Abstract
Hypoxia commonly occurs in roots in water-saturated soil and in maturing and germinating seeds. We here review the role of the mitochondria in the cellular response to hypoxia with an emphasis on the turnover of Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS) and their potential signaling function. Under hypoxia, aerobic respiration in the mitochondria can be limited by the oxygen supply, the electron transport component are more reduced and superoxide and NO are produced in increasing amounts at Complexes III and IV initiating the formation of a range of other ROS and RNS. Unless removed, these compounds can react with proteins either reversibly—one-step oxidation or nitrosylation of cysteine—or irreversibly by carbonylation and this affects the properties of the oxidized proteins in, as yet, mostly unknown ways. ROS, probably hydrogen peroxide, and/or oxidized peptides are thought to be responsible for retrograde signaling to the nucleus. NO, formed by nitrite reduction, is either recycled through the hemoglobin/NO cycle (an oxygen-consuming process) or lost from the tissue by diffusion. Under severe hypoxia this can be a significant drain on the plants fixed nitrogen reserves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- AOX:
-
Alternative oxidase
- CCO:
-
Cytochrome c oxidase
- Complex I:
-
NADH dehydrogenase complex
- Complex III:
-
Cytochrome bc1 complex
- Complex IV:
-
Cytochrome c oxidase complex
- ETC:
-
Electron transport chain
- HNE:
-
4-Hydroxy-2-nonenal
- IMM:
-
Inner mitochondrial membrane
- OMM:
-
Outer mitochondrial membrane
- PTM:
-
Posttranslational modification
- RNS:
-
Reactive nitrogen species
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
References
Affourtit C, Krab K, Moore AL (2001) Control of plant mitochondrial respiration. Biochim Biophys Acta 1504:58–69
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, Vienna, pp 267–297
Becana M, Dalton DA, Morana JF, Iturbe-Ormaetxea I, Matamorosa MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381
Bender A, Hajieva P, Moosmann B (2008) Adaptive antioxidant methionine accumulation in respiratory chain complexes explains the use of a deviant genetic code in mitochondria. Proc Natl Acad Sci USA 105:16496–16501
Bienert GP, Møller ALB, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn JP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192
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
Brand MD (1994) The stoichiometry of proton pumping and ATP synthesis in mitochondria. Biochemist 16:20–24
Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466–472
Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220
Colombatti F, Gonzalez DH, Welchen E (2014) Plant mitochondria under pathogen attack: A sigh of relief or a last breath? Mitochondrion, in press
Cooper CE (2002) Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 27:33–39
Darwent MJ, Armstrong W, Armstrong J, Beckett PM (2003) Exploring the radial and longitudinal aeration of primary maize roots by means of Clark-Type oxygen microelectrodes. Russ J Plant Physiol 50:722–732
Dordas C, Hasinoff BB, Igamberdiev AU, Manac’h N, Rivoal J, Hill RD (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35:763–770
Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219:66–72
Finkemeier I, Konig 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
Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398. doi:10.3389/fpls.2013.00398
Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445
Geigenberger P, Fernie AR, Gibon Y, Maja 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
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
Gupta KJ, Hebelstrup KH, Kruger NJ, Ratcliffe GR (2014) Nitric oxide is required for homeostasis of oxygen and reactive oxygen species in barley roots under aerobic conditions. Mol Plant 7:747–750
Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford
Hebelstrup KH, Jensen EO (2008) Expression of NO scavenging hemoglobin is involved in the timing of bolting in Arabidopsis thaliana. Planta 227:917–927
Hebelstrup KH, Igamberdiev AU, Hill RD (2007) Metabolic effects of hemoglobin gene expression in plants. Gene 398:86–93
Hebelstrup KH, Ostergaard-Jensen E, Hill RD (2008) Bioimaging techniques for subcellular localization of plant hemoglobins and measurement of hemoglobin-dependent nitric oxide scavenging in planta. Methods Enzymol 437:595–604
Hebelstrup KH, van Zanten M, Mandon J, Voesenek LACJ, Harren FJM, Cristescu SM, Møller IM, Mur LAJ (2012) Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana. J Exp Bot 63:5581–5591
Hebelstrup KH, Shah JK, Igamberdiev AU (2013) The role of nitric oxide and hemoglobin in plant development and morphogenesis. Physiol Plant 148:457–469
Hebelstrup KH, Shah JK, Simpson C, Schjoerring JK, Mandon J, Cristescu SM, Harren FJM, Christiansen MW, Mur LAJ, Igamberdiev AU (2014) An assessment of the biotechnological use of hemoglobin modulation in cereals. Physiol Plant 150:593–603
Hill RD (2012) Non-symbiotic haemoglobins—what’s happening beyond nitric oxide scavenging? AoB PLANTS 2012:pls004
Igamberdiev AU, Seregelyes C, Manac'h N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102
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
Igamberdiev AU, Bykova NV, Hill RD (2006) Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 223:1033–1040
Kozlov AV, Staniek K, Nohl H (1999) Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 454:127–130
Kristensen BK, Askerlund P, Bykova NV, Egsgaard H, Møller IM (2004) Identification of oxidised proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65:1839–1851
Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93:15036–15040
Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494
Maisonneuve E, Ducret A, Khoueiry P, Lignon S, Longhi S, Talla E, Dukan S (2009) Rules governing selective protein carbonylation. PLoS One 4(10):e7269. doi:10.1371/journal.pone.0007269
Matamoros MA, Fernandez-Garcia N, Wienkoop S, Loscos J, Saiz A, Becana M (2013) Mitochondria are an early target of oxidative modifications in senescing legume nodules. New Phytol 197:873–885. doi:10.1111/nph.12049
Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci USA 96:8271–8276
Millar AH, Bergersen FJ, Day DA (1994) Oxygen-affinity of terminal oxidases in soybean mitochondria. Plant Physiol Biochem 32:847–852
Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104
Møller IM (2001) Plant mitochondria and oxidative stress. Electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591
Møller IM (2007) Mitochondrial electron transport and oxidative stress. In: Logan DM (ed) Plant mitochondria, Annual plant reviews. Blackwell, Oxford, pp 185–211
Møller IM, Kristensen BK (2006) Protein oxidation in plant mitochondria detected as oxidized tryptophan. Free Radic Biol Med 40:430–435
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
Møller IM, Sweetlove LJ (2010) ROS signaling—specificity is required. Trends Plant Sci 15:370–374
Møller IM, Rogowska-Wrzesinska A, Rao RSP (2011) Protein carbonylation and metal-catalyzed oxidation in a cellular perspective. J Proteomics 74:2228–2242
Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier A, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794
Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol 190:351–368
Rao RS, Møller IM (2011) Pattern of occurrence and occupancy of carbonylation sites in proteins. Proteomics 11(21):4166–4173
Rao RSP, Møller IM, Thelen JJ, Miernyk JA (2014) Methionine oxidation: Bridging ROS and protein phosphorylation signaling. Cell Stress and Chaperones, in press
Rasmusson AG, Møller IM (2011) Mitochondrial electron transport and plant stress. In: Kempken F (ed) Plant mitochondria. Springer, New York, pp 357–381
Ribas-Carbo M, Berry JA, Azconn-Bieto J, Siedow JN (1994) The reaction of the plant mitochondrial cyanide-resistant alternative oxidase with oxygen. Biochim Biophys Acta 1188:205–212
Sainz M, Pérez-Rontomé C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M (2013) Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. Plant J 76:875–887
Salvato F, Havelund JF, Chen M, Rao RSP, Wrzesinska-Rogowska A, Jensen ON, Gang DR, Thelen JJ, Møller IM (2014) The potato tuber mitochondrial proteome. Plant Physiol 164:637–653
Smagghe BJ, Trent JT, Hargrove MS (2008) NO dioxygenase activity in hemoglobins is ubiquitous in vitro, but limited by reduction in vivo. PLos One 3:e2039
Smakowska E, Czarna M, Janska H (2014) Mitochondrial ATP-dependent proteases in protection against accumulation of carbonylated proteins. Mitochondrion, in press
Sowa AW, Duff SMG, Guy PA, Hill RD (1998) Altering hemoglobin levels changes energy status in maize cells under hypoxia. Proc Natl Acad Sci USA 95:10317–10321
Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378
Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474
Sugiura M, Georgescu MN, Takahashi M (2007) A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol 48:1022–1035
Sweetlove LJ, Møller IM (2009) Oxidation of proteins in plants—mechanisms and consequences. Adv Bot Res 52:1–23
Szal B, Jolivet Y, Hasenfratz-Sauderb MP, Dizengremel P, Rychter AM (2003) Oxygen concentration regulates alternative oxidase expression in barley roots during hypoxia and post-hypoxia. Physiol Plant 119:494–502
Tan Y-F, O’Toole N, Taylor NL, Millar AH (2010) Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol 152:747–761
Thiel J, Rolletschek H, Friedel S, Lunn JE, Nguyen TH, Feil R, Tschiersch H, Muller M, Borisjuk L (2011) Seed-specific elevation of non-symbiotic hemoglobin AtHb1: beneficial effects and underlying molecular networks in Arabidopsis thaliana. BMC Plant Biol 11:43
Vashisht D, Hesselink A, Pierik R, Ammerlaan JMH, Bailey-Serres J, Visser EJW, Pedersen O, van Zanten M, Vreugdenhil D, Jamar DCL, Voesenek LACJ, Sasidharan R (2011) Natural variation of submergence tolerance among Arabidopsis thaliana accessions. New Phytol 190:299–310
Vestergaard CL, Flyvbjerg H, Møller IM (2012) Intracellular signalling by diffusion—Can waves of hydrogen peroxide transmit intracellular information in plant cells? Front Plant Sci 3:295. doi:10.3389/fpls.2012.00295
Vigeolas H, Huhn D, Geigenberger P (2011) Nonsymbiotic hemoglobin-2 leads to an elevated energy state and to a combined increase in polyunsaturated fatty acids and total oil content when overexpressed in developing seeds of transgenic arabidopsis plants. Plant Physiol 155:1435–1444
Wang XG, Hargrove MS (2013) Nitric oxide in plants: the roles of ascorbate and hemoglobin. PLos One 8:12
Welchen E, Garcia L, Mansilla N, Gonzales DH (2014) Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirement. Front Plant Sci 4:551. doi:10.3389/fpls.2013.00551
Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH (2007) The cytotoxic lipid peroxidation product 4-hydroxy-2-nonenal covalently modifies a selective range of proteins linked to respiratory function in plant mitochondria. J Biol Chem 282:37436–37447
Wittenberg JB (1966) Molecular mechanism of hemoglobin-facilitated oxygen diffusion. J Biol Chem 241:104–114
Wittenberg JB (1970) Myoglobin-facilitated oxygen diffusion—role of myoglobin in oxygen entry into muscle. Physiol Rev 50:559–636
Wyman J (1966) Facilitated diffusion and possible role of myoglobin as a transport mechanism. J Biol Chem 241:115–121
Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129
Zaobornyj T, Ghafourifar P (2012) Strategic localization of heart mitochondrial NOS: a review of the evidence. Am J Physiol Heart Circ Physiol 303:H1283–H1293
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Hebelstrup, K.H., Møller, I.M. (2015). Mitochondrial Signaling in Plants Under Hypoxia: Use of Reactive Oxygen Species (ROS) and Reactive Nitrogen Species (RNS). In: Gupta, K., Igamberdiev, A. (eds) Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants. Signaling and Communication in Plants, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-319-10079-1_4
Download citation
DOI: https://doi.org/10.1007/978-3-319-10079-1_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-10078-4
Online ISBN: 978-3-319-10079-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)