Skip to main content
SpringerLink
Log in

The re-assimilation of ammonia produced by photorespiration and the nitrogen economy of C3 higher plants

  • Personal perspective
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Photorespiration involves the conversion of glycine to serine with the release of ammonia and CO2. In C3 terrestrial higher plants the flux through glycine and serine is so large that it results in the production of ammonia at a rate far exceeding that from reduction of new nitrogen entering the plant. The photorespiratory nitrogen cycle re-assimilates this ammonia using the enzymes glutamine synthetase and glutamine:2-oxoglutarateaminotransferase.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Artus NN, Naito S, Somerville CR, (1994) A mutant of Arabidopsis thaliana that defines a new locus for glycine decarboxylation Plant Cell Physiol 35:879–885

    CAS  Google Scholar 

  • Bassham JA, (2003) Mapping the carbon reduction cycle: a personal perspective Photosynth Res 76: 35–52

    Article  PubMed  Google Scholar 

  • Benson AA, (2002) Following the path of carbon in photosynthesis: a personal story Photosynth Res 73: 29–49

    Article  PubMed  CAS  Google Scholar 

  • Bird IF, Porter HK, Stocking CR, (1965) Intracellular localisation of enzymes associated with sucrose synthesis in leaves Biochim Biophys Acta 100: 366–365

    PubMed  CAS  Google Scholar 

  • Bird IF, Keys AJ, Whittingham CP, (1971) Intracellular location of enzymes of the glycolate pathway In: Forti G, Avron M, Melandri A, (eds) Proceedings of the Second International Congress on Photosynthesis Research Dr. W Junk The Hague pp 2215–2224

    Google Scholar 

  • Bird IF, Cornelius MJ, Keys AJ, Whittingham CP, (1972a) Oxidation and phosphorylation associated with the conversion of glycine to serine Phytochemistry 11: 1587–1594

    Article  CAS  Google Scholar 

  • Bird IF, Cornelius MJ, Keys AJ, Whittingham CP, (1972b) Adenosine triphosphate synthesis and the natural electron acceptor for synthesis of serine from glycine in leaves Biochem J 128: 191–192

    CAS  Google Scholar 

  • Bird IF, Cornelius MJ, Dyer TA, Keys AJ, (1973) The purity of chloroplasts isolated in non-aqueous media J Exp Bot 24: 211–215

    Article  CAS  Google Scholar 

  • Bird IF, Cornelius MJ, Keys AJ, Whittingham CP, (1974) Intracellular site of sucrose synthesis in leaves Phytochemistry 13: 59–64

    Article  CAS  Google Scholar 

  • Bird IF, Cornelius MJ, Keys AJ, Whittingham CP, (1978) Intramolecular labelling of sucrose made by leaves from [14C] carbon dioxide or [3–14C] serine Biochem J 172: 23–27

    PubMed  CAS  Google Scholar 

  • Blackwell RD, Murray AJS, Lea PJ, (1987) Inhibition of photosynthesis in barley with decreased levels of chloroplast glutamine synthetase activity J Exp Bot 38: 1799–1809

    Article  CAS  Google Scholar 

  • Douce R, Moore AL, Neuberger M, (1977) Isolation and oxidative properties of intact mitochondria isolated from spinach leaves Plant Physiol 60: 625–628

    PubMed  CAS  Google Scholar 

  • Douce R, Bourguignon J, Macheral D, Neuberger M, (1994) The glycine decarboxylase system in higher plant mitochondria: structure, function and bioenergetics Biochem Soc Trans 22: 184–188

    PubMed  CAS  Google Scholar 

  • Galmes J, Flexas J, Keys AJ, Cifre J, Mitchell AC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ, (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves Plant Cell Environ 28: 571–575

    Article  CAS  Google Scholar 

  • Gerhardt R, Heldt HW, (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in nonaqueous media Plant Physiol 75: 542–547

    Article  PubMed  Google Scholar 

  • Goldsworthy A, (1966) Experiments on the origin of CO2 released by tobacco leaf segments in the light Phytochemistry 5: 1013–1019

    Article  CAS  Google Scholar 

  • Goldsworthy A, (1970) Photorespiration Bot Rev 36: 321–340

    Article  CAS  Google Scholar 

  • Hickman SA, Keys AJ, (1971) Photorespiration in maize and tobacco leaves In: Forti G, Avron M, Melandri A, (eds) Proceedings of the Second International Congress on Photosynthesis Research Dr. W Junk The Hague pp 2225–2231

    Google Scholar 

  • Igamberdiev AU, Bykova NV, Lea PJ, Gardestrom P, (2001) The role of photorespiration in redox and energy balance of photosynthetic plant cells, a study with a barley mutant deficient in glycine decarboxylase Physiol Plant 111: 427–438

    Article  PubMed  CAS  Google Scholar 

  • Kendall AC, Wallsgrove RM, Hall NP, Turner JC, Lea PJ, (1986) Carbon and nitrogen assimilation in barley (Hordeum vulgare L.) mutants lacking ferredoxin-dependent glutamate synthase Planta 168: 316–323

    Article  CAS  Google Scholar 

  • Keys AJ (1973) Biochemical aspects of the conversion of inorganic nitrogen into plant protein. In: Jones JGW (ed) The Biological Efficiency of Protein Production, pp 69–82. Cambridge University Press, Cambridge

  • Keys AJ, (1986) Rubisco: its role in photorespiration Phil Trans R Soc Lond B313: 325–326

    Google Scholar 

  • Keys AJ (1999) In: Bryant JA, Burrell MM and Kruger NJ (eds) Plant Carbohydrate Biochemistry, pp 147–162. BIOS Scientific Publishers, Oxford, UK

  • Keys AJ and Leegood RC (2002) Photorespiratory carbon and nitrogen cycling: evidence from studies of mutant and transgenic plants. In: Foyer CH and Noctor G (eds) Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism. Kluwer Academic Publishers, Dordrecht, The Netherlands

  • Keys AJ, Bird IF, Cornelius MJ, Lea PJ, Wallsgrove RM, Miflin BJ, (1978) Photorespiratory nitrogen cycle Nature 275: 741–743

    Article  Google Scholar 

  • Kisaki T, Yoshida N, Imai A, (1971) Glycine decarboxylase and serine formation in spinach leaf mitochondrial preparation with reference to photorespiration Plant Cell Physiol 12: 275–288

    CAS  Google Scholar 

  • Kumarasinghe KS, Keys AJ, Whittingham CP, (1977a) The flux of carbon through the glycolate pathway during photosynthesis by wheat leaves J Exp Bot 28: 1247–1257

    Article  CAS  Google Scholar 

  • Kumarasinghe KS, Keys AJ, Whittingham CP, (1977b) Effects of certain inhibitors on photorespiration by wheat leaf segments J Exp Bot 28: 1163–1168

    Article  CAS  Google Scholar 

  • Lea PJ, Miflin BJ, (2003) Glutamate synthase and the synthesis of glutamate in plants Plant Physiol Biochem 41: 555–564

    Article  CAS  Google Scholar 

  • Ludwig LJ, Canvin DT, (1971) An open gas-exchange system for the simultaneous measurement of the CO2 and 14CO2 fluxes in leaves Can J Bot 49: 1299–1313

    CAS  Google Scholar 

  • Ludwig LJ, Krotkov G and Canvin DT (1969) The relationship of the products of photosynthesis to the substrates of for CO2 evolution in light and darkness. In: Metzner H (ed) Progress in Photosynthetic Research, Vol 1, pp 494–502

  • Miflin BJ, (1983) Glutamine metabolism: the key to the flow of nitrogen in plants In: Akazawa T, Asahi T, Imasaki H., Eds The New Frontiers in Plant Biochemistry Japan Scientific Societies Press, Tokyo and Martinus Nijhoff/Dr W Junk Publishers The Hague 93–106

    Google Scholar 

  • Murray AJS, Blackwell RD, Joy KW, Lea PJ, (1987) Photorespiratory N donors, aminotransferase specificity and photosynthesis in a mutant barley deficient in serine glyoxylate aminotransferase activity Planta 172: 106–103

    Article  CAS  Google Scholar 

  • Ogren WL, (2003) Affixing the O to Rubisco: discovering the source of photorespiratory glycolate and its regulation Photosynth Res 76: 53–63

    Article  PubMed  CAS  Google Scholar 

  • Oliver DJ, (1994) The glycine decarboxylase complex from plant mitochondria Ann Rev Plant Physiol Mol Biol 45: 323–337

    Article  CAS  Google Scholar 

  • Pierpoint WS, (1959) Mitochondrial preparations from leaves of tobacco (Nicotiana tabacum) Biochem J 71: 518–528

    PubMed  CAS  Google Scholar 

  • Rachmilevitch S, Cousins AB, Bloom AJ, (2004) Nitrate assimilation in plant shoots depends on photorespiration Proc Natl Acad Sci 101: 11506–11510

    Article  PubMed  CAS  Google Scholar 

  • Roberts GR, Keys AJ, Whittingham CP, (1970) The transport of photosynthetic products from chloroplasts of tobacco leaves J Exp Bot 21: 683–692

    Article  CAS  Google Scholar 

  • Somerville CR, (2001) An early Arabidopsis demonstration. Resolving a few issues concerning photorespiration Plant Physiol 125: 20–24

    Article  PubMed  CAS  Google Scholar 

  • Somerville CR, Ogren WL, (1979) A phosphoglycolate phosphatase-deficient mutant in Arabidopsis Nature 280: 833–836

    Article  CAS  Google Scholar 

  • Somerville CR, Ogren WL, (1980a) Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity Nature 286: 257–259

    Article  CAS  Google Scholar 

  • Somerville CR, Ogren WL, (1980b) Photorespiratory mutants of Arabidopsis thaliana deficient in serine-glyoxylate aminotransferease activity Proc Natl Acad Sci USA 77: 2684–2687

    Article  CAS  Google Scholar 

  • Somerville CR, Ogren WL, (1981) Photorespiratory deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity Plant Physiol 67: 666–671

    PubMed  CAS  Google Scholar 

  • Somerville CR, Ogren WL, (1982) Mutants of the cruciferous plant Arabidopsis thaliana lacking gycine decarboxylase activity Biochem J 202: 373–380

    PubMed  CAS  Google Scholar 

  • Stocking CR, (1959) Chloroplast isolation in nonaqueous media Plant Physiol 34: 56–61

    PubMed  CAS  Google Scholar 

  • Stocking CR, Shumway LK Weier TE, Greenwood D, (1968) Ultrastructure of chloroplasts isolated by nonaqueous extraction J Cell Biol 36: 270–275

    Article  CAS  PubMed  Google Scholar 

  • Taira M, Valtersson U, Burkhardt B, Ludwig RA, (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts Plant Cell 16: 2048–2058

    Article  PubMed  CAS  Google Scholar 

  • Tolbert NE, Benker C, Beck E, (1995) The oxygen and carbon dioxide compensation points of C3 plants – possible role in regulating atmospheric oxygen Proc Natl Acad Sci USA 92: 11230–11233

    Article  PubMed  CAS  Google Scholar 

  • Uemura K, Anwarussaman, Miyachi S, Yokota A, (1997) Ribulose−1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation Biochem Biophys Res Commun 233: 568–571

    Article  PubMed  CAS  Google Scholar 

  • Waidyanatha UPdeS, Keys AJ, Whittingham CP, (1975a) Effects of carbon dioxide on metabolism by the glycolate pathway in leaves J Exp Bot 26: 15–26

    Article  CAS  Google Scholar 

  • Waidyanatha UPdeS, Keys AJ, Whittingham CP, (1975b) Effects of oxygen on metabolism by the glycolate pathway in leaves J Exp Bot 26: 27–32

    Article  CAS  Google Scholar 

  • Walker DA, (2003) Chloroplasts in envelopes: CO2 fixation by fully functional chloroplasts Photosynth Res 76: 319–327

    Article  PubMed  CAS  Google Scholar 

  • Wallsgrove RM, Keys AJ, Bird IF, Cornelius MJ, Lea PJ, Miflin BJ, (1980) The location of glutamine synthetase in leaf cells and its role in the reassimilation of ammonia released in photorespiration J Exp Bot 31: 1005–1017

    Article  CAS  Google Scholar 

  • Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ, (1987) Barley mutants lacking chloroplast glutamine synthetase: biochemical and genetic analysis Plant Physiol 83: 155–158

    PubMed  CAS  Google Scholar 

  • Weissman GS, Keys AJ, (1969) Root growth with ammonium and nitrate in continuous flow nutrient solution Bull Torrey Bot Club 96: 149–155

    Article  CAS  Google Scholar 

  • Woo KC, Osmond CB, (1976) Glycine decarboxylation in mitochondria isolated from spinach leaves Aust J Plant Physiol 3: 771–785

    CAS  Google Scholar 

  • Woo KC, Osmond CB, (1977) Participation of leaf mitochondria in the photorespiratory carbon oxidation cycle: glycine decarboxylation activity in leaf mitochondria from different species and its intra-mitochondrial location Plant Cell Physiol – Special Issue 315–323

    Google Scholar 

  • Zelitch I, (1979) Photosynthesis and plant productivity Chem Eng News 5: 28–48

    Google Scholar 

Download references

Acknowledgements

I could not have taken part in the research described above without the encouragement and help of my late wife, Jessie. My thanks to Peter Lea and Ben Miflin for reading a draft of the manuscript and for the improvements they suggested. This paper was read by William Ogren; it was invited and edited by Govindjee.

Author information

Authors and Affiliations

  1. Rothamsted Research, Crop Production & Improvement Division, West Common, AL5 2JQ, Harpenden, Hertfordshire, UK

    Alfred J. Keys

Authors
  1. Alfred J. Keys
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alfred J. Keys.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Keys, A.J. The re-assimilation of ammonia produced by photorespiration and the nitrogen economy of C3 higher plants. Photosynth Res 87, 165–175 (2006). https://doi.org/10.1007/s11120-005-9024-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-005-9024-x

Keywords

Search

Navigation