Skip to main content
SpringerLink
Log in

Role of Plant Mitochondria in Nitric Oxide Homeostasis During Oxygen Deficiency

  • Chapter
  • First Online:
Nitric Oxide in Plants: Metabolism and Role in Stress Physiology

Abstract

During their life cycle, plants may be exposed to situations of reduced oxygen availability, such as those imposed by soil flooding, in which their tissues have to cope with restrictions of aerobic metabolism. The limited availability of oxygen for reduction by the mitochondrial respiratory chain has many effects on plant metabolism and physiology, negatively affecting the growth and productivity of economically important species. Nitrite has been considered a major alternative terminal acceptor of the respiratory chain under oxygen deprivation. The gaseous radical nitric oxide (NO) produced from mitochondrial nitrite reduction has emerged as an important mediator of plant tolerance to low oxygen tensions, regulating mitochondrial bioenergetics, gene expression and the pathways of plant hormones. In particular, a recent study has indicated the involvement of mitochondrial NO synthesis from nitrite in the nitrate-mediated response of soybean roots to hypoxia. The importance of processes for NO degradation in maintaining mitochondrial functionality and controlling root metabolism during an oxygen shortage has also been highlighted. In this regard, the involvement of respiratory proteins and non-symbiotic hemoglobins in NO degradation has been demonstrated. In the present chapter, advances in this area will be discussed with a special focus on the role of nitrogen nutrition and mitochondrial NO homeostasis for plant tolerance to oxygen deficiency.

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

Access this chapter

Log in via an institution
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
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

  • Ahsan N, Lee DG, Lee SH et al (2007) A proteomic screen and identification of waterlogging regulated proteins in tomato roots. Plant Soil 295:37–51

    CAS  Google Scholar 

  • Alam I, Lee DG, Kim KH et al (2010) Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage. J Biosci 35:49–62

    CAS  PubMed  Google Scholar 

  • Allegre A, Silvestre J, Morard P et al (2004) Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J Exp Bot 55:2625–2634

    CAS  PubMed  Google Scholar 

  • Amora Y, Chevionb M, Levinea 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

    CAS  PubMed  Google Scholar 

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–232

    CAS  Google Scholar 

  • Arnon DI (1937) Ammonium and nitrate nitrogen nutrition of barley at different seasons in relation to hydrogen-ion concentration, manganese, copper, and oxygen supply. Soil Sci 44:91–122

    CAS  Google Scholar 

  • Astier J, Rasul S, Koen E et al (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Benamar A, Rolletschek H, Borisjuk L et al (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777:1268–1275

    CAS  PubMed  Google Scholar 

  • Besson-Bard A, Astier J, Rasul S et al (2009) Current view of nitric oxide-responsive genes in plants. Plant Sci 177:302–309

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blokhina O, Fagerstedt KV (2010) Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol Biochem 48:359–373

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Brown GC, Cooper CE (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356:295–298

    CAS  PubMed  Google Scholar 

  • Castello PR, David PS, McClure T et al (2006) Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 3:277–287

    CAS  PubMed  Google Scholar 

  • Cleeter MW, Cooper JM, Darley-Usmar VM et al (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide, implications for neurodegenerative diseases. FEBS Lett 345:50–54

    CAS  PubMed  Google Scholar 

  • Cooper CE, Giulivi C (2007) Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am J Physiol Cell Physiol 292:C1993–C2003

    CAS  PubMed  Google Scholar 

  • Corpas FJ, Palma JM, Del Río LA, Barroso JB (2013) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 4:29

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  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 1777:470–476

    PubMed  Google Scholar 

  • del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792

    PubMed  Google Scholar 

  • Dordas C, Hasinoff BB, Igamberdiev AU et al (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35:763–770

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 487:223–250

    Google Scholar 

  • Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 181:401–404

    PubMed  Google Scholar 

  • Frungillo L, de Oliveira JF, Saviani EE et al (2013) Modulation of mitochondrial activity by S-nitrosoglutathione reductase in Arabidopsis thaliana cell lines. Biochim Biophys Acta 1827:239–247

    CAS  PubMed  Google Scholar 

  • Garcia-Novo F, Crawford RMM (1973) Soil aeration, nitrate reduction and flooding tolerance in higher plants. New Phytol 72:1031–1039

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Geigenberger P, Fernie AR, Gibon Y et al (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381:723–740

    CAS  PubMed  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

    CAS  Google Scholar 

  • Gout E, Boisson AM, Aubert S et al (2001) Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and phosphorous-31 nuclear magnetic resonance studies. Plant Physiol 125:921–925

    Google Scholar 

  • Guo K, Xia K, Yang ZM (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452

    CAS  PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011a) On the origins of nitric oxide. Trends Plant Sci 16:160–168

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Igamberdiev AU, Manjunatha G et al (2011b) The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci 181:520–526

    CAS  PubMed  Google Scholar 

  • Gupta KJ, Shah JK, Brotman Y et al (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

    CAS  PubMed  Google Scholar 

  • Hebelstrup KH, van Zanten M, Mandon J et al (2012) Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana. J Exp Bot 63:5581–5591

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hill RD (2012) Non-symbiotic haemoglobins-what’s happening beyond nitric oxide scavenging? AoB Plants 2012:pls004

    Google Scholar 

  • Horchani F, Aschi-Smiti S, Brouquisse R (2010) Involvement of nitrate reduction in the tolerance of tomato (Solanum lycopersicum L.) to prolonged root hypoxia. Acta Physiol Plant 32:1113–1123

    Google Scholar 

  • Horchani F, Prévot M, Boscari A et al (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155:1023–1036

    CAS  PubMed Central  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

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Igamberdiev AU, Seregélyes C, Manac’h N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102

    CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Baron K, Manac’h-Little N et al (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557–564

    CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plant 138:393–404

    CAS  PubMed  Google Scholar 

  • Jin CW, Du ST, Zhang YS et al (2009) Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum). Ann Bot 104:9–17

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kharitonov VG, Sundquist AR, Sharma VS (1994) Kinetics of nitric oxide autoxidation in aqueous solutions. J Biol Chem 269:5881–5883

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA et al (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E et al (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lea PJ (1993) Nitrogen metabolism. In: Lea PJ, Leegood RC (eds) plant biochemistry and molecular biology. Wiley, New York, pp 155–180

    Google Scholar 

  • Leitner M, Vandelle E, Gaupels F et al (2009) NO signals in the haze: Nitric oxide signaling in plant defence. Curr Opin Plant Biol 12:451–458

    CAS  PubMed  Google Scholar 

  • Leterrier M, Chaki M, Airaki M et al (2011) Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal Behav 6:789–793

    CAS  PubMed Central  PubMed  Google Scholar 

  • Logan DC, Millar AH, Sweetlove LJ et al (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malavolta E (1954) Studies on the nitrogenous nutrition of rice. Plant Physiol 29:98–99

    CAS  PubMed Central  PubMed  Google Scholar 

  • Manac’h-Little N, Igamberdiev AU, Hill RD (2005) Hemoglobin expression affects ethylene production in maize cell cultures. Plant Physiol Biochem 43:485–489

    PubMed  Google Scholar 

  • Martí MC, Florez-Sarasa I, Camejo D et al (2013) Response of mitochondrial antioxidant system and respiratory pathways to reactive nitrogen species in pea leaves. Physiol Plant 147:194–206

    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 USA 96:8271–8276

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meakin GE, Bueno E, Jepson B et al (2007) The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules. Microbiology 153:411–449

    CAS  PubMed  Google Scholar 

  • Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398:155–158

    CAS  PubMed  Google Scholar 

  • Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104

    CAS  PubMed  Google Scholar 

  • Modolo LV, Augusto O, Almeida IM et al (2005) Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Lett 579:3814–3820

    CAS  PubMed  Google Scholar 

  • Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants-where do we stand? Physiol Plant 138:372–383

    CAS  PubMed  Google Scholar 

  • Mugnai S, Azzarello E, Baluska F, Mancuso S (2012) Local root apex hypoxia induces NO-mediated hypoxic acclimation of the entire root. Plant Cell Physiol 53:912–920

    CAS  PubMed  Google Scholar 

  • Murphy MP (1999) Nitric oxide and cell death. Biochim Biophys Acta 1411:401–414

    CAS  PubMed  Google Scholar 

  • 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 190:472–487

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ober ES, Sharp RE (1996) A microsensor for direct measurement of O2 partial pressure within plant tissues. J Exp Bot 47:447–457

    CAS  Google Scholar 

  • Oliveira HC, Sodek L (2013) Effect of oxygen deficiency on nitrogen assimilation and amino acid metabolism by soybean root segments. Amino Acids 44:743–755

    Google Scholar 

  • Oliveira HC, Salgado I, Sodek L (2013a) Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia. Planta 237:255–264

    CAS  PubMed  Google Scholar 

  • Oliveira HC, Salgado I, Sodek L (2013b) Nitrite decreases ethanol production by intact soybean roots submitted to oxygen deficiency: a role for mitochondrial nitric oxide synthesis? Plant Signal Behav 8:e23578

    PubMed  Google Scholar 

  • Oliveira HC, Freschi L, Sodek L (2013c) Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency. Plant Physiol Biochem 66:141–149

    CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    CAS  PubMed Central  PubMed  Google Scholar 

  • Palmieri MC, Sell S, Huang X et al (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186

    CAS  PubMed  Google Scholar 

  • Parani MR, Myers R, Weirich H et al (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Perazzolli M, Dominici P, Romero-Puertas MC et al (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794

    CAS  PubMed Central  PubMed  Google Scholar 

  • Planchet E, Jagadis Gupta K et al (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

    CAS  PubMed  Google Scholar 

  • Radi R, Cassina A, Hodara R (2002) Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem 383:401–409

    CAS  PubMed  Google Scholar 

  • Ramirez L, Simontacchi M, Murgia I et al (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. Plant Sci 181:582–592

    CAS  PubMed  Google Scholar 

  • Ramírez-Aguilar SJ, Keuthe M, Rocha M et al (2011) The composition of plant mitochondrial supercomplexes changes with oxygen availability. J Biol Chem 286:43045–43053

    PubMed Central  PubMed  Google Scholar 

  • Roberts JKM, Andrade FH, Anderson IC (1985) Further evidence that cytoplasmic acidosis is a determinant of flooding intolerance in plants. Plant Physiol 77:492–494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rocha M, Licausi F, Araújo WL et al (2010) Glycolysis and the TCA-cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Laxa M, Mattè A et al (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rümer S, Gupta KJ, Kaiser WM (2009) Plant cells oxidize hydroxylamines to NO. J Exp Bot 60:2065–2072

    PubMed Central  PubMed  Google Scholar 

  • Sachs MM, Freeling M, Okimoto R (1980) The anaerobic proteins of maize. Cell 20:761–767

    CAS  PubMed  Google Scholar 

  • Sairam RK, Kumutha D, Ezhilmathi K et al (2008) Physiology and biochemistry of waterlogging tolerance in plants. Biol Plant 52:401–412

    CAS  Google Scholar 

  • Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24

    CAS  PubMed  Google Scholar 

  • Sánchez C, Cabrera JJ, Gates AJ et al (2011) Nitric oxide detoxification in the rhizobia-legume symbiosis. Biochem Soc Trans 39:184–188

    PubMed  Google Scholar 

  • Santos-Filho PR, Vitor SC, Frungillo L et al (2012) Nitrate reductase- and nitric oxide-dependent activation of sinapoylglucose:malate sinapoyltransferase in leaves of Arabidopsis thaliana. Plant Cell Physiol 53:1607–1616

    CAS  PubMed  Google Scholar 

  • Salgado I, Modolo LV, Augusto O et al (2006) Mitochondrial nitric oxide synthesis during plant-pathogen interactions: role of nitrate reductase in providing substrates. In: Lamattina L, Polacco JC (eds) Plant cell monographs, nitric oxide in plant growth, development and stress physiology, vol 6. Springer, Berlin, pp. 239–254

    Google Scholar 

  • Saviani EE, Orsi CH, Oliveira JFP et al (2002) Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett 510:136–140

    CAS  PubMed  Google Scholar 

  • Shingaki-Wells RN, Huang S, Taylor NL et al (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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455

    CAS  PubMed  Google Scholar 

  • Simonin V, Galina A (2013) Nitric oxide inhibits succinate dehydrogenase-driven oxygen consumption in potato tuber mitochondria in an oxygen tension-independent manner. Biochem J 449:263–273

    CAS  PubMed  Google Scholar 

  • 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 166:926–937

    CAS  PubMed  Google Scholar 

  • Sousa CAF, Sodek L (2002) The metabolic response of plants to oxygen deficiency. Braz J Plant Physiol 14:83–94

    Google Scholar 

  • Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Stoimenova M, Libourel IGL, 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

    CAS  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

    CAS  PubMed  Google Scholar 

  • Stuehr DJ, Santolini J, Wang ZQ et al (2004) Update on mechanism and catalytic regulation in the NO synthases. J Biol Chem 279:36167–36170

    CAS  PubMed  Google Scholar 

  • Sturms R, DiSpirito AA, Hargrove MS (2011) Plant and cyanobacterial hemoglobins reduce nitrite to nitric oxide under anoxic conditions. Biochemistry 50:3873–3878

    CAS  PubMed  Google Scholar 

  • Thomas AL, Sodek L (2005) Development of nodulated soybean plant after flooding of the root system with different sources of nitrogen. Braz J Plant Physiol 17:291–297

    CAS  Google Scholar 

  • Tiso M, Tejero J, Kenney C et al (2012) Nitrite reductase activity of nonsymbiotic hemoglobins from Arabidopsis thaliana. Biochemistry 51:5285–5292

    CAS  PubMed  Google Scholar 

  • Trought MCT, Drew MC (1981) Alleviation of injury to young wheat plants in anaerobic solution cultures in relation to the supply of nitrate and other inorganic nutrients. J Exp Bot 32:509–522

    CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T et al (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    CAS  PubMed  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 131:1529–1543

    PubMed Central  PubMed  Google Scholar 

  • van Dongen JT, Fröhlich A, Ramírez-Aguilar SJ et al (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

    PubMed Central  PubMed  Google Scholar 

  • van Faassen EE, Bahrami S, Feelisch M et al (2009) Nitrite as regulator of hypoxic signaling in mammalian physiology. Med Res Rev 29:683–741

    PubMed Central  PubMed  Google Scholar 

  • Vanlerberghe GC, Cvetkovska M, Wang J (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plant 137:392–406

    CAS  PubMed  Google Scholar 

  • Wendehenne D, Hancock JT (2011) New frontiers in nitric oxide biology in plant. Plant Sci 181:507–508

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Yadav S, David A, Bhatla SC (2010) Nitric oxide modulates specific steps of auxin-induced adventitious rooting in sunflower. Plant Signal Behav 5:1163–1166

    CAS  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide: Biol Chem 5:261–270

    CAS  Google Scholar 

  • Zabalza A, van Dongen JT, Froehlich A et al (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zottini M, Formentin E, Scattolin M et al (2002) Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett 515:75–78

    CAS  PubMed  Google Scholar 

Download references

Acknowledgment

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support (grant 473090/2011–2).

Author information

Authors and Affiliations

  1. Departamento de Biologia Animal e Vegetal, Centro de Ciências Biológicas, Universidade Estadual de Londrina (UEL), CP 10011, Londrina, PR, 86057-970, Brazil

    Halley Caixeta Oliveira

  2. Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), CP 6109, Campinas, SP, 13083-970, Brazil

    Ione Salgado

Authors
  1. Halley Caixeta Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ione Salgado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ione Salgado .

Editor information

Editors and Affiliations

  1. Faculty of Science, Department of Biology, University of Tabuk, Tabuk, Saudi Arabia

    M. Nasir Khan

  2. Faculty of Science, Department of Biology, University of Tabuk, Tabuk, Saudi Arabia

    Mohammad Mobin

  3. Plant Physiology Section,Department of Botany, Aligarh Muslim University, Aligarh, India

    Firoz Mohammad

  4. Departamento de Bioquímica Biol. Cellular y Molecular de Plantas, Estación Experimental del Zaidín Consejo Superior de Investigaciones Científicas, Granada, Spain

    Francisco J. Corpas

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Oliveira, H.C., Salgado, I. (2014). Role of Plant Mitochondria in Nitric Oxide Homeostasis During Oxygen Deficiency. In: Khan, M., Mobin, M., Mohammad, F., Corpas, F. (eds) Nitric Oxide in Plants: Metabolism and Role in Stress Physiology. Springer, Cham. https://doi.org/10.1007/978-3-319-06710-0_4

Download citation

Publish with us

Policies and ethics

Search

Navigation