Skip to main content
Log in

Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3-C4 intermediate species of Moricandia

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Photorespiratory metabolism of the C3-C4 intermediate species Moricandia arvensis (L.) DC has been compared with that of the C3 species, Moricandia moricandioides (Boiss.) Heywood. Assays of glycollate oxidase (EC 1.1.3.1), glyoxylate aminotransferases (EC 2.6.1.4, EC 2.6.1.45) and hydroxypyruvate reductase (EC 1.1.1.29) indicate that the capacity for flux through the photorespiratory cycle is similar in both species. Immunogold labelling with monospecific antibodies was used to investigate the cellular locations of ribulose 1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39), glycollate oxidase, and glycine decarboxylase (EC 2.1.2.10) in leaves of the two species. Ribulose 1,5-bisphosphate carboxylase/oxygenase was confined to the stroma of chloroplasts and glycollate oxidase to the peroxisomes of all photosynthetic cells in leaves of both species. However, whereas glycine decarboxylase was present in the mitochondria of all photosynthetic cells in M. moricandioides, it was only found in the mitochondria of bundle-sheath cells in M. arvensis. We suggest that localized decarboxylation of glycine in the leaves of M. arvensis will lead to improved recapture of photorespired CO2 and hence a lower rate of photorespiration.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

kDa:

kilodalton

RuBP:

ribulose-1,5-bisphosphate

References

  • Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24, 1–15

    Google Scholar 

  • Bergman, A., Gardestrom, P., Ericson, I. (1980) Method to obtain a chlorophyll-free preparation of intact mitochondria from spinach leaves. Plant Physiol. 66, 442–445

    Google Scholar 

  • Blake, M.S., Johnston, K.H., Russell-Jones, G.J., Gotschlich, E.C. (1984) A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal. Biochem. 136, 175–179

    PubMed  Google Scholar 

  • Bouton, J.H., Brown, R.H., Evans, P.T., Jernstedt, J.A. (1986) Photosynthesis, leaf anatomy, and morphology of progeny from hybrids between C3 and C3/C4 Panicum species. Plant Physiol. 80, 487–492

    Google Scholar 

  • Brown, R.H. (1980) Photosynthesis of grass species differing in carbon dioxide fixation pathways. IV. Analysis of reduced oxygen response in Panicum milioides and Panicum schenckii. Plant Physiol. 65, 346–349

    Google Scholar 

  • Day, D.A., Neuburger, M., Douce, R. (1985a) Biochemical characterization of chlorophyll-free mitochondria from pea leaves. Aust. J. Plant Physiol. 12, 219–228

    Google Scholar 

  • Day, D.A., Neuburger, M., Douce, R. (1985b) Interactions between glycine decarboxylase, the tricarboxylic acid cycle and the respiratory chain in pea leaf mitochondria. Aust. J. Plant Physiol. 12, 119–130

    Google Scholar 

  • Douce, R. (1985) Mitochondria in higher plants. Structure, function, and biogenesis. Academic Press, New York London

    Google Scholar 

  • Edwards, G.E., Walker, D.A. (1983) C3, C4: Mechanisms, and cellular and environmental regulation, of photosynthesis. Blackwell Scientific, Oxford London

    Google Scholar 

  • Estabrook, R.W. (1967) Mitochondrial respiratory control and the polarographic measurement of ADP: O ratios. Methods Enzymol. 10, 41–47

    Google Scholar 

  • Hall, N.P., Reggiani, R., Lea, P.J. (1985) Molecular weights of glycollate oxidase from C3 and C4 plants determined during early stages of purification. Phytochemistry 24, 1645–1648

    Article  Google Scholar 

  • Holaday, A.S., Shieh, Y.-J., Lee, K.W., Chollet, R. (1981) Anatomical, ultrastructural and enzymic studies of leaves of Moricandia arvensis, a C3-C4 intermediate species. Biochim. Biophys. Acta 637, 334–341

    Google Scholar 

  • Holbrook, G.P., Chollet, R. (1986) Photorespiratory properties of protoplasts from C3-C4 intermediate species of Moricandia. Plant Sci. 46, 87–96

    Article  Google Scholar 

  • Hunt, S., Smith, A.M., Woolhouse, H.W. (1987) Evidence for a light-dependent system for reassimilation of photorespiratory CO2, which does not include a C4 cycle, in the C3-C4 intermediate species Moricandia arvensis. Planta 171, 227–234

    Google Scholar 

  • Jackson, C., Dench, J.E., Hall, D.O., Moore, A.L. (1979) Separation of mitochondria from contaminating subcellular structures utilizing silica sol gradient centrifugation. Plant Physiol. 64, 150–153

    Google Scholar 

  • Jensen, R.G., Bahr, J.T. (1977) Ribulose 1,5-bisphosphate carboxylase-oxygenase. Annu. Rev. Plant Physiol. 28, 379–400

    Article  Google Scholar 

  • Jensen, W.A. (1962) Botanical histochemistry. W.H. Freeman and Co., San Francisco

    Google Scholar 

  • Kohn, L.D., Utting, J.M. (1982) Hydroxypyruvate reductase (d-glycerate dehydrogenase) from Pseudomonas. Methods Enzymol. 89, 341–345

    PubMed  Google Scholar 

  • Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

    PubMed  Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. (1951) Protein measurement with Folin-phenol reagent. J. Biol. Chem. 193, 265–275

    PubMed  Google Scholar 

  • Monson, R.K., Edwards, G.E., Ku, M.S.B. (1984) C3-C4 intermediate photosynthesis in plants. Bioscience 34, 563–574

    Google Scholar 

  • Nash, D., Wiskich, J.T. (1983) Properties of substantially chlorophyll-free pea leaf mitochondria prepared by sucrose density gradient separation. Plant Physiol. 71, 627–634

    Google Scholar 

  • Neuburger, M., Journet, E.P., Bligny, R., Carde, J.P., Douce, R. (1982) Purification of plant mitochondria by isopycnic centrifugation in density gradients of Percoll. Arch. Biochem. Biophys. 217, 312–323

    PubMed  Google Scholar 

  • Nishimura, M., Douce, R., Akazawa, T. (1982) Isolation and characterization of metabolically competent mitochondria from spinach leaf protoplasts. Plant Physiol. 69, 916–920

    Google Scholar 

  • O'Brien, T.P., McCully, M.E. (1981) The study of plant structure. Principles and selected methods. Termarcarphi Pty. Ltd., Melbourne

    Google Scholar 

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

    Article  Google Scholar 

  • Ohnishi, J., Kanai, R. (1983) Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants. I. Glycine oxidation by mitochondria. Plant Cell Physiol. 24, 1411–1420

    Google Scholar 

  • Perrot-Rechenmann, C., Chollet, R., Gadal, P. (1984) In situ immunofluorescent localization of phosphoenolpyruvate and ribulose 1,5-bisphosphate carboxylases in leaves of C3, C4, and C3-C4 intermediate Panicum species. Planta 161, 266–271

    Google Scholar 

  • Petit, P., Cantrel, C. (1986) Mitochondria from Zea mays leaf tissues: Differentiation of carbon assimilation and photorespiratory activity between mesophyll and bundle sheath cells. Physiol. Plant. 67, 442–446

    Google Scholar 

  • VandenBosch, K.A. (1986) Light and electron microscopic visualization of uricase by immunogold labelling of sections of resin-embedded soybean nodules. J. Microsc. 143, 187–197

    Google Scholar 

  • Walker, J.L., Oliver, D.J. (1986) Glycine decarboxylase multienzyme complex. Purification and partial characterization from pea leaf mitochondria. J. Biol. Chem. 261, 2214–2221

    PubMed  Google Scholar 

  • Walton, N.J., Woolhouse, H.W. (1986) Enzymes of serine and glycine metabolism in leaves and non-photosynthetic tissues of Pisum sativum L. Planta 167, 119–128

    Google Scholar 

  • Wells, B. (1985) Low temperature box and tissue handling device for embedding biological tissue for immunostaining in electron microscopy. Micron Microsc. Acta 16, 49–53

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rawsthorne, S., Hylton, C.M., Smith, A.M. et al. Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3-C4 intermediate species of Moricandia . Planta 173, 298–308 (1988). https://doi.org/10.1007/BF00401016

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00401016

Key words