Pietta PG (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Polgreen KE, Featherstone J, Willis AC, Harris DA (1995) Primary structure and properties of the inhibitory protein of the mitochondrial ATPase (H+-ATP synthase) from potato. Biochim Biophys Acta Bioenergetics 1229:175–180

    Article  Google Scholar 

  • Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, Davies KJA (2006) Free radical biology and medicine: it's a gas, man! Am J Physiol Regul Integr Comp Physiol 291:R491–R511

    CAS  PubMed  Google Scholar 

  • Qiao W, Fan L (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246

    Article  CAS  PubMed  Google Scholar 

  • Rawyler A, Arpagaus S, Braendle R (2002) Impact of oxygen stress and energy availability on membrane stability of plant cells. Ann Bot 90:499–507

    Article  CAS  PubMed  Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 2:152–159

    Article  Google Scholar 

  • Rinalducci S, Murgiano L, Zolla L (2008) Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot 59:3781–3801

    Article  CAS  PubMed  Google Scholar 

  • Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Jacquot J (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74:259–268

    Article  CAS  PubMed  Google Scholar 

  • Rouslin W (1991) Regulation of the mitochondrial ATPase in situ in cardiac muscle: role of the inhibitor subunit. J Bioenerg Biomembr 23:873–888

    Article  CAS  PubMed  Google Scholar 

  • Rubbo H, Radi R (2008) Protein and lipid nitration: role in redox signaling and injury. Biochim Biophys Acta 1780:1318–1324

    CAS  PubMed  Google Scholar 

  • Sairam R, Kumutha D, Ezhilmathi K, Deshmukh P, Srivastava G (2008) Physiology and biochemistry of waterlogging tolerance in plants. Biol Plant 52:401–412

    Article  CAS  Google Scholar 

  • Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, van Montagu M, Inzé D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. PNAS 94:2745–2750

    Article  CAS  PubMed  Google Scholar 

  • Santosa I, Ram P, Boamfa E, Laarhoven L, Reuss J, Jackson M, Harren F (2007) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta 226:193–202

    Article  CAS  PubMed  Google Scholar 

  • Sattler SE, Mene-Saffrane L, Farmer EE, Krischke M, Mueller MJ, DellaPenna D (2006) Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants. Plant Cell 18:3706–3720

    Article  CAS  PubMed  Google Scholar 

  • Scebba F, Sebastiani L, Vitagliano C (1998) Changes in activity of antioxidative enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiol Plant 104:747–752

    Article  CAS  Google Scholar 

  • Serbinova EA, Packer L (1994) Antioxidant properties of α-tocopherol and α-tocotrienol. Methods Enzymol 234:354–366

    Article  CAS  PubMed  Google Scholar 

  • Sgherri C, Cosi E, Navari-Izo F (2003) Phenols and antioxidative status of Raphanus sativus grown in copper excess. Physiol Plant 118:21–28

    Article  CAS  PubMed  Google Scholar 

  • Skulachev VP (1998) Uncoupling: new approaches to an old problem of bioenergetics. Biochim Biophys Acta Bioenergetics 1363:100–124

    Article  CAS  Google Scholar 

  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78:661–669

    Article  CAS  Google Scholar 

  • Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235

    CAS  PubMed  Google Scholar 

  • Sorg O (2004) Oxidative stress: a theoretical model or a biological reality? C R Biol 327:649–662

    Article  CAS  PubMed  Google Scholar 

  • Stohr C, Stremlau S (2006) Formation and possible roles of nitric oxide in plant roots. J Exp Bot 57:463–470

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stoimenova M, Libourel IG, Ratcliffe RG, Kaiser WM (2003) The role of nitrate reduction in the anoxic metabolism of roots II. Anoxic metabolism of tobacco roots with or without nitrate reductase activity. Plant Soil 253:155–167

    Article  CAS  Google Scholar 

  • St-Pierre J, Brand MD, Boutilier RG (2000) Mitochondria as ATP consumers: cellular treason in anoxia. PNAS 97:8670–8674

    Article  CAS  PubMed  Google Scholar 

  • Su Z, Chai M-F, Lu P-L, An R, Chen J, Wang X-C (2007) AtMTM1, a novel mitochondrial protein, may be involved in activation of the manganese-containing superoxide dismutase in Arabidopsis. Planta 226:1031–1039

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto M, Furui S, Suzuki Y (1997) Molecular cloning and characterisation of a cDNA encoding putative phospholipid hydroperoxide glutathione peroxidase from spinach. Biosci Biotech Biochem 61:1379–1381

    Article  CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  Google Scholar 

  • Szal B, Jolivet Y, Hasenfratz-Sauder M, Dizengremel P, Rychter AM (2003) Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia. Physiol Plant 119:494–502

    Article  CAS  Google Scholar 

  • Takahama U, Oniki T (1997) A peroxide/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol Plant 101:845–852

    Article  CAS  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    Article  CAS  PubMed  Google Scholar 

  • Thomas CE, McLean LR, Parker RA, Ohlweiler DF (1992) Ascorbate and phenolic antioxidant interactions in prevention of liposomal oxidation. Lipids 27:543–550

    Article  CAS  PubMed  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

    Article  PubMed  CAS  Google Scholar 

  • Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 2:421–427

    Google Scholar 

  • Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984

    Article  PubMed  CAS  Google Scholar 

  • van Dongen JT, Frohlich A, Ramirez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2009) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 103:269–280

    Article  PubMed  CAS  Google Scholar 

  • van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529

    Article  PubMed  CAS  Google Scholar 

  • Vianello A, Macrì F (1999) Proton pumping pyrophosphatase from higher plant mitochondria. Physiol Plant 105:763–768

    Article  CAS  Google Scholar 

  • Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245

    Article  Google Scholar 

  • Visser EJW, Voesenek LACJ, Vartapetian BB, Jackson MB (2003) Flooding and plant growth. Ann Bot 91:107–109

    Article  CAS  Google Scholar 

  • Ushimaru T, Kanematsu S, Shibasaka M, Tsuji H (1999) Effect of hypoxia on the antioxidative enzymes in aerobically grown rice (Oryza sativa) seedlings. Physiol Plant 107:81–187

    Article  Google Scholar 

  • Willekens H, Inzé D, van Montagu M, van Camp W (1995) Catalase in plants. Mol Breed 1:207–228

    Article  CAS  Google Scholar 

  • Wingate VPM, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210

    Article  CAS  PubMed  Google Scholar 

  • Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434–456

    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 

  • Yan B, Dai Q, Liu X, Huang S, Wang Z (1996) Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261–268

    Article  CAS  Google Scholar 

  • Yang X-D, Dong C-J, Liu J-Y (2006) A plant mitochondrial phospholipid hydroperoxide glutathione peroxidase: its precise localization and higher enzymatic activity. Plant Mol Biol 62:951–962

    Article  CAS  PubMed  Google Scholar 

  • Yordanova R, Popova L (2007) Flooding-induced changes in photosynthesis and oxidative status in maize plants. Acta Physiol Plant 29:535–541

    Article  CAS  Google Scholar 

  • Yu Z, Zhang J, Wang X, Chen J (2008) Excessive copper induces the production of reactive oxygen species, which is mediated by phospholipase D, nicotinamide adenine dinucleotide phosphate oxidase and antioxidant systems. J Integr Plant Biol 50:157–167

    Article  CAS  PubMed  Google Scholar 

  • Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmalzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098

    Article  CAS  PubMed  Google Scholar 

  • Zsigmond L, Rigo G, Szarka A, Szekely G, Otvos K, Darula Z, Medzihradszky KF, Koncz C, Koncz Z, Szabados L (2008) Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 146:1721–1737

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kurt V. Fagerstedt .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Blokhina, O., Fagerstedt, K.V. (2010). Oxygen Deprivation, Metabolic Adaptations and Oxidative Stress. In: Mancuso, S., Shabala, S. (eds) Waterlogging Signalling and Tolerance in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10305-6_7

Download citation

Publish with us

Policies and ethics