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Purification and properties of glycolate oxidase from plants with different photosynthetic pathways: Distinctness of C4 enzyme from that of a C3 species and a C3–C4 intermediate

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Abstract

Glycolate oxidase (GO; EC 1.1.3.1) was purified from the leaves of three plant species:Amaranthus hypochondriacus L.(NAD-ME type C4 dicot),Pisum sativum L. (C3 species) andParthenium hysterophorus L. (C3–C4. intermediate). A flavin moiety was present in the enzyme from all the three species. The enzyme from the C4 plant had a low specific activity, exhibited lower KM for glycolate, and required a lower pH for maximal activity, compared to the C3 enzyme. The enzyme from the C4 species oxidized glyoxylate at <10% of the rate with glycolate, while the GO from the C3 plant oxidized glyoxylate at a rate of about 35 to 40% of that with glycolate. The sensitivity of GO from C4 plant to α-hydroxypyridinemethane sulfonate, 2-hydroxy-3-butynoate and other inhibitors was less than that of the enzyme from C3 source. The properties of GO fromParthenium hysterophorus, were similar to those of the enzyme fromPisum sativum. The characteristics of glycolate oxidase from leaves of a C4 plant,Amaranthus hypochondriacus are different from those of the C3 species or the C3–C4 intermediate.

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Abbreviations

FMN:

flavin mononucleotide

GO:

glycolate oxidase

HBA:

2-hydroxy-3-butynoate

α-HPMS:

α-hydroxypyridinemethane sulfonate

PEP:

phosphoenolpyruvate

PCMB:

p-chloromercuribenzoate

PHMB:

p-hydroxymecuribenzoate

References

  • Andreo CS, Gonzalez DH and Iglesias AA (1987) Higher plant phosphoenolpyruvate carboxylase. Structure and regulation. FEBS Lett 213: 1–8

    Google Scholar 

  • Artus NN and Edwards GE (1985) NAD-malic enzyme from plants. FEBS Lett 182: 225–233

    Google Scholar 

  • Baker AL and Tolbert NE (1967) Purification and some properties of an alternate form of glycollate oxidase. Biochim Biophys Acta 131: 179–187

    Google Scholar 

  • Baumann G and Przybilski CH (1990) 4-substituted 3-hydroxy-1-H pyrrole-2,5-dione derivatives: Inhibition of glycolate oxidase and of photosynthesis inChenopodium album. Biochem Physiol Pflanzen 186: 395–402

    Google Scholar 

  • Behrends W, Rausch U, Löffler H-G and Kindl H (1982) Purification of glycollate oxidase from greening cucumber cotyledons. Planta 156: 566–571

    Google Scholar 

  • Betsche T, Schaller D and Melkonian M (1992) Indentification and characterization of glycolate oxidase and related enzymes from the endocyanotic algaCyanophora paradoxa and pea leaves. Plant Physiol 98: 887–893

    Google Scholar 

  • Canvin DT (1990) Photorespiration and CO2-concentrating mechanisms. In: Dennis DT and Turpin DH (eds) Plant Physiology, Biochemistry and Molecular Biology, pp 253–273. Orient Longmann, Harlow, Essex, UK

    Google Scholar 

  • Cornish-Bowden A (1985) A Fortran program for robust regression of enzyme kinetic data. In: Mayer RJ and Billet E (eds) Techniques in the Life Sciences, B1/II Supplement. Protein and Enzyme Biochemistry, BS 115, pp 1–22. Elsevier Scientific Publishers, Shannon, Ireland

    Google Scholar 

  • Davies DD and Asker H (1983) Synthesis of oxalic acid by enzymes from lettuce leaves. Plant Physiol 72: 134–138

    Google Scholar 

  • Devi MT and Raghavendra AS (1993a) Partial reduction in activities of photorespiratory enzymes in C3–C4 intermediates ofAlternanthera andParthenium. J Exp Bot 44: 779–784

    Google Scholar 

  • Devi MT and Raghavendra AS (1993b) Photorespiration in C3–C4 intermediate species ofAlternanthera andParthenium: Reduced ammonia production and increased capacity of CO2 refixation in the light. Photosynth Res 38: 177–184

    Google Scholar 

  • Devi MT and Raghavendra AS (1994) Formation of photorespiratory glycolate and glyoxylate in leaf discs of C3–C4 intermediates: Reduced sensitivity to external bicarbonate. Photosynthetica 30: 455–463

    Google Scholar 

  • Devi MT, Rajagopalan AV and Raghavendra AS (1995) Predominant localization of mitochondria enriched with glycinedecarboxylating enzymes in bundle sheath cells ofAlternanthera tenella, a C3-C4 intermediate species. Plant Cell Environ 18: 589–594

    Google Scholar 

  • Doravari S and Canvin DT (1980) Effect of butyl 2-hydroxy-3-butynoate on sunflower leaf photosynthesis and photorespiration. Plant Physiol 66: 628–631

    Google Scholar 

  • Emes MJ and Erismann KH (1984) Purification and properties of glycolate oxidase fromLemna minor L. Int J Biochem 16: 1373–1378

    Google Scholar 

  • Fendrich G and Ghisla S (1982) Studies on glycollate oxidase from pea leaves. Determination of stereospecificity and mode of inhibition by α-hydroxybutynoate. Biochim Biophys Acta 702: 242–248

    Google Scholar 

  • Frigerio NA and Harbury HA (1958) Preparation and some properties of crystalline glycollic acid oxidase of spinach. J Biol Chem 231: 135–157

    PubMed  Google Scholar 

  • Gross W and Beevers H (1989) Subcellular distribution of enzymes of glycolate metabolism in the algaCyanidium caldarium. Plant Physiol 90: 799–805

    Google Scholar 

  • Huang AHC, Trelease RN and MooreJr THS (1983) Plant Peroxisomes. Academic Press, New York

    Google Scholar 

  • Iwamoto K and Ikawa T (1992) Purification and characterization of glycolate oxidase from brown algaSpatoglossum pacificum. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 919–922. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Kerr MW and Groves D. (1975) Purification and properties of glycolate oxidase fromPisum sativum leaves. Phytochemistry 14: 359–362

    Google Scholar 

  • Kindl H (1982) Glyoxysome biogenesis via cytosolic pools. Ann NY Acad Sci 386: 314–326

    Google Scholar 

  • Kuckzmak M and Tolbert NE (1962) Glycolic acid oxidase formation in greening leaves. Plant Physiol 37: 729–734

    Google Scholar 

  • Leegood RC (1993) The Calvin cycle and photorespiration. In: Lea PJ and Leegood RC (eds) Plant Biochemistry and Molecular Biology, pp 27–45. John Wiley and Sons Ltd, Chichester, UK

    Google Scholar 

  • Lindquist Y and Bränden C-I (1979) Preliminary crystallographic data for glycollate oxidase from spinach. J Biol Chem 154: 7403–7404

    Google Scholar 

  • Lindquist Y and Bränden C-I (1980) Structure of glycolate oxidase from spinach at a resolution of 5.5 Å. J Mol Biol 143: 201–211

    PubMed  Google Scholar 

  • Lindquist Y and Bränden C-I (1985) Structure of glycolate oxidase from spinach. Proc Natl Acad Sci USA 82: 6855–6859

    Google Scholar 

  • Liu AY and Black CCJr (1972) Glycolate metabolism in mesophyll cells and bundle sheath cells isolated from crabgrassDigitaria sanguinalis (L.) Scop., leaves. Arch Biochem Biophys 149: 269–280

    PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL and Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 93: 265–272

    Google Scholar 

  • Morgan CL, Turner SR and Rawsthorne S (1993) Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C3–C4 intermediate species from different genera. Planta 190: 468–473.

    Google Scholar 

  • Nishimura M, Akhmedov YD, Strazalka K and Akazawa T (1983) Purification and characterization of glycolate oxidase from pumpkin cotyledons. Arch Biochem Biophys 222: 397–402

    PubMed  Google Scholar 

  • Ogren WL (1984) Photorespiration: Pathways, regulation and modification. Annu Rev Plant Physiol 35: 415–442

    Google Scholar 

  • Rajagopalan AV, Devi MT and Raghavendra AS (1994) Molecular biology of C4 phosphoenolpyruvate carboxylase: Structure, regulation and genetic engineering. Photosynth Res 39: 115–135

    Google Scholar 

  • Rawsthorne S (1992) C3–C4 intermediate photosynthesis: Linking physiology to gene expression. Plant J 2: 267–274

    Google Scholar 

  • Rawsthorne S, vonCammerer S, Brroks A and Leegood RC (1992) Metabolic interactions in leaves of C3–C4 intermediate plants. In: Tobin AK (ed) Plant Organelles, pp 113–139. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Richardson KE and Tolbert NE (1963) Oxidation of glycolic acid to oxalic acid by glycolic acid oxidase. J Biol Chem 236: 1280–1284

    Google Scholar 

  • Salin ML and Homann PH (1973) Glycolate metabolism in young and old tobacco leaves, and effects of α-hydroxy-2-pyridine methane sulphonic acid. Can J Bot 51: 1857–1865

    Google Scholar 

  • Shapiro AL, Vinuela E and Maizel JVJr (1967) Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun 29: 815–820

    Google Scholar 

  • Stabenau H and Säftel W (1982) A peroxisomal glycollate oxidase in the algaMougoetia. Planta 154: 165–176

    Google Scholar 

  • Tolbert NE (1981) Metabolic pathways in peroxisomes and glyoxysomes. Annu Rev Biochem 50: 133–157

    PubMed  Google Scholar 

  • Tolbert NE, Clagett CO and Burris RH (1949) Products of the oxidation of glycollic acid andl-lactic acid by enzymes from tobacco leaves. J Biol Chem 181: 905–914

    PubMed  Google Scholar 

  • Wessinger ME, Edwards GE and Ku MSB (1989) Quality and kinetic propeties of ribulose 1,5-bisphosphate carboxylase in C3, C4, C3–C4 intermediate species ofFlaveria (Asteraceae). Plant Cell Physiol 30: 665–677.

    Google Scholar 

  • Yin Z-H, Heber U and Raghavendra AS (1993) Light-induced pH changes in leaves of C4 plants. Comparison of cytosolic alkalization and vacuolar acidification with that of C3 plants. Planta 189: 267–277.

    Google Scholar 

  • Zelitch I (1992) Control of plant productivity by regulation of photorespiration. Bioscience 42: 510–516

    Google Scholar 

  • Zelitch I and Ochoa S (1953) Oxidation and reduction of glycolic and glyoxylic acids in plants. 1. Glycolic acid oxidase. J Biol Chem 201: 707–718

    PubMed  Google Scholar 

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Devi, M.T., Rajagopalan, A.V. & Raghavendara, A.S. Purification and properties of glycolate oxidase from plants with different photosynthetic pathways: Distinctness of C4 enzyme from that of a C3 species and a C3–C4 intermediate. Photosynth Res 47, 231–238 (1996). https://doi.org/10.1007/BF02184284

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  • DOI: https://doi.org/10.1007/BF02184284

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