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. 1981 Feb 1;77(2):155–175. doi: 10.1085/jgp.77.2.155

Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. Comparison of wild type with ERG-defective mutants

PMCID: PMC2215424  PMID: 6790662

Abstract

The dependence of pigment granule migration (PGM) upon the receptor potential was examined using several strains of electroretinogram (ERG)- defective mutants of Drosophila melanogaster. The mutants that have a defective lamina component but a normal receptor component of the ERG (no on-transient A [nonA] and tan) exhibited normal pigment granule migration. The mutants that have very small or no receptor potentials (certain no receptor potential A [norpA] alleles), on the other hand, exhibited no PGM. In the case of the temperature-sensitive norpA mutant, norpAH52, normal PGM was present at 17 degrees but not at 32 degrees C or above, corresponding to its electrophysiological phenotype. In the transient receptor potential (trp) mutant, whose receptor potential decays to the baseline within a few seconds during a sustained light stimulus, the pigment granules initially moved close to the rhabdomere when light was turned on but moved away after about 5 s during a sustained light stimulus. All these results lend strong support to the notion that PGM is initiated by a light-evoked depolarization of the receptor membrane, i.e., the receptor potential. However, under certain experimental conditions, the receptor potentials failed to induce PGM in the trp mutant. The depolarization of the receptor, thus, appears to be closely associated with PGM but is not a sufficient condition for PGM.

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Selected References

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  1. Alawi A. A., Jennings V., Grossfield J., Pak W. L. Phototransduction mutants of Drosophila melanogaster. Adv Exp Med Biol. 1972;24(0):1–21. doi: 10.1007/978-1-4684-8231-7_1. [DOI] [PubMed] [Google Scholar]
  2. Alawi A. A., Pak W. L. On-transient of insect electroretinogram: its cellular origin. Science. 1971 Jun 4;172(3987):1055–1057. doi: 10.1126/science.172.3987.1055. [DOI] [PubMed] [Google Scholar]
  3. Baumann F., Mauro A. Effect of hypoxia on the change in membrane conductance evoked by illumination in arthropod photoreceptors. Nat New Biol. 1973 Aug 1;244(135):146–148. doi: 10.1038/newbio244146b0. [DOI] [PubMed] [Google Scholar]
  4. Boschek C. B. On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zellforsch Mikrosk Anat. 1971;118(3):369–409. doi: 10.1007/BF00331193. [DOI] [PubMed] [Google Scholar]
  5. Brown H. M., Cornwall M. C. Spectral correlates of a quasi-stable depolarization in barnacle photoreceptor following red light. J Physiol. 1975 Jul;248(3):555–578. doi: 10.1113/jphysiol.1975.sp010988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown J. E., Blinks J. R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol. 1974 Dec;64(6):643–665. doi: 10.1085/jgp.64.6.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. E., Brown P. K., Pinto L. H. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol. 1977 May;267(2):299–320. doi: 10.1113/jphysiol.1977.sp011814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Byers H. R., Porter K. R. Transformations in the structure of the cytoplasmic ground substance in erythrophores during pigment aggregation and dispersion. I. A study using whole-cell preparations in stereo high voltage electron microscopy. J Cell Biol. 1977 Nov;75(2 Pt 1):541–558. doi: 10.1083/jcb.75.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cosens D. J., Manning A. Abnormal electroretinogram from a Drosophila mutant. Nature. 1969 Oct 18;224(5216):285–287. doi: 10.1038/224285a0. [DOI] [PubMed] [Google Scholar]
  10. Cosens D., Perry M. M. The fine structure of the eye of a visual mutant, A-type of Drosophila melanogaster. J Insect Physiol. 1972 Sep;18(9):1773–1786. doi: 10.1016/0022-1910(72)90109-6. [DOI] [PubMed] [Google Scholar]
  11. Cosens D., Wright R. Light elicited isolation of the complementary visual input systems in white-eye Drosophila. J Insect Physiol. 1975 May;21(5):1111–1120. doi: 10.1016/0022-1910(75)90124-9. [DOI] [PubMed] [Google Scholar]
  12. Deland M. C., Pak W. L. Reversibly temperature sensitive phototransduction mutant of Drosophila melanogaster. Nat New Biol. 1973 Aug 8;244(136):184–186. doi: 10.1038/newbio244184a0. [DOI] [PubMed] [Google Scholar]
  13. Franceschini N., Kirschfeld K. Les phénoménes de pseudopupille dans l'oeil compose de Drosophila. Kybernetik. 1971 Nov;9(5):159–182. doi: 10.1007/BF02215177. [DOI] [PubMed] [Google Scholar]
  14. Hotta Y., Benzer S. Abnormal electroretinograms in visual mutants of Drosophila. Nature. 1969 Apr 26;222(5191):354–356. doi: 10.1038/222354a0. [DOI] [PubMed] [Google Scholar]
  15. Hotta Y., Benzer S. Genetic dissection of the Drosophila nervous system by means of mosaics. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1156–1163. doi: 10.1073/pnas.67.3.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KINOSITA H. Electrophoretic theory of pigment migration within fish melanophore. Ann N Y Acad Sci. 1963 Feb 15;100:992–1004. [PubMed] [Google Scholar]
  17. Kirschfeld K., Franceschini N. Ein Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik. 1969 May;6(1):13–22. doi: 10.1007/BF00288624. [DOI] [PubMed] [Google Scholar]
  18. Lo M. V., Wong F., Pak W. L. Increase in intracellular free calcium concentration of Limulus photoreceptors caused by a metabolic inhibitor. Vision Res. 1980;20(6):539–544. doi: 10.1016/0042-6989(80)90129-7. [DOI] [PubMed] [Google Scholar]
  19. Menzel R., Lange G. Anderungen der Feinstruktur im Komplexauge von Formica polyctena bei der Helladaptation. Z Naturforsch B. 1971 Apr;26(4):357–359. [PubMed] [Google Scholar]
  20. Miller W. H., Cawthon D. F. Pigment granule movement in Limulus photoreceptors. Invest Ophthalmol. 1974 May;13(5):401–405. [PubMed] [Google Scholar]
  21. Minke B., Wu C., Pak W. L. Induction of photoreceptor voltage noise in the dark in Drosophila mutant. Nature. 1975 Nov 6;258(5530):84–87. doi: 10.1038/258084a0. [DOI] [PubMed] [Google Scholar]
  22. Muijser H., Leutscher-Hazelhoff J. T., Stavenga D. G., Kuiper J. W. Photopigment conversions expressed in receptor potential and membrane resistance of blowfly visual sense cells. Nature. 1975 Apr 10;254(5500):520–522. doi: 10.1038/254520a0. [DOI] [PubMed] [Google Scholar]
  23. Nolte J., Brown J. E. Ultraviolet-induced sensitivity to visible light in ultraviolet receptors of Limulus. J Gen Physiol. 1972 Feb;59(2):186–200. doi: 10.1085/jgp.59.2.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Paj W. K., Istrit S. E., Deland M. C., Wu C. F. Photoreceptor mutant of Drosophia: is protein involved in intermediate steps of phototransduction? Science. 1976 Nov 26;194(4268):956–959. doi: 10.1126/science.824732. [DOI] [PubMed] [Google Scholar]
  25. Pak W. L., Grossfield J., Arnold K. S. Mutants of the visual pathway of Drosophila melanogaster. Nature. 1970 Aug 1;227(5257):518–520. doi: 10.1038/227518b0. [DOI] [PubMed] [Google Scholar]
  26. Pak W. L., Grossfield J., White N. V. Nonphototactic mutants in a study of vision of Drosophila. Nature. 1969 Apr 26;222(5191):351–354. doi: 10.1038/222351a0. [DOI] [PubMed] [Google Scholar]
  27. Stavenga D. G., Flokstra J. H., Kuiper J. W. Photopigment conversions expressed in pupil mechanism of blowfly visual sense cells. Nature. 1975 Feb 27;253(5494):740–742. doi: 10.1038/253740a0. [DOI] [PubMed] [Google Scholar]
  28. Wong F., Wu C. F., Mauro A., Pak W. L. Persistence of prolonged light-induced conductance change in arthropod photoreceptors on recovery from anoxia. Nature. 1976 Dec 16;264(5587):661–664. doi: 10.1038/264661a0. [DOI] [PubMed] [Google Scholar]
  29. YASUZUMI G., DEGUCHI N. Submicroscopic structure of the compound eye as revealed by electron microscopy. J Ultrastruct Res. 1958 Apr;1(3):259–270. doi: 10.1016/s0022-5320(58)80007-6. [DOI] [PubMed] [Google Scholar]

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