Skip to main content

Higher Plant Mitochondria as a Source for NO

  • Chapter
  • First Online:

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 5))

Abstract

Higher plant mitochondria produce nitric oxide (NO) by two separate systems. One is a mitochondrial nitric oxide synthase (NOS), which catalyzes the synthesis of NO and l-citrulline from l-arginine using NAD(P)H. The other one is the respiratory electron transport chain, with the terminal oxidases, CytOx and AOX, which both reduce nitrite to NO. While oxygen is obligatory for the former reaction, the latter activity appears very low in air but high under oxygen deficiency. However, even under anoxia, the rate of nitrite:NO reduction rarely reaches ±1% of respiratory electron transport. For as yet unknown reasons, nitrite:NO reduction appears absent in mitochondria from green leaves. The contribution of NOS and of nitrite reduction to overall NO production, and possible functions of nirite:NO reduction under hypoxia/anoxia are discussed.

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

Buying options

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 PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Arredondo-Peter R, Moran JF, Sarath G, Luan P, Klucas RV (1997) Molecular cloning of the cowpea leghemoglobin II gene and expression of its cDNA in Escherichia coli. Purification and characterization of the recombinant protein. Plant Physiol 114:493–500

    Article  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ, McCabe PF (1999) Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 463:151–154

    Article  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupianez JA, del Rio LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274:36729–36733

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–344

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Butt YKC, Lum JHK, Lo DCL (2003) Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies. Planta 216:762–771

    PubMed  CAS  Google Scholar 

  • Catoni E, Desimone M, Hilpert M, Wipf D, Kunze R, Schneider A, Flügge UI, Schumacher K, Frommer WB (2003) Expression pattern of a nuclear encoded mitochondrial arginine-ornithine translocator gene from Arabidopsis. BMC Plant Biology 3:1

    Article  PubMed  Google Scholar 

  • Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and functions. Trends Plant Sci 10:195–200

    Article  PubMed  CAS  Google Scholar 

  • Ghafourifar P, Richter C (1997) Nitric oxide synthase activity in mitochondria. FEBS Lett 418:291–296

    Article  PubMed  CAS  Google Scholar 

  • Godber BLJ, 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  PubMed  CAS  Google Scholar 

  • Gueguen V, Macherel D, Jaquinod M, Douce R, Bourguignon J (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J Biol Chem 275:5016–5025

    Article  PubMed  CAS  Google Scholar 

  • Giulivi C, Poderoso JJ, Boveris A (1998) Production of nitric oxide by mitochondria. J Biol Chem 273:11038–11043

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–104

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

    Article  PubMed  CAS  Google Scholar 

  • Hentze MW, Kuhn LC (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93:8175–8182

    Article  PubMed  CAS  Google Scholar 

  • Hill RD, Igamberdiev AU, Baron KN (2007) Nitric Oxide as an Alternative Electron Carrier During Oxygen Deprivation (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  • Hoyos ME, Palmieri L, Wertin T, Arrigoni R, Polacco J, Palmieri F (2003) Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast. Plant J 33:1027–1033

    Article  PubMed  CAS  Google Scholar 

  • Kowaltowski AJ (2000) Alternative mitochondrial functions in cell physiopathology: beyond ATP production. Brazilian J Med Biol Res 33:241–250

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kuo WN, Ku TW, Jones DL, Baptiste J (1995) Nitric oxide synthase immunoreactivity in baker's yeasts, lobster and wheat germ. Biochem Arch 11:73–78

    CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

  • Lo DCL, Butt YKC, Chan YSG (2000) False nitric oxide synthase immunoreactivity in Asparagus Bean (Vigna sesquipdalis). Nitric Oxide: Biol Chem 4:175

    Article  CAS  Google Scholar 

  • Meyer C, Stöhr C (2003) Soluble and plasma membrane-bound enzymes involved in nitrate and nitrite metabolism. In: Foyer C, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in photosynthesis and respiration, vol 12. Kluwer, Dordrecht, The Netherlands, pp 49–62

    Google Scholar 

  • Millar AH, Day DA, Mathieu C (2002) Nitric oxide synthesis by plants and its potential impact on nitrogen and respiratory metabolism. In: Foyer C, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in photosynthesis and respiration, vol 12. Kluwer, Dordrecht, The Netherlands, pp 193–204

    Google Scholar 

  • Millar TM, Stevens CR, Benjamin N, Eisenthal R, Harrison R, Blake DR (1998) Xanthine oxidoreductase catalyses the reduction of nitrate and nitrite to nitric oxide under hypoxic conditions. FEBS Lett 427:225–228

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rébeillé F, Macherel D, Mouillon JM, Garin J, Douce R (1997) Folate biosynthesis in higher plants: purification and molecular cloning of a bifunctional 6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase/7,8-dihydropteroate synthase localized in mitochondria. EMBO J 16:947–957

    Article  PubMed  Google Scholar 

  • Ribiero EA, Cunha FQ, Tamashino WMSC, Martins IS (1999) Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells. FEBS Lett 445:283–286

    Article  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  PubMed  CAS  Google Scholar 

  • Salgado I, Modolo LV, Augusto O, Braga MR, Oliveira HC (2007) Mitochondrial Nitric Oxide Synthesis During Plant–Pathogen Interactions: Role of Nitrate Reductase in Providing Substrates (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  • Sen S, Cheema IR (1995) Nitric oxide synthase and calmodulin immunoreactivity in plant embryonic tissue. Biochem Arch 11:221–227

    CAS  Google Scholar 

  • Shiva S, Brookes PS, Patel RP, Anderson PG, Darley-Usmar VM (2001) Nitric oxide partitioning into mitochondrial membranes and the control of respiration at cytochrome c oxidase. Proc Natl Acad Sci USA 98:7212–7217

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Stöhr C (2007) Nitric oxide – a product of plant nitrogen assimilation. In: Lamattina L, Polacco JC (eds) Nitric oxide in plant growth. Plant Cell Monographs, vol 6. Springer, Berlin Heidelberg New York (in press)

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Taylor ER, Nie XZ, MacGregor AW, Hill RD (1994) A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol Biol 24:853–862

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Trevaskis B, Watts RA, Andersson C, Llewellyn D, Hargrove MS, Olson JS, Dennis ES, Peacock WJ (1997) Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proc Natl Acad Sci USA 94:12230–12234

    Article  PubMed  CAS  Google Scholar 

  • Vanlerberghe GC, McIntosh L (1996) Signals regulating the expression of the nuclear gene encoding alternative oxidase of plant mitochondria. Plant Physiol 111:589–595

    PubMed  CAS  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 Biochem 3:261–270

    Article  CAS  Google Scholar 

  • Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA 101:15811–15816

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (DFG), SFB 567 and Ka 456-15/1-3.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Werner M. Kaiser .

Editor information

Lorenzo Lamattina Joseph C. Polacco

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kaiser, W.M., Gupta, K.J., Planchet, E. (2006). Higher Plant Mitochondria as a Source for NO. In: Lamattina, L., Polacco, J.C. (eds) Nitric Oxide in Plant Growth, Development and Stress Physiology. Plant Cell Monographs, vol 5. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2006_081

Download citation

Publish with us

Policies and ethics