Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T04:45:41.388Z Has data issue: false hasContentIssue false

Visual receptor cycle in normal and period mutant Drosophila: Microspectrophotometry, electrophysiology, and ultrastructural morphometry

Published online by Cambridge University Press:  02 June 2009

De-Mao Chen
Affiliation:
Division of Biological Sciences, The University of Missouri-Columbia, Columbia
J. Scott Christianson
Affiliation:
Division of Biological Sciences, The University of Missouri-Columbia, Columbia
Randall J. Sapp
Affiliation:
Division of Biological Sciences, The University of Missouri-Columbia, Columbia
William S. Stark
Affiliation:
Division of Biological Sciences, The University of Missouri-Columbia, Columbia

Abstract

Visual pigment, sensitivity, and rhabdomere size were measured throughout a 12-h light/12-h dark cycle in Drosophila. Visual pigment and sensitivity were measured during subsequent constant darkness [dark/dark (D/D)]. MSP (microspectrophotometry) and the ERG (electroretinogram) revealed a cycling of visual pigment and sensitivity, respectively. A visual pigment decrease of 40% was noted at 4 h after light onset that recovered 2–4 h later in white-eyed (otherwise wild-type, w per+) flies. The ERG sensitivity [in w per+ flies in light/dark (L/D)] decreased by 75% at 4 h after light onset, more than expected if mediated by visual pigment (MSP) changes alone. ERG sensitivity begins decreasing 8 h before light onset while decreases in visual pigment begin 2 h after light onset. These cycles continue in constant darkness (D/D), suggesting a circadian rhythm. White-eyed period (per) mutants show similar cycles of visual pigment level and sensitivity in L/D; per's alterations, if any on the D/D cycles were subtle. The cross-sectional areas of rhabdomeres in w per+ were measured using electron micrographic (EM) morphometry. Area changed little through the L/D cycle.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arikawa, K., Morikawa, Y., Suzuki, T. & Eguchi, E. (1988). Intrinsic control of rhabdom size and rhodopsin content in the crab compound eye by a circadian biological clock. Experientia 44, 219220.CrossRefGoogle ScholarPubMed
Barlow, R.B.J., Kaplan, E., Renninger, G.H. & Saito, T. (1987). Circadian rhythms in Limulus photoreceptors. Journal of General Physiology 89, 353378.CrossRefGoogle ScholarPubMed
Boschek, C.B. & Hamdorf, K. (1976). Rhodopsin particles in the photoreceptor membrane of an insect. Zeitschrift fur Naturforschung 31C, 763.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361363.CrossRefGoogle ScholarPubMed
Chen, D.-M., Christianson, V.S., Sapp, R.J. & Stark, W.S. (1990). Circadian facets of sensitivity rhodopsin and rhabdomere in Drosophila. Neuroscience Abstracts 16, 1332.Google Scholar
Dowse, H.B. & Ringo, J.M. (1987) Further evidence that the circadian clock in Drosophila is a population of ultradian oscillators. Journal of Biological Rhythms 2, 6576.CrossRefGoogle ScholarPubMed
Hall, J.C. & Rosbash, M. (1987). Genes and biological rhythms. Trends in Genetics 3, 185191.CrossRefGoogle Scholar
Hall, J.C. & Rosbash, M. (1988). Mutations and molecules influencing biological rhythms. Annual Review of Neuroscience 11, 373393.CrossRefGoogle ScholarPubMed
Hamblen, M., Zehring, W.A., Kyriacou, C.P., Reddy, P., Yu, Q., Wheeler, D.A., Zwiebel, L.J., Konopka, R.J., Rosbach, M. & Hall, J.C. (1986). Germ-line transformation involving DNA from the period locus in Drosophila melanogaster: Overlapping genomic fragments that restore circadian and ultradian rhythmicity of per 0 andper - mutants. Journal of Neurogenetics 3, 249291.CrossRefGoogle Scholar
Hardin, P.E., Hall, J.C. & Rosbash, M. (1990). Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature (London) 343, 536540.CrossRefGoogle ScholarPubMed
Harris, W.A., Ready, D.F., Lipson, E.D., Hudspeth, A.J. & Stark, W.S. (1977). Vitamin A deprivation and Drosophila photopigments. Nature (London) 266, 648650.CrossRefGoogle ScholarPubMed
Harris, W.A., Stark, W.S. & Walker, J.A. (1976). Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. Journal of Physiology (London) 256, 415439.Google ScholarPubMed
Isono, K., Hariyama, T., Kito, Y. & Tsukahara, Y. (1986). Exogenous and diurnal rhythms of chromophore turnover of visual pigment in the locust analysed by HPLC. Neuroscience Research Supplement 4, S1–S10.CrossRefGoogle ScholarPubMed
Katz, M.L., Gao, C.L., Kutryb, M., Norberg, N., White, R.H. & Stark, W.S. (1991). Maintenance of opsin density in photoreceptor outer segments of retinoid-deprived rats. Investigative Ophthalmology and Visual Science 32, 19681995.Google ScholarPubMed
Kirschfeld, K. (1986). Activation of visual pigments: Chromophore structure and function. In The Molecular Mechanism of Photoreception, ed. Stieve, H., pp. 149. Berlin: Springer-Verlag.Google Scholar
La Vail, M.M. (1980). Circadian nature of rod outer segment disc shedding in the rat. Investigative Ophthalmology and Visual Science 19, 407410.Google ScholarPubMed
Liu, X., Lorenz, L., Yu, Q. & Hall, J.C. (1988). Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes and Development 2, 228238.CrossRefGoogle ScholarPubMed
Pabst, M.A. & Kral, K. (1989). Effects of green light and darkness on the ultrastructure of ocellar photoreceptors in the wasp Papavespala germanica. Zeitschrift fur Mikroskopishque Anatomine 103, 459475.Google Scholar
Rosbash, M. & Hall, J.C. (1989). The molecular biology of biological rhythms. Neuron 3, 387398.CrossRefGoogle Scholar
Saez, L. & Young, M.W. (1988). In situ localization of the per clock protein during development of Drosophila melanogaster. Molecular and Cellular Biology 8, 53785385.Google ScholarPubMed
Sapp, R.J., Christianson, J.S. & Stark, W.S. (1991). Turnover of membrane and opsin in visual receptors of normal and mutant Drosophila. Journal of Neurocytology 20, 597608.CrossRefGoogle ScholarPubMed
Shaw, S.R. (1981). Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera. In Neurons without Impulses. Society for Experimental Biology Seminar Series 6, ed. Roberts, A. & Bush, B.M.H., pp. 61116. Cambridge University Press.Google Scholar
Siwicki, K.K., Eastman, C., Petersen, G., Rosbash, M. & Hall, J.C. (1988). Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1, 141150.CrossRefGoogle Scholar
Stark, W.S. (1977a). Diet, vitamin A and vision in Drosophila. Drosophila Information Service 52, 47.Google Scholar
Stark, W.S. (1977b). Sensitivity and adaptation in R7, an ultraviolet photoreceptor, in the Drosophila retina. Journal of Comparative Physiology 115, 4759.CrossRefGoogle Scholar
Stark, W.S., Chen, D.M., Christianson, J.S. & Sapp, R.J. (1989a). Entrainment of a circadian rhythm in the rhodopsin cycle of white and white-eyed period mutant Drosophila. Investigative Ophthalmology and Visual Science (Suppl.) 30, 291.Google Scholar
Stark, W.S., Christianson, J.S., Maier, L. & Chen, D.M. (1991). Inherited and environmentally induced retinal degenerations in Drosophila. In Retinal Degenerations, ed. Anderson, R.E., Hollyfield, J.G. & La Vail, M.M., pp. 6175. New York: CRC Press, Inc.Google Scholar
Stark, W.S. & Clark, A.W. (1973). Visual synaptic structure in normal and blind Drosophila. Drosophila Information Service 50, 105106.Google Scholar
Stark, W.S., Ivanyshyn, A.M. & Greenberg, R.M. (1977). Sensitivity and photopigments of R1–6, a two-peaked photoreceptor, in Drosophila, Calliphora and Musca. Journal of Comparative Physiology 121, 289305.CrossRefGoogle Scholar
Stark, W.S. & Johnson, M.A. (1980). Microspectrophotometry of Drosophila visual pigments: Determinations of conversion efficiency in R1–6 receptors. Journal of Comparative Physiology 140, 275286.CrossRefGoogle Scholar
Stark, W.S. & Sapp, R. (1988). Eye color pigment granules in wild-type and mutant Drosophila melanogaster. Canadian Journal of Zoology 66, 13011308.CrossRefGoogle Scholar
Stark, W.S. & Sapp, R.J. (1987). Ultrastructure of the retina of Drosophila melanogaster: the mutant ora (outer rhabdomeres absent) and its inhibition of degeneration in rdgB (retinal degeneration-B), Journal of Neurogenetics 4, 227240.Google ScholarPubMed
Stark, W.S. & Sapp, R.J. (1989). Retinal degeneration and photoreceptor maintenance in Drosophila: rdgB and its interaction with other mutants. In Inherited and Environmentally Induced Retinal Degenerations, ed. La Vail, M.M., Anderson, R.E. & Hollyfield, J.G., pp. 467489. New York: Liss.Google Scholar
Stark, W.S., Sapp, R.J. & Carlson, S.D. (1989b). Photoreceptor maintenance and degeneration in the norpA (no receptor potentialA) mutant of Drosophila melanogaster. Journal of Neurogenetics 5, 4959.CrossRefGoogle ScholarPubMed
Stark, W.S., Sapp, R.J. & Haymer, D.S. (1989c). Eye color pigment granules in Drosophila mauritiana: Mosaics produced by excision of a transposable element. Pigment Cell Research 2, 8692.CrossRefGoogle ScholarPubMed
Stark, W.S., Sapp, R.J. & Schilly, D. (1988). Rhabdomere turnover and rhodopsin cycle: Maintenance of retinula cells in Drosophila melanogaster. Journal of Neurocytology 17, 499509.CrossRefGoogle ScholarPubMed
Stark, W.S., Schilly, D., Christianson, J.S., BONE, R.A. & LANDRUM, J.T. (1990). Photoreceptor-specific efficiencies of β-carotene, zeaxanthin and lutein for photopigment formation deduced from receptor mutant Drosophila melanogaster. Journal of Comparative Physiology 166, 429436.Google ScholarPubMed
Stark, W.S. & Tan, E.W.P. (1982). Ultraviolet light: Photosensitivity and other effects on the visual system. Photochemistry and Photobiology 36, 371380.CrossRefGoogle ScholarPubMed
Stark, W.S., Walker, K.D. & Eidel, J.M. (1985). Ultraviolet and blue light induced damage to the Drosophila retina: Microspectrophotometry and electrophysiology. Current Eye Research 4, 10591075.CrossRefGoogle Scholar
Stavenga, D.G. (1975). Optical qualities of the fly eye—An approach from the side of geometrical, physical and waveguide optics. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 126144. New York: Springer-Verlag Berlin Heidelberg.CrossRefGoogle Scholar
Stowe, S. (1980). Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell and Tissue Research 211, 419440.CrossRefGoogle Scholar
White, R.H. (1964). The effect of light upon the ultrastructure of the mosquito eye. American Zoologist 4, 433.Google Scholar
White, R.H. (1968). The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. III. Multivesicular bodies and protein uptake. Journal of Experimental Zoology 169, 261278.CrossRefGoogle Scholar
Wilcox, M. & Franceschini, N. (1984). Illumination induces dye incorporation into photoreceptor cells. Science 225, 851854.CrossRefGoogle ScholarPubMed
Williams, D.S. (1982). Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell and Tissue Research 226, 629639.CrossRefGoogle Scholar
Young, R.W. (1970). Visual Cells. Scientific American 223 (October), 8091.CrossRefGoogle ScholarPubMed
Young, R.W. (1978). Rhythmic shedding of rod and cone membranes. Investigative Ophthalmology and Visual Science 17, 105116.Google Scholar
Zerr, D.M., Hall, J.C., Rosbash, M. & Siwicki, K.K. (1990). Circadian fluctuations of the period protein immunoreactivity in the CNS and the visual system of Drosophila. Journal of Neuroscience 10, 27492762.CrossRefGoogle ScholarPubMed
Zinkl, G., Maier, L., Studer, K., Sapp, R., Chen, D.M. & Stark, W.S. (1990). Microphotometric, ultrastructural, and electrophysiological analyses of light-dependent processes on visual receptors in white-eyed wild-type and norpA (no receptor potential) mutant Drosophila. Visual Neuroscience 5, 429439.CrossRefGoogle ScholarPubMed