Skip to main content
×
Home
    • Aa
    • Aa

Visual pigment composition in zebrafish: Evidence for a rhodopsin–porphyropsin interchange system

  • W. TED ALLISON (a1), THEODORE J. HAIMBERGER (a1), CRAIG W. HAWRYSHYN (a1) and SHELBY E. TEMPLE (a1)
Abstract

Numerous reports have concluded that zebrafish (Danio rerio) possesses A1-based visual pigments in their rod and cone photoreceptors. In the present study, we investigated the possibility that zebrafish have a paired visual pigment system. We measured the spectral absorption characteristics of photoreceptors from zebrafish maintained in different temperature regimes and those treated with exogenous thyroid hormone using CCD-based microspectrophotometry. Rods from fish housed at 15°C and 28°C were not significantly different, having λmax values of 503 ± 5 nm (n = 106) and 504 ± 6 nm (n = 88), respectively. Thyroid hormone treatment (held at 28°C), however, significantly shifted the λmax of rods from 503 ± 5 nm (n = 194) to 527 ± 8 nm (n = 212). Cone photoreceptors in fish housed at 28°C (without thyroid hormone treatment) had λmax values of 361 ± 3 nm (n = 2) for ultraviolet-, 411 ± 5 nm (n = 18) for short-, 482 ± 6 nm (n = 9) for medium-, and 565 ± 10 nm (n = 14) for long-wavelength sensitive cones. Thyroid hormone treatment of fish held at 28°C significantly shifted the λmax of long-wavelength sensitive cones to 613 ± 11 nm (n = 20), substantially beyond that of the λmax of the longest possible A1-based visual pigment (∼580 nm). Thyroid hormone treatment produced smaller shifts of λmax in other cone types and increased the half-band width. All shifts in photoreceptor λmax values resulting from thyroid hormone treatment matched predictions for an A1- to A2-based visual pigment system. We therefore conclude that zebrafish possess a rhodopsin–porphyropsin interchange system that functions to spectrally tune rod and cone photoreceptors. We believe that these observations should be carefully considered during analysis of zebrafish spectral sensitivity.

Copyright
Corresponding author
Address correspondence and reprint requests to: Craig W. Hawryshyn, Department of Biology, University of Victoria, P.O. Box 3020 Stn. CSC, Victoria, British Columbia, Canada, V8W 3N5. E-mail chawrysh@uvic.ca
References
Hide All

REFERENCES

Allen, D.M. (1971). Photic control of the proportions of two visual pigments in a fish. Vision Research 11, 10771112.
Allen, D.M. & Munz, F.W. (1983). Visual pigment mixtures and scotopic spectral sensitivity in rainbow trout. Environmental Biology of Fishes 8, 185190.
Allen, D.M., McFarland, W.N., Munz, F.W., & Poston, H.A. (1973). Changes in visual pigments of trout. Canadian Journal of Zoology 51 (9), 901914.
Allison, W.T., Dann, S.G., Helvik, J.V., Bradley, C., Moyer, H.D., & Hawryshyn, C.W. (2003). Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). Journal of Comparative Neurology 461, 294306.
Beatty, D.D. (1984). Visual pigments and the labile scotopic visual system of fish. Vision Research 24, 15631573.
Bilotta, J. & Saszik, S. (2001). The zebrafish as a model visual system. International Journal of Developmental Neuroscience 19, 621629.
Bilotta, J., Saszik, S., & Sutherland, S.E. (2001). Rod contributions to the electroretinogram of the dark-adapted developing zebrafish. Developmental Dynamics 222, 564570.
Blatz, P.E. & Liebman, P.A. (1973). Wavelength regulation in visual pigments. Experimental Eye Research 17, 573580.
Bridges, C.D.B. (1972). The rhodopsin-porphyropsin visual system. In Handbook of Sensory Physiology, Vol. VII, ed. Dartnall, H.J., pp. 417480. Berlin: Springer-Verlag.
Brown, P.K., Gibbons, I.R., & Wald, G. (1963). The visual cells and visual pigment of the mudpuppy, Nectarus. Journal of Cell Biology 19, 79106.
Cameron, D.A. (2002). Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Visual Neuroscience 19, 365372.
Carleton, K.L. & Kocher, T.D. (2001). Cone opsin genes of African cichlid fishes: Tuning spectral sensitivity by differential gene expression. Molecular Biology and Evolution 18, 15401550.
Chinen, A., Hamaoka, T., Yamada, Y., & Kawamura, S. (2003). Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163, 663675.
Connaughton, V.P. & Dowling, J.E. (1998). Comparative morphology of distal neurons in larval and adult zebrafish retinas. Vision Research 38, 1318.
Dann, S.G., Allison, W.T., Levin, D.B., Taylor, J.S., & Hawryshyn, C.W. (2004). Salmonid opsin sequences undergo positive selection and indicate an alternate evolutionary relationship in Oncorhynchus. Journal of Molecular Evolution 58, 400412.
Dartnall, H.J. & Lythgoe, J.N. (1965). The spectral clustering of visual pigments. Vision Research 5, 81100.
Goldsmith, P. & Harris, W.A. (2003). The zebrafish as a tool for understanding the biology of visual disorders. Seminars in Cell and Developmental Biology 14, 1118.
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G., & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509528.
Harosi, F.I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 13591367.
Hawryshyn, C.W., Haimberger, T.J., & Deutschlander, M.E. (2001). Microspectrophotometric measurements of vertebrate photoreceptors using CCD-based detection technology. Journal of Experimental Biology 204, 24312438.
Hisatomi, O., Satoh, T., & Tokunaga, F. (1997). The primary structure and distribution of killifish visual pigments. Vision Research 37, 30893096.
Hunt, D.M., Wilkie, S.E., Bowmaker, J.K., & Poopalasundaram, S. (2001). Vision in the ultraviolet. Cellular and Molecular Life Sciences 58, 15831598.
Kennedy, D. (1957). A comparative study of spectral sensitivity in tadpoles and adult frogs. Journal of Cellular and Comparative Physiology 50, 155165.
Koskelainen, A., Ala-Laurila, P., Fyhrquist, N., & Donner, K. (2000). Measurement of thermal contribution to photoreceptor sensitivity. Nature 403, 220223.
Krauss, A. & Neumeyer, C. (2003). Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vision Research 43, 12731282.
Kusmic, C. & Gualtieri, P. (2000). Morphology and spectral sensitivities of retinal and extraretinal photoreceptors in freshwater teleosts. Micron 31, 183200.
Levine, J.S. & MacNichol, E.F., Jr. (1979). Visual pigments in teleost fishes: Effects of habitat, microhabitat, and behavior on visual system evolution. Sensory Processes 3, 95131.
Li, L. (2001). Zebrafish mutants: Behavioral genetic studies of visual system defects. Developmental Dynamics 221, 365372.
Loew, E.R. (1995). Determinants of visual pigment spectral location and photoreceptor cell spectral sensitivity. In Neurobiology and Clinical Aspects of the Outer Retina, ed. Djamgoz, M.B.A., pp. 5777. London: Chapman & Hall.
Loew, E.R. & Dartnall, H.J. (1976). Vitamin A1/A2-based visual pigment mixtures in cones of the rudd. Vision Research 16, 891896.
Nawrocki, L., BreMiller, R., Streisinger, G., & Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Research 25, 15691576.
Neuhauss, S.C. (2003). Behavioral genetic approaches to visual system development and function in zebrafish. Journal of Neurobiology 54, 148160.
Neuhauss, S.C., Biehlmaier, O., Seeliger, M.W., Das, T., Kohler, K., Harris, W.A., & Baier, H. (1999). Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. Journal of Neuroscience 19, 86038615.
Palacios, A.G., Goldsmith, T.H., & Bernard, G.D. (1996). Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Visual Neuroscience 13, 411421.
Parry, J.W. & Bowmaker, J.K. (2000). Visual pigment reconstitution in intact goldfish retina using synthetic retinaldehyde isomers. Vision Research 40, 22412247.
Raymond, P.A., Barthel, L.K., Rounsifer, M.E., Sullivan, S.A., & Knight, J.K. (1993). Expression of rod and cone visual pigments in goldfish and zebrafish: A rhodopsin-like gene is expressed in cones. Neuron 10, 11611174.
Raymond, P.A., Barthel, L.K., & Stenkamp, D.L. (1996). The zebrafish ultraviolet cone opsin reported previously is expressed in rods. Investigative Ophthalmology and Visual Science 37, 948950.
Robinson, J., Schmitt, E.A., Harosi, F.I., Reece, R.J., & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the U.S.A. 90, 60096012.
Saszik, S. & Bilotta, J. (1999). The effects of temperature on the dark-adapted spectral sensitivity function of the adult zebrafish. Vision Research 39, 10511058.
Schwanzara, S.A. (1967). The visual pigments of freshwater fishes. Vision Research 7, 121148.
Taylor, M.R., Van Epps, H.A., Kennedy, M.J., Saari, J.C., Hurley, J.B., & Brockerhoff, S.E. (2000). Biochemical analysis of phototransduction and visual cycle in zebrafish larvae. Methods in Enzymology 316, 536557.
Tsin, A.T. & Beatty, D.D. (1978). Goldfish rhodopsin: P499. Vision Research 18, 14531455.
Tsin, A.T. & Beatty, D.D. (1979). Scotopic visual pigment composition in the retinas and vitamins A in the pigment epithelium of the goldfish. Experimental Eye Research 29, 1526.
Tsin, A.T., Liebman, P.A., Beatty, D.D., & Drzymala, R. (1981). Rod and cone visual pigments in the goldfish. Vision Research 21, 943946.
Van Epps, H.A., Yim, C.M., Hurley, J.B., & Brockerhoff, S.E. (2001). Investigations of photoreceptor synaptic transmission and light adaptation in the zebrafish visual mutant nrc. Investigative Ophthalmology and Visual Science 42, 868874.
Vihtelic, T.S., Doro, C.J., & Hyde, D.R. (1999). Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Visual Neuroscience 16, 571585.
Whitmore, A.V. & Bowmaker, J.K. (1989). Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd Scardinius erythrophthalmus. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 166, 103115.
Yokoyama, S. & Radlwimmer, F.B. (2001). The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158, 16971710.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 5
Total number of PDF views: 33 *
Loading metrics...

Abstract views

Total abstract views: 216 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd October 2017. This data will be updated every 24 hours.