Log in

Morphological and functional characteristics of arpa (receptor potential absent) visual mutant of the blowfly (Calliphora erythrocephala)

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    We have discovered a previously unreported visual mutant of the blowfly,Calliphora erythrocephala. It shows a reduced or absent visual performance, e.g., in escape and optomotor behavior. The effects of this mutation on the ultrastructure were studied by electron microscopy (Figs. 3–8) and on electrophysiological function, by intracellular recordings (Figs. 1 and 2).

  2. 2.

    The genetic basis of this spontaneous mutation was studied by test crosses of mutant and wild-type flies. The defect appears to be in an autosomal recessive gene (Table 1).

  3. 3.

    Of the mutant stock studied soon after eclosion (n = 18) 35% shows optomotor reactions, whereas only 6% studied in later life (n = 240) shows any optomotor behavior.

  4. 4.

    The absence of the receptor potentials in photoreceptor cells is not directly associated with structural disorders in the early life of these mutant flies, but several types of degenerative changes are manifested in the retinular cells later on. The optomotorically blind specimens have normal (about −60 mV) resting membrane voltages but no detectable receptor cell voltage response to light, indicating a block in phototransduction. The spectral and polarization sensitivities of optomotor-positive flies are normal (Fig. 2).

  5. 5.

    At the beginning of degeneration the number of lysosomes in the receptor cells is increased compared with normal flies, but their number as well as that of other components of the cell interior decrease later on. During the progression of the degeneration, the rhabdomeres shrink while the mitochondria swell and disintegrate (Figs. 6–8).

  6. 6.

    The blocking of phototransduction is proposed to lead to disturbance of the turnover of the rhabdomeres and finally to degeneration of the receptor cells.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /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

norpA :

no receptor potential A

ora :

outer rabdomere absent

rdgA :

retinal degeneration A

rdgB :

retinal degeneration B

rER:

rough endoplasmic reticulum

sER:

smooth endoplasmic reticulum

rpa :

receptor potential absent

References

  • Alawi AA, Jennings V, Grossfield J, Pak WL (1972) Phototransductionmutants ofDrosophila melanogaster. In: Arden GB (ed) The visual system: Neurophysiology, biophysics and their clinical applications. Plenum, New York, pp 1–21

    Google Scholar 

  • Benzer S (1973) Genetic dissection of behavior. Sci Am 229:2–15

    Google Scholar 

  • Blondeau J, Heisenberg M (1982) The three-dimensional optomotor torque system ofDrosophila melanogaster. J Comp Physiol 145:321–329

    Google Scholar 

  • Burkhardt D (1962) Spectral sensitivity and other response characteristics of single visual cells in the arthropod eye. Symp Soc Exp Biol 16:86–109

    Google Scholar 

  • Carlson SD, Stark WS, Chi C (1984) Rapid light induced degeneration of photoreceptor terminals inrdgB mutantDrosophila. Invest Ophthalmol Visual Sci Suppl “ARVO 84”

  • Hardie RC (1985) Functional organization of the fly retina. In: Ottoson D (ed) Progress in sensory physiology 5. Springer, Berlin Heidelberg New York, pp 1–79

    Google Scholar 

  • Harris WA, Stark WS (1977) Hereditary retinal degeneration inDrosophila melanogaster. A mutant defect associated with the phototransduction process. J Gen Physiol 69:261–291

    Google Scholar 

  • Harris WA, Stark WS, Walker JA (1976) Genetic dissection of the photoreceptor system in the compound eye ofDrosophila melanogaster. J Physiol 256:415–439

    Google Scholar 

  • Heisenberg M (1979) Genetic approach to a visual system. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology vol. VII/6A). Springer, Berlin Heidelberg New York, pp 665–679

    Google Scholar 

  • Hirosawa K, Hotta Y (1982) Morphological analysis of photoreceptor membranes in mutantDrosophila eyes. In: Hollyfield JG (ed) The structure of eye. Elsevier/North Holland, pp 45–53

    Google Scholar 

  • Hotta Y, Benzer S (1970) Genetic dissection of theDrosophila nervous system by means of mosaics. Proc Natl Acad Sci USA 67:1156–1163

    Google Scholar 

  • Inoue H, Yoshioka T, Hotta Y (1985) A genetic study of inositol triphosphate involvement in phototransduction usingDrosophila mutants. Biochem Biophys Res Commun 132:513–519

    Google Scholar 

  • Inoue H, Yoshioka T, Hotta Y (1988) Membrane associated phospholipase-C ofDrosophila retina. J Biochem 103:91–94

    Google Scholar 

  • Järvilehto M (1985) The eye: Vision and perception. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon, Oxford New York Toronto, pp 355–429

    Google Scholar 

  • Järvilehto M, Moring J (1976) Spectral and polarization sensitivity of identified retinal cells of the fly. In: Zeltler F, Weiler R (eds) Neural principles in vision. Springer, Berlin Heidelberg, pp 214–226

    Google Scholar 

  • Järvilehto M, Zettler F (1971) Localized intracellular potentials from pre- and postsynaptic components in the external plexiform layer of an insect retina. Z Vergl Physiol 75:422–440

    Google Scholar 

  • Järvilehto M, Zettler F (1973) Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina. Z Zellforsch 136:291–306

    Google Scholar 

  • Järvilehto M, Weckström M, Kouvalainen E, Harjula R (1986) Ultrastructural and functional pathology of the compound eye of the retinal degeneration mutant. Proc Scand Electron Microsc: 17

  • Johnson MA, Frayer KL, Stark WS (1982) Characteristics ofrdgA: Mutants with retinal degeneration inDrosophila. J Insect Physiol 28:233–242

    Google Scholar 

  • Laughlin SB (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 133–280

    Google Scholar 

  • Lo M-VL, Pak WL (1981) Light-induced pigment granule migration in the retinular cells ofDrosophila melanogaster: Comparison of wild type with ERG defective mutants. J Gen Physiol 77:155–175

    Google Scholar 

  • Meyertholen EP, Stein PJ, Williams MA, Ostroy SE (1987) Studies of theDrosophila norpA phototransduction mutant. II. Photoreceptor degeneration and rhodopsin maintenance. J Comp Physiol A 161:793–798

    Google Scholar 

  • Pak WL (1975) Mutations affecting the vision ofDrosophila melanogaster. In: King RC (ed) Handbook of genetics, vol 3. Plenum, New York, pp 703–733

    Google Scholar 

  • Payne R (1986) Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol triphosphate. Photobiochem Photobiophys 13:373–397

    Google Scholar 

  • Schwemer J (1985) Turnover of photoreceptor membrane and visual pigment in invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 303–326

    Google Scholar 

  • Stark WS, Carlson SD (1984) Blue and ultraviolet light induced damage to theDrosophila melanogaster Meigen (Diptera: Drosophilidae). J Insect Morphol Embryol 14:243–254

    Google Scholar 

  • Stark WS, Sapp R (1987a) Development and senescence of thenorpA (no receptor potential) mutant ofDrosophila. Invest Ophthalmol Visual Sci Suppl “ARVO 87”

  • Stark WS, Sapp R (1987b) Ultrastructure of the retina ofDrosophila melanogaster: The mutantora (outer rhabdomere absent) and its inhibition of degeneration inrdgB (retinal degeneration B). J Neurogenetics 4:227–240

    Google Scholar 

  • Stark WS, Sapp R, Hartman CR (1986) Retinal degeneration and membrane cycling inrdgB mutantDrosophila: Interaction with mutants which block the receptor potential and the lysosomal enzyme acid phosphatase. Int Congr of Eye Research in Nagoya

  • Strausfeld NJ (1971) The organization of the insect visual system (Light microscopy), I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z Zellforsch 121:377–441

    Google Scholar 

  • Torkkeli P, Weckström M, Kouvalainen E, Järvilehto M (1987) Retinal degeneration mutation in blowfly: functional and ultrastructural analysis. Neurosci 22 [Suppl]: 1240

    Google Scholar 

  • Williams DS (1982) Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell Tissue Res 226:629–639

    Google Scholar 

  • Wilson MJ, Ostroy SE (1987) Studies of theDrosophila norpA phototransduction mutant. I. Electrophysiological changes and the offsetting effect of light. J Comp Physiol A 161:785–791

    Google Scholar 

  • Yoshioka T, Inoue H, Hotta Y (1983) Defective phospholipid metabolism in the retinular cell membrane ofnorpA. (no receptor potential) visual transduction mutants ofDrosophila. Biochem Biophys Res Commun 111:567–573

    Google Scholar 

  • Yoshioka T, Inoue H, Hotta Y (1984) Absence of diglyceride kinase activity in the photoreceptor cells ofDrosophila mutants. Biochem Biophys Res Commun 119:389–395

    Google Scholar 

  • Yoshioka T, Inoue H, Hotta Y (1985) Absence of phosphatidylinositol phosphodiesterase in the head of aDrosophila visual mutant,norpA (no receptor potential A). J Biochem 97:1251–1254

    Google Scholar 

  • Young RW (1977) Visual cell renewal systems and the problem of retinitis pigmentosa. In: Landers MB, Wolbarsht MY, Dowling JE, Laties AM (eds) Pigmentosa: clinical implications of current research. Plenum, New York, pp 93–113

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Torkkeli, P., Weckström, M., Kouvalainen, E. et al. Morphological and functional characteristics of arpa (receptor potential absent) visual mutant of the blowfly (Calliphora erythrocephala). J. Comp. Physiol. 165, 333–341 (1989). https://doi.org/10.1007/BF00619352

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00619352

Keywords

Navigation