Skip to main content
SpringerLink
Log in

Decarboxylation of glycine contributes to carbon isotope fractionation in photosynthetic organisms

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Carbon isotope effects were investigated for the reaction catalyzed by the glycine decarboxylase complex (GDC; EC 2.1.2.10). Mitochondria isolated from leaves of pea (Pisum sativum L.) and spinach (Spinacia oleracea L.) were incubated with glycine, and the CO2 evolved was analyzed for the carbon isotope ratio (δ13C). Within the range of parameters tested (temperature, pH, combination of cofactors NAD+, ADP, pyridoxal 5-phosphate), carbon isotope shifts of CO2 relative to the C1-carboxyl carbon of glycine varied from +14‰ to −7‰. The maximum effect of cofactors was observed for NAD+, the removal of which resulted in a strong 12C enrichment of the CO2 evolved. This indicates the possibility of isotope effects with both positive and negative signs in the GDC reaction. The measurement of δ13C in the leaves of the GDC-deficient barley (Hordeum vulgare L.) mutant (LaPr 87/30) plants indicated that photorespiratory carbon isotope fractionation, opposite in sign when compared to the carbon isotope effect during CO2 photoassimilation, takes place in vivo. Thus the key reaction of photorespiration catalyzed by GDC, together with the key reaction of CO2 fixation catalyzed by ribulose-1,5-bisphosphate carboxylase, both contribute to carbon isotope fractionation in photosynthesis.

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

  • Arens NC, Jahren AH and Amundson R (2000) Can C3 plants faithfully record the carbon isotopic composition of atmospheric carbon dioxide? Paleobiology 26: 137–164

    Article  Google Scholar 

  • Bergman A and Ericson I (1983) Effects of NADH, succinate and malate on the oxidation of glycine in spinach leaf mitochondria. Physiol Plant 59: 421–427

    Article  CAS  Google Scholar 

  • Blackwell RD, Murray AJS and Lea PJ (1990) Photorespiratory mutants of the mitochondrial conversion of glycine to serine. Plant Physiol 94: 1316–1322

    PubMed  CAS  Google Scholar 

  • Christeller JT, Laing WA and Troughton JH (1976) Isotope discrimination by ribulose 1,5-bisphosphate carboxylase. No effect of temperature or HCO3 - concentration. Plant Physiol 57: 580–582

    PubMed  CAS  Google Scholar 

  • Craig H (1957) Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12: 133–149

    Article  CAS  Google Scholar 

  • Dalziel K and Londesborough JC (1968) The mechanisms of reductive carboxylation reactions. Carbon dioxide or bicarbonate as substrate of nicotinamide-adenine dinucleotide phosphate-linked isocitrate dehydrogenase and ‘malic’ enzyme. Biochem J 110: 223–230

    PubMed  CAS  Google Scholar 

  • Duranceau M, Ghashghaie J, Badeck F, Deleens E and Cornic G (1999) δ 13C of CO2 respired in the dark in relation to δ 13C of leaf carbohydrates in Phaseolus vulgaris L. under progressive drought. Plant Cell Environ 22: 515–523

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR and Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503–537

    Article  CAS  Google Scholar 

  • Gardeström P and Edwards GE (1983) Isolation of mitochondria from leaves of C3, C4, and crassulacean acid metabolism plants. Methods Enzymol 148: 421–432

    Google Scholar 

  • Gillon JS and Griffiths H (1997) The influence of (photo)respiration on carbon isotope discrimination in plants. Plant Cell Environ 20: 1217–1230

    Article  Google Scholar 

  • Gueguen V, Macherel D, Neuburger M, Saint Pierre C, Jaquinod M, Gans P, Douce R and Bourguignon J (1999) Structural and functional characterization of H protein mutants of the glycine decarboxylase complex. J Biol Chem 274: 26344–26352

    Article  PubMed  CAS  Google Scholar 

  • Guy RD, Fogel ML and Berry JA (1993) Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101: 37–47

    PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Ivlev AA, Threlkeld CN and Bykova NV (1998) Mitochondrial oxidative decarboxylation of glycine is a point of carbon isotope fractionation in photosynthetic tissue. In: Møller IM, Gardeström P, Glimelius K and Glaser E (eds) Plant Mitochondria: From Gene to Function, pp 365–369. Backhuys Publishers, Leiden, The Netherlands

    Google Scholar 

  • Igamberdiev AU, Bykova NV, Lea PJ and Gardeström 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 

  • Ivlev AA (1993) On the flows of light and heavy carbon during photosynthesis and photorespiration coupling. Russian J Plant Physiol 40: 752–758

    Google Scholar 

  • Ivlev AA, Bykova NV and Igamberdiev AU (1996) Fractionation of carbon (13C/12C) isotopes in glycine decarboxylase reaction. FEBS Lett 386: 174–176

    Article  PubMed  CAS  Google Scholar 

  • Ivlev AA, Igamberdiev AU, Threlkeld C and Bykova NV (1999a) Carbon isotope effects in the glycine decarboxylase reaction in vitro on mitochondria from pea and spinach. Russian J Plant Physiol 46: 653–660

    CAS  Google Scholar 

  • Ivlev AA, Pichuzkin VI and Knyazev DA (1999b) Developmental changes in the carbon isotope composition of wheat organs in relation to photorespiration. Russian J Plant Physiol 46: 443–451

    CAS  Google Scholar 

  • Jordan F, Kuo DJ and Monse EU (1978) Carbon kinetic isotope effects on pyruvate decarboxylation catalyzed by yeast pyruvate dehydrogenase complex. J Am Chem Soc 100: 2872–2878

    Article  CAS  Google Scholar 

  • Kalinkina LG and Udelnova TM (1991) Mechanism of involvement of the glycolate pathway in accumulation of free proline in a marine Chlorella under conditions of salinity. Sov Plant Physiol 38: 687–696

    Google Scholar 

  • Klein SM and Sagers RD (1966) Glycine metabolism. I. Properties of the system catalyzing the exchange of bicarbonate with the carboxyl group of glycine in Peptococcus glycinophilus. J Biol Chem 241: 197–205

    PubMed  CAS  Google Scholar 

  • Krömer S (1995) Respiration during photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 46: 45–70

    Article  Google Scholar 

  • Lenne C, Neuburger M and Douce R (1993) Effect of high physiological temperatures on NAD+ content of green leaf mitochondria – apparent inhibition of glycine oxidation. Plant Physiol 102: 1157–1162

    PubMed  CAS  Google Scholar 

  • Lennon AM, Pratt J, Leach G and Moore A (1995) Developmental regulation of respiratory activity in pea leaves. Plant Physiol 107: 925–932

    PubMed  CAS  Google Scholar 

  • Lin GH and Ehleringer JR (1997) Carbon isotopic fractionation does not occur during dark respiration in C3 and C4. Plant Physiol 114: 391–394

    PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL and Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275

    PubMed  CAS  Google Scholar 

  • Melander L and Saunders J (1980) Reaction Rates of Isotopic Molecules. Wiley, New York

    Google Scholar 

  • Neuburger M, Polidori AM, Pietre E, Faure M, Jourdain A, Bourguignon J, Pucci B and Douce R (2000) Interaction between the lipoamide-containing H-protein and the lipoamide dehydrogenase (L-protein) of the glycine decarboxylase multienzyme system. 1. Biochemical studies. Eur J Biochem 267: 2882–2889

    Article  PubMed  CAS  Google Scholar 

  • O'Leary MH (1989) Multiple isotope effects on enzyme catalyzed reactions. Annu Rev Biochem 58: 377–401

    Article  PubMed  Google Scholar 

  • Ohlsson KEA and Wallmark PH (1999) Novel calibration with correction for drift and non-linear response for continuous flow isotope ratio mass spectrometry applied to the determination of δ 15N, total nitrogen, δ 13C and total carbon in biological material. Analyst 124: 571–577

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oliver DJ and Sarojini G (1987) Regulation of glycine decarboxylase by serine. In: Biggins J (ed) Progress in Photosynthesis Research, Vol III, pp 573–576. Martinus Nijhoff Publishers, The Hague

    Google Scholar 

  • Oliver DJ, Neuburger M, Bourguignon J and Douce R (1990) Glycine metabolism by plant mitochondria. Physiol Plant 80: 487–491

    Article  CAS  Google Scholar 

  • Park R and Epstein S (1960) Carbon isotope fractionation during photosynthesis. Geochim Cosmochim Acta 21: 110–119

    CAS  Google Scholar 

  • Raven JA and Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of isotopes of carbon in plants. New Phytol 116: 505–529

    Article  CAS  Google Scholar 

  • Sarojini G and Oliver DJ (1987) Glyoxylate and pyridoxal 5-phosphate inhibition of isolated glycine decarboxylase. In: Biggins J (ed) Progress in Photosynthesis Research, Vol III, pp 569–572. Martinus Nijhoff Publishers, The Hague

    Google Scholar 

  • Sarojini G and Oliver DJ (1993) Extraction and partial characterization of the glycine decarboxylase multienzyme complex from pea leaf mitochondria. Plant Physiol 72: 194–199

    Google Scholar 

  • Smith BN and Epstein S (1971) Two categories of 13C/12C ratios for higher plants. Plant Physiol 47: 380–384

    PubMed  CAS  Google Scholar 

  • Tobin AK, Sumar N, Patel M, Moore AL and Stewart GR (1988) Development of photorespiration during chloroplast biogenesis in wheat leaves. J Exp Bot 39: 833–843

    CAS  Google Scholar 

  • Tobin AK, Thorpe JR, Hylton CM and Rawsthorne S (1989) Spatial and temporal influences on the cell-specific distribution of glycine decarboxylase in leaves of wheat (Triticum aestivum L.) and pea (Pisum sativum L.). Plant Physiol 91: 1219–1225

    Article  PubMed  CAS  Google Scholar 

  • Vauclare P, Diallo N, Bourguignon J, Macherel D and Douce R (1996) Regulation of the expression of the glycine decarboxylase complex during pea leaf development. Plant Physiol 112: 1523–1530

    PubMed  CAS  Google Scholar 

  • Wingler A, Lea PJ and Leegood RC (1997) Control of photosynthesis in barley plants with reduced activities of glycine decarboxylase. Planta 202: 171–178

    Article  CAS  Google Scholar 

  • Wingler A, Lea PJ and Leegood RC (1999a) Photorespiratory metabolism of glyoxylate and formate in glycine-accumulating mutants of barley and Amaranthus edulis. Planta 207: 518–526

    Article  CAS  Google Scholar 

  • Wingler A, Quick WP, Bungard RA, Bailey KJ, Lea PJ and Leegood RC (1999b) The role of photorespiration during drought stress: An analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. Plant Cell Environ 22: 361–373

    Article  CAS  Google Scholar 

  • Yates KK and Robbins LL (1999) Radioisotope tracer studies of inorganic carbon and Ca in microbially derived CaCO3. Geochim Cosmochim Acta 63: 129–136

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, 901 87, Umeå, Sweden

    Abir U. Igamberdiev, Natalia V. Bykova & Per Gardeström

  2. Agrochemistry Faculty, K.A.Timiryazev Agricultural Academy, Moscow, 127550, Russia

    Alexander A. Ivlev

  3. US Geology Survey, Denver Federal Centre, CO, 80225, USA

    Charles N. Threlkeld

  4. Department of Biological Sciences, Lancaster University, Lancaster, LA1 4YQ, UK

    Peter J. Lea

Authors
  1. Abir U. Igamberdiev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander A. Ivlev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia V. Bykova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charles N. Threlkeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter J. Lea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Per Gardeström
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abir U. Igamberdiev.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Igamberdiev, A.U., Ivlev, A.A., Bykova, N.V. et al. Decarboxylation of glycine contributes to carbon isotope fractionation in photosynthetic organisms . Photosynthesis Research 67, 177–184 (2001). https://doi.org/10.1023/A:1010635308668

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010635308668

Search

Navigation