Skip to main content
Log in

Denitrification by plant roots? New aspects of plant plasma membrane-bound nitrate reductase

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

A specific form of plasma membrane-bound nitrate reductase in plants is restricted to roots. Two peptides originated from plasma membrane integral proteins isolated from Hordeum vulgare have been assigned as homologues to the subunit NarH of respiratory nitrate reductase of Escherichia coli. Corresponding sequences have been detected for predicted proteins of Populus trichocarpa with high degree of identities for the subunits NarH (75%) and NarG (65%), however, with less accordance for the subunit NarI. These findings coincide with biochemical properties, particularly in regard to the electron donors menadione and succinate. Together with the root-specific and plasma membrane-bound nitrite/NO reductase, nitric oxide is produced under hypoxic conditions in the presence of nitrate. In this context, a possible function in nitrate respiration of plant roots and an involvement of plants in denitrification processes are discussed.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

PM:

Plasma membrane

NR:

Nitrate reductase

NI-NOR:

Nitrite/NO reductase

References

  • Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, Yu Y-K (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J 272:5101–5109

    Article  PubMed  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 44:91–121

    Article  CAS  Google Scholar 

  • Bérczi A, Lüthje S, Asard H (2001) b-type cytochromes in plasma membranes of Phaseolus vulgaris hypocotyls, Arabidopsis thaliana leaves, and Zea mays roots. Protoplasma 217:50–55

    Article  PubMed  Google Scholar 

  • Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH, Strynadka NC (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nat Struct Biol 10:681–687

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Blasco F, Iobbi C, Giordano G, Chippaux M, Bonnefoy V (1989) Nitrate reductase of Escherichia coli: completion of the nucleotide sequence of the nar operon and reassessment of the role of the alpha and beta subunits in iron binding and electron transfer. J Mol Gen Genet 218:249–256

    Article  CAS  Google Scholar 

  • Blasco F, Guigliarelli B, Magalon A, Asso M, Giordano G, Rothery RA (2001) The coordination and function of the redox centres of the membrane-bound nitrate reductases. Cell Mol Life Sci 58:179–193

    Article  PubMed  CAS  Google Scholar 

  • Bonete MJ, Martínez-Espinosa RM, Pire C, Zafrilla B, Richardson DJ (2008) Nitrogen metabolism in haloarchaea. Saline Systems 4:9

    Article  PubMed  Google Scholar 

  • Botrel A, Magne C, Kaiser WM (1996) Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34:645–652

    CAS  Google Scholar 

  • Buc J, Giordani R (1998) A spectrophotometric method for kinetic studies with quinine-dependent oxidoreductase. Application to detection in membranes of nitrate reductase activity with menadione and duroquinone as electron donors. Enzyme Microbial Technol 22:165–169

    Article  CAS  Google Scholar 

  • Eick M, Stöhr C (2009) Proteolysis at the plasma membrane of tobacco roots: biochemical evidence and possible roles. Plant Physiol Biochem 47:1003–1008

    Article  PubMed  CAS  Google Scholar 

  • Einsle O, Kroneck PMH (2004) Structural basis of denitrification. Biol Chem 385:875–883

    Article  PubMed  CAS  Google Scholar 

  • Elliott SJ, Hoke KR, Heffron K, Palak M, Rothery RA, Weiner JH, Armstrong FA (2004) Voltammetric studies of the catalytic mechanism of the respiratory nitrate reductase from Escherichia coli: how nitrate reduction and inhibition depend on the oxidation state of the active site. Biochem 43:799–807

    Article  CAS  Google Scholar 

  • Fan TWM, Higashi RM, Lane AN (1988) An in vivo 1H and 31P NMR investigation of the effect of nitrate on hypoxic metabolism in maize roots. Arch Biochem Biophys 266:592–606

    Article  PubMed  CAS  Google Scholar 

  • Furt F, Simon-Plas F, Mongrand S (2011) Lipids of the plasma membrane. In: Murphy AS, Wendy P, Schulz B (eds) The plant plasma membrane. Plant Cell Monographs 19. Springer, Heidelberg, pp 3–30

    Google Scholar 

  • Hempel K, Pané-Farré J, Otto A, Sievers S, Hecker M, Becher D (2010) Quantitative cell surface proteome profiling for SigB-dependent protein expression in the human pathogen Staphylococcus aureus via biotinylation. J Proteome Res 9:1579–1590

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones GJ, Morel FMM (1988) Plasmalemma redox activity in the diatom Thalassiosira. A possible role for nitrate reductase. Plant Physiol 87:143–147

    Article  PubMed  CAS  Google Scholar 

  • Jormakka M, Richardson D, Byrne B, Iwata S (2004) Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure 12:95–104

    Article  PubMed  CAS  Google Scholar 

  • Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273

    Article  PubMed  CAS  Google Scholar 

  • Kunze M, Riedel J, Lange U, Hurwitz R, Tischner R (1997) Evidence for the presence of GPI-anchored PM-NR in leaves of Beta vulgaris and for PM-NR in barley leaves. Plant Physiol Biochem 35(507):512

    Google Scholar 

  • Lüthje S, Van Gestelen P, Córdoba-Pedregosa MC, González-Reyes JA, Asard H, Villalba JM, Böttger M (1998) Quinones in plant plasma membranes—a missing link? Protoplasma 205:43–51

    Article  Google Scholar 

  • Lüthje S, Hopff D, Schmitt A, Meisrimler C-N, Menckhoff L (2009) Hunting for low abundant redox proteins in plant plasma membranes. J Proteomics 72:475–483

    Article  PubMed  Google Scholar 

  • MacGregor CH (1975) Solubilization of Escherichia coli nitrate reductase by a membrane-bound protease. J Bacteriol 121:1102–1110

    PubMed  CAS  Google Scholar 

  • Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ (2007) Look on the positive side! The orientation, identification and bioenergetics of ‘Archaeal’ membrane-bound nitrate reductases. FEMS Microbiol Lett 276:129–139

    Article  PubMed  CAS  Google Scholar 

  • Meyer C, Stöhr C (2002) Soluble and plasma membrane-bound enzymes involved in nitrate and nitrite metabolism. In: Foyer CH, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Kluwer, Dordrecht, pp 49–62

    Google Scholar 

  • Moche M, Stremlau S, Hecht L, Göbel C, Feussner I, Stöhr C (2010) Effect of nitrate supply and mycorrhizal inoculation on characteristics of tobacco root plasma membrane vesicles. Planta 231:425–436

    Article  PubMed  CAS  Google Scholar 

  • Möller IM, Crane FL (1990) Redox processes in the plasma membrane. In: Larsson C, Möller IM (eds) Plant plasma membrane: structure, function, and molecular biology. Springer, Heidelberg, pp 93–126

    Google Scholar 

  • Müller E, Albers BP, Janiesch P (1994) Influence of nitrate and ammonium nutrition on fermentation, nitrate reductase activity and adenylate energy charge of roots of Carex pseudocyperus L. and Carex sylvatica Huds. exposed to anaerobic nutrient solutions. Plant Soil 166:221–230

    Article  Google Scholar 

  • Oberson J, Pavelic D, Braendle R, Rawyler A (1999) Nitrate increases membrane stability in potato cells under anoxia. J Plant Physiol 155:792–794

    Article  CAS  Google Scholar 

  • Palmgren MG, Bækgaard L, Lóopez-Marqués RL, Fuglsang AT (2011) Plasma membrane ATPases. In: Murphy AS, Wendy P, Schulz B (eds) The plant plasma membrane. Plant Cell Monographs 19. Springer, Heidelberg, pp 177–191

    Google Scholar 

  • Pihlatie M, Ambus P, Rinne J, Pilegaard K, Vesala T (2005) Plant-mediated nitrous oxide emissions from beech (Fagus sylvatica) leaves. New Phytol 168:93–98

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Reck U (2003) Reinigung und biochemische Charakterisierung der plasmamembrangebundenen Nitratreduktase aus Wurzeln von Tabak (Nicotiana tabacum L. cv. Samsun N. N.). Osnabrück. Der Andere Verlag. ISBN 3-89959-139-9

  • Reggiani R, Brambilla I, Bertani A (1985a) Effect of exogenous nitrate on anaerobic metabolism in excised rice roots I. Nitrate reduction and pyridine nucleotide pools. J Exp Bot 36:1193–1199

    Article  CAS  Google Scholar 

  • Reggiani R, Brambilla I, Bertani A (1985b) Effect of exogenous nitrate on anaerobic metabolism in excised rice roots II. Fermentative activity and adenylic energy charge. J Exp Bot 36:1698–1704

    Article  CAS  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Nat Acad Sci USA 91:11841–11843

    Article  PubMed  CAS  Google Scholar 

  • Richardson DJ, van Spanning RJM, Ferguson SJ (2007) The prokaryotic nitrate reductases. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 21–36

    Chapter  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

    Article  PubMed  CAS  Google Scholar 

  • Robinson C, Bolhuis A (2001) Protein targeting by the twin-arginine translocation pathway. Nature Rev Mol Cell Biol 2:350–356

    Article  CAS  Google Scholar 

  • Saglio PH, Drew MC, Pradet A (1988) Metabolic acclimation to anoxia induced by low (2–4 kPa partial pressure) oxygen retreatment (hypoxia) in root tips of Zea mays. Plant Physiol 86:61–66

    Article  PubMed  CAS  Google Scholar 

  • Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847

    Article  PubMed  CAS  Google Scholar 

  • Sodergren EJ, DeMoss JA (1988) narI region of the Escherichia coli nitrate reductase (nar) operon contains two genes. J Bacteriol 170:1721–1729

    PubMed  CAS  Google Scholar 

  • Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186

    Article  PubMed  CAS  Google Scholar 

  • Stöhr C (1999) Relationship of nitrate supply with growth rate plasma membrane-bound and cytosolic nitrate reductase, and tissue nitrate content in tobacco plants. Plant Cell Environ 22:169–177

    Article  Google Scholar 

  • Stöhr C (2007) Nitric oxide—a product of plant nitrogen metabolism. In: Lamattina L, Polacco JC (eds) Nitric oxide in plant growth, development and stress physiology. Springer, Heidelberg, pp 15–34

    Chapter  Google Scholar 

  • Stöhr C, Mäck G (2001) Diurnal changes in nitrogen assimilation of tobacco roots. J Exp Bot 52:1283–1289

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Stöhr C, Ullrich WR (1997) A succinate-oxidizing nitrate reductase is located at the plasma membrane of plant roots. Planta 203:129–132

    Article  Google Scholar 

  • Stöhr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293–2303

    Article  PubMed  Google Scholar 

  • Stöhr C, Schuler F, Tischner R (1995) Glycosyl-phosphatidylinositol anchored proteins exist in the plasma membrane of Chlorella saccharophila (Krüger) Nadson. Plasma-membrane-bound nitrate reductase as an example. Planta 196:284–287

    Article  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 

  • 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 

  • Takaya N (2009) Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi. Biosci Biotechnol Biochem 73:1–8

    Article  PubMed  CAS  Google Scholar 

  • Tischner R, Ward MR, Huffaker RC (1989) Evidence for a plasmamembrane-bound nitrate reductase involved in nitrate uptake of Chlorella sorokiniana. Planta 178:19–24

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, de Pamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa. (Torr & Gray) Sci 313:1596–1604

    CAS  Google Scholar 

  • van Spanning RJM, Richardson DJ, Ferguson ST (2007) Introduction to the biochemistry and molecular biology of denitrification. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 3–20

    Chapter  Google Scholar 

  • Vartapetian BB, Polyakova LI (1999) Protective effect of exogenous nitrate on the mitochondrial ultrastructure of Oryza sativa coleoptiles under strict anoxia. Protoplasma 206:163–167

    Article  CAS  Google Scholar 

  • Vartapetian BB, Andreeva IN, Generozova IP, Polyakova LI, Maslova IP, Dolgikh YI, Stepanova AY (2003) Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. Ann Bot 91:155–172

    Article  PubMed  CAS  Google Scholar 

  • Ward MR, Grimes HD, Huffaker RC (1989) Latent nitrate reductase activity is associated with the plasma membrane of corn roots. Planta 177:470–475

    Article  PubMed  CAS  Google Scholar 

  • Wienkoop S, Schlichting R, Ullrich WR, Stöhr C (2001) Different diurnal cycles of expression of two nitrate reductase transcripts in tobacco roots. Protoplasma 217:15–19

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li R, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X, Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GKS, Yang H (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:266–281

    Article  CAS  Google Scholar 

Download references

Acknowledgment

We thank all former and current members of the Stöhr laboratory for excellent technical assistance. We also thank Dr. Dörte Becher and Martin Moche at the Institute of Microbial Physiology and Molecular Biology (University Greifswald) for the mass spectrometric analysis of the gel samples.

Conflict of interests

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christine Stöhr.

Additional information

Handling Editor: David Robinson

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eick, M., Stöhr, C. Denitrification by plant roots? New aspects of plant plasma membrane-bound nitrate reductase. Protoplasma 249, 909–918 (2012). https://doi.org/10.1007/s00709-011-0355-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-011-0355-5

Keywords

Navigation