Advertisement

Journal of Comparative Physiology A

, Volume 160, Issue 2, pp 195–203 | Cite as

Spectral sensitivity of light induced respiratory activity of photoreceptor mitochondria in the intact fly

  • J. Tinbergen
  • D. G. Stavenga
Article

Summary

FlyCalliphora erythrocephala (white eyed) photoreceptors were investigated in intact, living animals by microspectrofluorometry in vivo. The fluorescence of mitochondrial flavoproteins (Tinbergen and Stavenga 1986) was used to monitor transient changes in oxidative metabolism, which were induced by a test light following a stimulus of variable intensity.

Two stimulus types were applied, a brief, activating illumination and a prolonged, adapting illumination, respectively. The intensity ranges of activation and adaptation appear to be separated by ca. 3 log units.

Action spectra for inducing a criterion activation or adaptation of the light-dependent mitochondrial system are virtually indistinguishable and closely resemble the spectral sensitivity measured electrophysiologically, thus reinforcing the hypothesis (Hamdorf and Langer 1966; Stavenga and Tinbergen 1983) that the light-induced changes in oxidative metabolism in fly photoreceptors are closely linked to the phototransduction process.

On the basis of the literature we conclude that a light-induced rise in cytosolic calcium concentration is the likely cause for enhancing mitochondrial activity.

Keywords

Oxidative Metabolism Stimulus Type Living Animal Spectral Sensitivity Respiratory Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Autrum H, Tscharntke H (1962) Der Sauerstoffverbrauch der Insektenretina im Licht und im Dunkeln. Z Vergl Physiol 45:695–710Google Scholar
  2. Bernard GD, Stavenga DG (1979) Spectral sensitivities of retinular cells measured in intact living flies by an optical method. J Comp Physiol 134:95–107Google Scholar
  3. Berridge MJ, Irvine RF (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312:315–321Google Scholar
  4. Blumenfeld A, Erusalimsky J, Heichal O, Selinger Z, Minke B (1985) Light-activated guanosinetriphosphate inMusca eye membranes resembles the prolonged depolarizing after potential in photoreceptor cells. Proc Natl Acad Sci USA 82:7116–7120Google Scholar
  5. Bolsover SR, Brown JE (1985) Calcium ion, an intracellular messenger of light adaptation, also participates in excitation ofLimulus photoreceptors. J Physiol 364:381–393Google Scholar
  6. Brown JE, Blinks JR (1974) Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. J Gen Physiol 64:643–665Google Scholar
  7. Brown JE, Rubin LJ (1984) A direct demonstration that inositol-trisphosphate induces an increase in intracellular calcium inLimulus photoreceptors. Biochem Biophys Res Comm 125:1137–1142Google Scholar
  8. Brown JE, Rubin LJ, Ghalayini AJ, Tarver AL, Irvine RF, Berridge MJ, Anderson RE (1984) Myo-Inositol polyphosphate may be a messenger for visual excitation inLimulus photoreceptors. Nature 311:160–162Google Scholar
  9. Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134Google Scholar
  10. Chance B, Schoener B, Oshino R, Itshak F, Nakase Y (1979) Oxidation-reduction ratio studies of mitochondria in freezetrapped samples. J Biol Chem 254:4764–4771Google Scholar
  11. Coles JA, Orkand RK (1982) Sodium activity in drone photoreceptors. J Physiol (Lond) 332:16P-17PGoogle Scholar
  12. Coles JA, Tsacopoulos M, Dunant Y (1984) Régulation de l'extra-consommation d'O2 par les photorécepteurs du faux bourdon à la suite d'un flash de lumière. Klin Mbl Augenheilk 184:332–333Google Scholar
  13. Fain GL, Lisman JE (1981) Membrane conductances of photoreceptors. Progr Biophys Molec Biol 37:91–147Google Scholar
  14. Fein A (1986) Excitation and adaptation ofLimulus photoreceptors by light and inositol 1,4,5-trisphosphate. Trends Neurosci 9:110–114Google Scholar
  15. Fein A, Payne R, Corson DW, Berridge MJ, Irvine RF (1984) Photoreceptor excitation and adaptation by inositol 1,4,5 trisphosphate. Nature 311:157–160Google Scholar
  16. Hamdorf K, Kaschef AH (1964) Der Sauerstoffverbrauch des Facettenauges vonCalliphora erythrocephala in Abhängigkeit von der Temperatur und dem Ionenmilieu. Z Vergl Physiol 48:251–265Google Scholar
  17. Hamdorf K, Langer H (1966) Der Sauerstoffverbrauch des Facettenauges vonCalliphora erythrocephala in Abhängigkeit von der Wellenlänge des Reizlichtes. Z Vergl Physiol 52:386–400Google Scholar
  18. Hamdorf K, Schwemer J (1975) Photoregeneration and the adaptation process in insect photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 363–389Google Scholar
  19. Hardie RC (1979) Electrophysiological analysis of fly retina. I. Comparative properties of R1–6 and R7 and 8. J Comp Physiol 129:19–33Google Scholar
  20. Hardie RC (1985) Functional organization of the fly retina. Progr Sens Physiol 5:1–79Google Scholar
  21. Hillman P, Hochstein S, Minke B (1983) Transduction in invertebrate photoreceptors: Role of pigment bistability. Physiol Rev 63:668–772Google Scholar
  22. Jones GJ, Tsacopoulos M (1987) The response to coloured light flashes of the oxygen consumption of the honeybee drone retina. J Gen Physiol (in press)Google Scholar
  23. Kirschfeld K, Feiler R, Hardie R, Vogt K, Franceschini N (1983) The sensitizing pigment in fly photoreceptors. Properties and candidates. Biophys Struct Mech 10:81–92Google Scholar
  24. Laughlin SB, Hardie RC (1978) Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J Comp Physiol 128:319–340Google Scholar
  25. Levy S, Fein A (1985) Relationship between light sensitivity and intracellular free Ca concentration inLimulus ventral photoreceptors. J Gen Physiol 85:805–841Google Scholar
  26. Lisman JE, Strong JA (1979) The initiation of excitation and light adaptation inLimulus ventral photoreceptors. J Gen Physiol 73:219–243Google Scholar
  27. Minke B, Kirschfeld K (1984) Non-local interactions between light induced processes inCalliphora photoreceptors. J Comp Physiol A 154:175–187Google Scholar
  28. Muijser H (1979) The receptor potential of retinular cells of the blowflyCalliphora: the role of sodium, potassium and calcium ions. J Comp Physiol 132:87–95Google Scholar
  29. Payne R, Corson DW, Fein A (1986a) Pressure injection of calcium both excites and adaptsLimulus ventral photoreceptors. J Gen Physiol 88:107–126Google Scholar
  30. Payne R, Corson DW, Fein A, Berridge MJ (1986b) Excitation and adaptation ofLimulus ventral photoreceptors by inositol (1,4,5) trisphosphate result from a rise in intracellular calcium. J Gen Physiol 88:127–142Google Scholar
  31. Rodieck RW (1973) The vertebrate retina. Principles of structure and function. Freeman, San FranciscoGoogle Scholar
  32. Sacktor B (1975) Biochemistry of insect flight. In: Candy DJ, Kilby BA (eds) Insect biochemistry and function. Chapman and Hall, London, pp 1–88Google Scholar
  33. Schwemer J (1979) Molekulare Grundlagen der Photorezeption bei der SchmeißfliegeCalliphora erythrocephala Meig. Habilitationsschrift, BochumGoogle Scholar
  34. Schwemer J (1984) Renewal of visual pigment in photoreceptors of the blowfly. J Comp Physiol A 154:535–547Google Scholar
  35. Smakman JGJ, Stavenga DG (1986) Spectral sensitivity of blowfly photoreceptors: dependence on waveguide effects and pigment concentration. Vision Res 7:1019–1025Google Scholar
  36. Somlyo AP, Bond M, Somlyo AV (1985) Calcium content of mitochondria and endoplasmic reticulum in liver frozen rapidly in vivo. Nature 314:622–625Google Scholar
  37. Stavenga DG, Tinbergen J (1983) Light dependence of oxidative metabolism in fly compound eyes studied in vivo by microspectrofluorometry. Naturwissenschaften 70:618–620Google Scholar
  38. Streck P (1972) Der Einfluß des Schirmpigmentes auf das Sehfeld einzelner Sehzellen der FliegeCalliphora erythrocephala Meig. Z Vergl Physiol 76:372–402Google Scholar
  39. Strong JA, Lisman J (1978) Initiation of light adaptation in barnacle photoreceptors. Science 200:1485–1487Google Scholar
  40. Tinbergen J, Stavenga DG (1986) Photoreceptor redox state monitored in vivo by transmission and fluorescence microspectrophotometry in blowfly compound eyes. Vision Res 26:239–243Google Scholar
  41. Trujillo-Cenóz O (1972) The structural organization of the compound eye in insects. In: Fuortes MGF (ed), Handbook of sensory physiology, vol VII/2. Springer, Berlin Heidelberg New York, pp 5–61Google Scholar
  42. Tsacopoulos M, Poitry S (1982) Kinetics of oxygen consumption after a single flash of light in photoreceptors of the drone (Apis mellifera). J Gen Physiol 80:19–55Google Scholar
  43. Tsacopoulos M, Orkand RK, Coles JA, Levy S, Poitry S (1983) Oxygen uptake occurs faster than sodium pumping in bee retina after a light flash. Nature 301:604–606Google Scholar
  44. Tsacopoulos M, Fein A, Poitry S (1986) Stimulus-induced increase of mitochondrial respiration in a single neuron. Experientia 42:642Google Scholar
  45. Vogt K (1983) Is the fly visual pigment a rhodopsin? Z Naturforsch 38C:329–333Google Scholar
  46. Walz B (1983) Calcium-sequestering smooth endoplasmic reticulum in retinula cells of the blowfly. J Ultrastruct Res 81:240–248Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • J. Tinbergen
    • 1
  • D. G. Stavenga
    • 1
  1. 1.Department of Biophysics, Laboratorium voor Algemene NatuurkundeRijksuniversiteit GroningenCM GroningenThe Netherlands

Personalised recommendations