Skip to main content
Log in

Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: Metabolites related to the redox status and sucrose biosynthesis

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The patterns of cellular metabolites related to redox status and sucrose biosynthesis in mesophyll protoplasts of pea (Pisum sativum L.) were examined in the absence or presence of oligomycin (inhibitor of oxidative phosphorylation) or antimycin A (inhibitor of cytochrome pathway) or salicylhydroxamic acid (SHAM) (inhibitor of alternative pathway). The increase on illumination in the rate of photosynthesis or cellular metabolites was more at optimal CO2 (1.0 mM NaHCO3) compared to that at limiting CO2 (0.1 mM NaHCO3). Furthermore, the inhibition of photosynthesis in presence of mitochondrial inhibitors was more pronounced at optimal CO2 than that at limiting CO2. There was a marked increase in steady-state levels of triose-P/PGA (phosphoglyceric acid) and glucose-6-phosphate (Glc-6-P) in the presence of oligomycin and antimycin A. In contrast, SHAM caused a marked increase in malate/OAA (oxaloacetate). We suggest that dissipation of excess redox equivalents generated in photosynthesis occurs through both cytochrome and alternative pathways, while sucrose biosynthesis is backed up by cytochrome pathway alone. Thus, mitochondrial respiration (through both cytochrome and alternative pathways of mitochondrial electron transport) optimizes chloroplast photosynthesis by modulating cellular metabolites related to both intracellular redox state and sucrose biosynthesis.

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.

Similar content being viewed by others

References

  • Agostino A, Heldt HW and Hatch MD (1996) Mitochondrial respiration in relation to photosynthetic C4 acid decarboxylation in C4 species. Aust J Plant Physiol 23: 1–7

    Google Scholar 

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

    Google Scholar 

  • Backhausen JE, Kitzmann C and Scheibe R (1994) Competition between electron acceptors in photosynthesis: Regulation of the malate valve during CO2 fixation and nitrite reduction. Photosynth Res 42: 75–86

    Google Scholar 

  • Bergmeyer HU (1983) Methods of Enzymatic Analysis, Ed 3. Verlag Chemie, Weinheim, Germany

    Google Scholar 

  • Day DA and Wiskich JT (1995) Regulation of alternative oxidase activity in higher plants. J Bioenerg Biomembr 27: 379–385

    PubMed  Google Scholar 

  • Doncaster HD, Adcock MD and Leegood RC (1989) Regulation of photosynthesis in leaves of C4 plants following a transition from high to low CO2. Biochim Biophys Acta 973: 176–184

    Google Scholar 

  • Gardeström P (1993) Metabolite levels in the chloroplast and extrachloroplast compartments of barley leaf protoplasts during the initial phase of photosynthetic induction. Biochim Biophys Acta 1183: 327–332

    Google Scholar 

  • Gardeström P and Lernmark U (1995) The contribution of mitochondria to energetic metabolism in Photosynthetic cells. J Bioenerg Biomembr 27: 415–421

    PubMed  Google Scholar 

  • Heineke D, Riens B, Grosse G, Hoferichter P, Peter U, Flügge U-I and Heldt HW(1991) Redox transfer across the inner chloroplast envelope membrane. Plant Physiol 95: 1131–1137

    Google Scholar 

  • Heldt HW (1997) Plant Biochemistry and Molecular Biology. Oxford University Press, Oxford, UK

    Google Scholar 

  • Igamberdiev AU, Hurry V, Krömer S and Gardeström P (1998) The role of mitochondrial electron transport during photosynthetic induction. A study with barley (Hordeum vulgare) protoplasts incubated with rotenone and oligomycin. Physiol Plant 104: 431–439

    Google Scholar 

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

    Google Scholar 

  • Krömer S and Heldt HW (1991) On the role of mitochondrial oxidative phosphorylation in photosynthesis metabolism as studied by the effect of oligomycin on photosynthesis in protoplasts and leaves of barley (Hordeum vulgare). Plant Physiol 95: 1270–1276

    Google Scholar 

  • Krömer S, Malmberg G and Gardeström P (1993) Mitochondrial contribution to photosynthetic metabolism. A study with barley (Hordeum vulgare) leaf protoplasts at different light intensities and CO2 concentrations. Plant Physiol 102: 947–955

    PubMed  Google Scholar 

  • Krömer S, Stitt M and Heldt HW (1988) Mitochondrial oxidative phosphorylation participating in photosynthetic metabolism of a leaf cell. FEBS Lett 226: 352–356

    Google Scholar 

  • Lambers H (1985) Respiration in intact plants and tissues: its regulation and dependence on environmental factors, metabolism and invaded organisms. In: Douce R and Day DA (eds) Encyclopaedia of Plant Physiology, New Series, Vol 18. Higher Plant Cell Respiration, pp 418–473. Springer-Verlag, Berlin

    Google Scholar 

  • McIntosh L (1994) Molecular biology of the alternative oxidase. Plant Physiol 105: 781–786

    PubMed  Google Scholar 

  • Padmasree K and Raghavendra AS (1998) Interaction with respiration and nitrogen metabolism. In: Raghavendra AS (ed) Photosynthesis: A Comprehensive Treatise, pp 197–211. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Padmasree K and Raghavendra AS (1999a) Importance of oxidative electron transport over oxidative phosphorylation in optimizing photosynthesis in mesophyll protoplasts of pea (Pisum sativum L.).Physiol Plant 105: 546–553

    Google Scholar 

  • Padmasree K and Raghavendra AS (1999b) Prolongation of photosynthetic induction as a consequence of interference with mitochondrial oxidative metabolism in mesophyll protoplasts of the pea (Pisum sativum L.). Plant Sci 142: 29–36

    Google Scholar 

  • Raghavendra AS, Padmasree K and Saradadevi K (1994) Interdependence of photosynthesis and respiration in plant cells: Interactions between chloroplasts and mitochondria. Plant Sci 97: 1–14

    Google Scholar 

  • Raghavendra AS, Reumann S and Heldt HW (1998) Participation of mitochondrial metabolism in photorespiration. Plant Physiol 116: 1333–1337

    PubMed  Google Scholar 

  • Robinson SA, Ribas-Carbo M, Yakir D, Giles L, Reuveni Y and Berry JA (1995) Beyond SHAM and cyanide: Opportunities for studying the alternative oxidase in plant respiration using oxygen isotope discrimination. Aust J Plant Physiol 22: 487–496

    Google Scholar 

  • Saradadevi K and Raghavendra AS (1992) Dark respiration protects photosynthesis against photoinhibition in mesophyll protoplasts of pea (Pisum sativum). Plant Physiol 99: 1232–1237

    Google Scholar 

  • Saradadevi K and Raghavendra AS (1994) Inhibition of photosynthesis by osmotic stress in pea (Pisum sativum) mesophyll protoplasts is intensified by chilling or photoinhibitory light; intriguing responses of respiration. Plant Cell Environ 17: 739–746

    Google Scholar 

  • Scheibe R (1987) NADPC malate dehydrogenase in C3 plants: Regulation and role of a light-activated enzyme. Physiol Plant 71: 393–400

    Google Scholar 

  • Siedow JN and Umbach AL (1995) Plant mitochondrial electron transfer and molecular biology. The Plant Cell 7: 821–831

    PubMed  Google Scholar 

  • Stitt M, Wirtz W, Gerhardt R, Heldt HW, Spencer C, Walker D and Foyer C(1985) A comparative study of metabolite levels in plant leaf material in the dark. Planta 166: 354–364

    Google Scholar 

  • Vanlerberghe GC, Vanlerberghe AE and McIntosh L (1997) Molecular genetic evidence of the ability of alternative oxidase to support respiratory carbon metabolism. Plant Physiol 113: 657–661

    PubMed  Google Scholar 

  • Winter H, Robinson DG and Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193: 530–535

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Padmasree, K., Raghavendra, A. Response of photosynthetic carbon assimilation in mesophyll protoplasts to restriction on mitochondrial oxidative metabolism: Metabolites related to the redox status and sucrose biosynthesis. Photosynthesis Research 62, 231–239 (1999). https://doi.org/10.1023/A:1006382518725

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006382518725

Navigation