Abstract
Even during optimal growth conditions, the availability of oxygen to plant cells can get limited due to the diffusion resistance of the tissue for oxygen. However, plants can probably regulate the rate of respiratory oxygen consumption which is thought to play a role during periods of low-oxygen stress as it postpones oxygen to become limiting as respiratory substrate. At present, limitation of oxygen becomes more and more important in the context of climate change and concomitant changed environmental stress conditions such as flooding. One mechanism by which plants can react to survive periods of low-oxygen stress is to save on oxygen by downregulating energy requiring processes such as storage metabolism. For this, a series of drastic metabolic adaptations is initiated in plants upon hypoxia. In this chapter, it is discussed how plants adapt to low-oxygen availability via metabolic responses and by regulating respiratory oxygen consumption as a function of the actual oxygen concentration.
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References
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Araújo WL, Ishizaki K, Nunes-Nesi A, Tohge T, Larson TR, Krahnert I, Balbo I, Witt S, Dörmann P, Graham IA, Leaver CJ, Fernie AR (2011) Analysis of a range of catabolic mutants provides evidence that phytanoyl-coenzyme A does not act as a substrate of the electron-transfer flavoprotein/electron-transfer flavoprotein:ubiquinone oxidoreductase complex in Arabidopsis during dark-induced senescence. Plant Physiol 157:55–69
Araújo WL, Nunes-Nesi A, Nikoloski Z, Sweetlove LJ, Fernie AR (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ 35:1–21
Armstrong W, Armstrong J (2014) Plant internal oxygen transport (diffusion and convection) and measuring and modelling oxygen gradients. In: van Dongen JT, Licausi F (eds) Low oxygen stress in plants. Springer, Heidelberg
Armstrong W, Beckett PM (2011) Experimental and modelling data contradict the idea of respiratory down-regulation in plant tissues at an internal [O2] substantially above the critical oxygen pressure for cytochrome oxidase. New Phytol 190:431–441
Armstrong W, Strange ME, Cringle S, Beckett PM (1994) Microelectrode and modelling study of oxygen distribution in roots. Ann Bot 74:287–299
Ast C, Draaijer A (2014) Oxygen sensing in plants. In: van Dongen JT, Licausi F (eds) Low oxygen stress in plants, vol 21, Plant cell monographs. Springer, Heidelberg
Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek L, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138
Barding GA Jr, Fukao T, Béni S, Bailey-Serres J, Larive CK (2011) Differential metabolic regulation governed by the rice SUB1A gene during submergence stress and identification of alanylglycine by 1H NMR spectroscopy. J Proteome Res 11:320–330
Barding GA Jr, Béni S, Fukao T, Bailey-Serres J, Larive CK (2013) Comparison of GC-MS and NMR for metabolite profiling of rice subjected to submergence stress. J Proteome Res 12:898–909
Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase Rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296(5575):2026–2028
Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel MH, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777(10):1268–1275
Berthold DA, Andersson ME, Nordlund P (2000) New insights into the structure and function of the alternative oxidase. Biochim Biophys Acta 1460:241–254
Biais B, Beauvoit B, Allwood J, Deborde C, Maucourt M, Goodacre R, Rolin D, Moing A (2010) Metabolic acclimation to hypoxia revealed by metabolite gradients in melon fruit. J Plant Physiol 167:242–245
Blokhina OB, Chirkova TV, Fagerstedt KV (2001) Anoxic stress leads to hydrogen peroxide formation in plant cells. J Exp Bot 52:1179–1190
Bologa KL, Fernie AR, Leisse A, Loureiro ME, Geigenberger P (2003) A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiol 132:2058–2072
Borecký J, Maia IG, Costa ADT, Jezek P, Chaimovich H, de Andrade PBM, Vercesi AE, Arruda P (2001) Functional reconstitution of Arabidopsis thaliana plant uncoupling mitochondrial protein (AtPUMP1) expressed in Escherichia coli. FEBS Lett 505:240–244
Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytol 182(1):17–30
Brown GC, Hafner RP, Brand MD (2005) A ‘top-down’ approach to the determination of control coefficients in metabolic control theory. Eur J Biochem 188:321–325
Burke PV, Poyton RO (1998) Structure/function of oxygen-regulated isoforms in cytochrome c oxidase. J Exp Biol 201:1163–1175
Bykova NV, Egsgaard H, Møller IM (2003) Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 540(1–3):141–146
Chandel NS, Budinger GR, Schumacker PT (1996) Molecular oxygen modulates cytochrome c oxidase function. J Biol Chem 271:18672–18677
Clifton R, Lister R, Parker KL, Sappl PG, Elhafez D, Millar AH, Day DA, Whelan J (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol Biol 58:193–212
Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334
Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42:273–282
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
Dudkina NV, Heinemeyer J, Sunderhaus S, Boekema EJ, Braun HP (2006) Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends Plant Sci 11(5):232–240
Eubel H, Heinemeyer J, Sunderhaus S, Braun HP (2004) Respiratory chain supercomplexes in plant mitochondria. Plant Physiol Biochem 42(12):937–942
Fang JK, Prabu SK, Sepuri NB, Raza H, Anandatheerthavarada HK, Galati D, Spear J, Avadhani NG (2007) Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 581(7):1302–1310
Felle HH (2005) pH regulation in anoxic plants. Ann Bot 96(4):519–532
Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia—is survival a balancing act? Trends Plant Sci 9:449–456
Fukao T, Bailey-Serres J (2008) Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci U S A 105:16814–16819
Fukao T, Yeung E, Bailey-Serres J (2012) The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiol 160:1795–1807
Fukuda R, Zhang H, Kim J, Shimoda L, Dang CV, Semenza GL (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129:111–122
Galkin A, Abramov AY, Frakich N, Duchen MR, Moncada S (2009) Lack of oxygen deactivates mitochondrial complex I: implications for ischemic injury? J Biol Chem 284:36055–36061
Gardner PR, Costantino G, Szabó C, Salzman AL (1997) Nitric oxide sensitivity of the aconitases. J Biol Chem 272:25071–25076
Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256
Geigenberger P, Fernie AR, Gibon Y, Christ M, Stitt M (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381:723–740
Gibbs J, Greenway H (2003) Review: mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30(1):1–47
Gibon Y, Vigeolas H, Tiessen A, Geigenberger P, Stitt M (2002) Sensitive and high throughput metabolite assays for inorganic pyrophosphate, ADPGlc, nucleotide phosphates, and glycolytic intermediates based on a novel enzymic cycling system. Plant J 30:221–235
Gnaiger E, Lassnig B, Kuznetsov AV, Margreiter R (1998) Mitochondrial respiration in the low oxygen environment of the cell. Effect of ADP on oxygen kinetics. Biochim Biophys Acta 1365:249–254
Gupta KJ, Zabalza A, van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16(3):160–168
Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015–1069
Heazlewood JL, Millar AH (2005) AMPDB: the Arabidopsis mitochondrial protein database. Nucleic Acids Res 33:605–610
Ho QT, Verboven P, Verlinden BE, Schenk A, Delele MA, Rolletschek H, Vercammen J, Nicolaï BM (2010) Genotype effects on internal gas gradients in apple fruit. J Exp Bot 61:2745–2755
Ho QT, Verboven P, Verlinden BE, Herremans E, Wevers M, Carmeliet J, Nicolaï BM (2011) A three-dimensional multiscale model for gas exchange in fruit. Plant Physiol 155(3):1158–1168
Holtzapffel RC, Castelli J, Finnegan PM, Millar AH, Whelan J, Day DA (2003) A tomato alternative oxidase protein with altered regulatory properties. Biochim Biophys Acta 1606(1–3):153–162
Hütter E, Renner K, Jansen-Dürr P, Gnaiger E (2002) Biphasic oxygen kinetics of cellular respiration and linear oxygen dependence of antimycin A inhibited oxygen consumption. Mol Biol Rep 29:83–87
Ito J, Taylor NL, Castleden I, Weckwerth W, Millar AH, Heazlewood JL (2009) A survey of the Arabidopsis thaliana mitochondrial phosphoproteome. Proteomics 9(17):4229–4240
Kennedy RA, Rumpho ME, Fox TC (1992) Anaerobic metabolism in plants. Plant Physiol 100(1):1–6
Kimmerer TW, Stringer MA (1988) Alcohol dehydrogenase and ethanol in the stems of trees: evidence for anaerobic metabolism in the vascular cambium. Plant Physiol 87:693–697
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
Laisk A, Oja V, Eichelmann H (2007) Kinetics of leaf oxygen uptake represent in planta activities of respiratory electron transport and terminal oxidases. Physiol Plant 131:1–9
Lara MV, Budde CO, Porrini L, Borsani J, Murray R, Andreo CS, Drincovich MF (2011) Peach (Prunus persica) fruit response to anoxia: reversible ripening and biochemical changes. Plant Cell Physiol 52(2):392–403
Lee TC, Langston-Unkefer PJ (1985) Pyruvate decarboxylase from Zea mays L.: I. Purification and partial characterization from mature kernels and anaerobically treated roots. Plant Physiol 79(1):242–247
Licausi F, Giorgi FM, Schmälzlin E, Usadel B, Perata P, van Dongen JT, Geigenberger P (2011) HRE-type genes are regulated by growth-related changes in internal oxygen concentrations during the normal development of potato (Solanum tuberosum) tubers. Plant Cell Physiol 52(11):1957–1972
Limami AM, Glévarec G, Ricoult C, Clique J-B, Planchet E (2008) Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. J Exp Bot 59:2325–2335
Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation and mature zones of Vitis roots: influence of oxygen availability. Planta 214:767–774
Maricle BR, Lee RW (2007) Root respiration and oxygen flux in salt marsh grasses from different elevational zones. Mar Biol 151:413–423
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 14:8271–8276
McDonald AE, Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Physiol Part D Genomics Proteomics 1:357–364
Millar AH, Day DA (1997) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398(2–3):155–158
Millar AH, Wiskich JT, Whelan J, Day DA (1993) Organic acid activation of the alternative oxidase of plant mitochondria. FEBS Lett 329:259–262
Millar AH, Hoefnagel MHN, Day DA, Wiskich JT (1996) Specificity of the organic acid activation of alternative oxidase in plant mitochondria. Plant Physiol 111:613–618
Millar A, Eubel H, Jänsch L, Kruft V, Heazlewood J, Braun HP (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Mol Biol 56(1):77–90
Mommer L, Visser EJ (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann Bot 96:581–589
Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190(2):472–487
Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol 122(2):573–582
Nikoloski Z, van Dongen JT (2011) Modeling alternatives for interpreting the change in oxygen-consumption rates during hypoxic conditions. New Phytol 190(2):273–276; author reply 276–278
Ober ES, Sharp RE (1996) A microsensor for direct measurement of O2 partial pressure within plant tissues. J Exp Bot 47:447–457
Pedreschi R, Franck C, Lammertyn J, Erban A, Kopka J, Hertog M, Verlinden B, Nicolai B (2009) Metabolic profiling of ‘Conference’ pears under low oxygen stress. Postharvest Biol Technol 51:123–130
Planchet E, Gupta JK, 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(5):732–743
Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214
Podestá FE, Plaxton WC (1991) Kinetic and regulatory properties of cytosolic pyruvate kinase from germinating castor oil seeds. Biochem J 279(Pt 2):495–501
Porterfield DM, Kuang A, Smith PJS, Crispi ML, Musgrave ME (1999) Oxygen-depleted zones inside reproductive structures of Brassicaceae: implications for oxygen control of seed development. Can J Bot 77:1439–1446
Pucciariello C, Parlanti S, Banti V, Novi G, Perata P (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol 159(1):184–196
Puntarulo S, Cederbaum AI (1988) Effect of oxygen concentration on microsomal oxidation of ethanol and generation of oxygen radicals. Biochem J 251:787–794
Ramirez-Aguilar SJ, Keuthe M, Rocha M, Fedyaev VV, Kramp K, Gupta KJ, Rasmusson AG, Schulze WX, van Dongen JT (2011) The composition of plant mitochondrial supercomplexes changes with the oxygen availability. J Biol Chem 286:43045–43053
Rasmusson AG, Sool KL, Ethon TE (2004) Alternative NAD(P)H dehydrogenases of plant mitochondria. Annu Rev Plant Biol 55:23–39
Rasmusson AG, Geisler DA, Møller IM (2008) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8(1):47–60, Unique aspects of plant mitochondria
Rasmusson AG, Fernie AR, van Dongen JT (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiol Plant 137:371–382
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 13:30750–30756
Ribas-Carbo 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 109:829–837
Ricoult C, Echeverria LO, Cliquet JB, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula. J Exp Bot 57:3079–3089
Rivoal J, Ricard B, Pradet A (1990) Purification and partial characterization of pyruvate decarboxylase from Oryza sativa L. Eur J Biochem 194(3):791–797
Roberts JKM, Callis J, Wemmer D, Walbot V, Jardetzky O (1984) Mechanism of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia. Proc Natl Acad Sci U S A 81:3379–3383
Rocha M, Sodek L, Licausi F, Hameed MW, Dornelas MC, van Dongen JT (2010a) Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids 39(4):1043–1053
Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010b) Glycolysis and the TCA-cycle are linked by Alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152(3):1501–1513
Rolletschek H, Borisjuk L, Koschorreck M, Wobus U, Weber H (2002) Legume embryos develop in a hypoxic environment. J Exp Bot 53(371):1099–1107
Rolletschek H, Weschke W, Weber H, Wobus U, Borisjuk L, Rosenfeld E, Beauvoit B (2004) Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. J Exp Bot 55:1351–1359
Rolletschek H, Melkus G, Grafahrend-Belau E, Fuchs J, Heinzel N, Schreiber F, Jakob PM, Borisjuk L (2011) Combined noninvasive imaging and modeling approaches reveal metabolic compartmentation in the barley endosperm. Plant Cell 23(8):3041–54
Schäfer E, Dencher NA, Vonck J, Parcej DN (2007) Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 46:12579–12585
Schmälzlin E, van Dongen JT, Klimant I, Marmodée B, Steup M, Fisahn J, Geigenberger P, Löhmannsröben HG (2005) An optical multifrequency phase-modulation method using microbeads for measuring intracellular oxygen concentrations in plants. Biophys J 89:1339–1345
Shingaki-Wells RN, Huang S, Taylor NL, Carroll AJ, Zhou W, Millar AH (2011) Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant Physiol 156:1706–1724
Skutnik M, Rychter AM (2009) Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. J Plant Physiol 166(9):926–937
Solaini G, Baracca A, Lenaz G, Sgarbi G (2010) Hypoxia and mitochondrial oxidative metabolism. Biochim Biophys Acta Bioenerg 1797:1171–1177
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 32:891–904
Thomson CJ, Greenway H (1991) Metabolic evidence for stelar anoxia in maize roots exposed to low O2 concentrations. Plant Physiol 96:1294–1301
Tihanyi K, Talbot B, Brzezinski R, Thirion JP (1989) Purification and characterization of alcohol dehydrogenase from soybean. Phytochemistry 28(5):1335–1338
Tovar-Méndez A, Miernyk JA, Randall DD (2003) Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 270(6):1043–1049
Tucker ML, Laties GG (1985) The dual role of oxygen in avocado fruit respiration; kinetic analysis and computer modelling of diffusion-affected respiratory oxygen isotherms. Plant Cell Environ 8:117–127
Turrens JF (2004) Mitochondrial formation of reactive oxygen species. J Physiol 552(2):335–344
Umbach AL, Ng VS, Siedow JN (2006) Regulation of plant alternative oxidase activity: a tale of two cysteines. Biochim Biophys Acta 1757(2):135–142
van Bodegom PM, Sorrell BK, Oosthoek A, Bakker C, Aerts R (2008) Separating the effects of partial submergence and soil oxygen demand on plant physiology. Ecology 89(1):193–204
van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529–1543
van Dongen JT, Roeb GW, Dautzenberg M, Fröhlich A, Vigeolas H, Minchin PEH, Geigenberger P (2004) Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds. Plant Physiol 135:1809–1821
van Dongen JT, Fröhlich A, Ramírez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2008) 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
van Dongen JT, Gupta KJ, Ramírez-Aguilar SJ, Araújo WL, Nunes-Nesi A, Fernie AR (2011) Regulation of respiration in plants: a role for alternative metabolic pathways. J Plant Physiol 168(12):1434–1443
Vanlerberghe GC, McIntosh L (1997) Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48:703–734
Vercesi AE, Borecký J, Maia Ide G, Arruda P, Cuccovia IM, Chaimovich H (2006) Plant uncoupling mitochondrial proteins. Annu Rev Plant Biol 57:383–404
Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inactivation of plant aconitase by hydrogen-peroxide. Biochem J 276:643–648
Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708
Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide 5(3):261–270
Zabalza A, van Dongen JT, Fröhlich A, Oliver SN, Faix B, Gupta KJ, Schmälzlin 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
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Päpke, C., Ramirez-Aguilar, S., Antonio, C. (2014). Oxygen Consumption Under Hypoxic Conditions. In: van Dongen, J., Licausi, F. (eds) Low-Oxygen Stress in Plants. Plant Cell Monographs, vol 21. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1254-0_10
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