Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-11T09:19:08.835Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  25 February 2005

W. TED ALLISON ,
THEODORE J. HAIMBERGER ,
CRAIG W. HAWRYSHYN  and
SHELBY E. TEMPLE
W. TED ALLISON
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
THEODORE J. HAIMBERGER
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
CRAIG W. HAWRYSHYN
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
SHELBY E. TEMPLE
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

RetinaTeleost fishGiant danioChromophoreThyroxine
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 945 - 952
Copyright
© 2004 Cambridge University Press

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

REFERENCES

Allen, D.M. (1971). Photic control of the proportions of two visual pigments in a fish. Vision Research 11, 1077–1112.Google Scholar
Allen, D.M. & Munz, F.W. (1983). Visual pigment mixtures and scotopic spectral sensitivity in rainbow trout. Environmental Biology of Fishes 8, 185–190.Google Scholar
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), 901–914.Google Scholar
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, 294–306.Google Scholar
Beatty, D.D. (1984). Visual pigments and the labile scotopic visual system of fish. Vision Research 24, 1563–1573.Google Scholar
Bilotta, J. & Saszik, S. (2001). The zebrafish as a model visual system. International Journal of Developmental Neuroscience 19, 621–629.Google Scholar
Bilotta, J., Saszik, S., & Sutherland, S.E. (2001). Rod contributions to the electroretinogram of the dark-adapted developing zebrafish. Developmental Dynamics 222, 564–570.Google Scholar
Blatz, P.E. & Liebman, P.A. (1973). Wavelength regulation in visual pigments. Experimental Eye Research 17, 573–580.Google Scholar
Bridges, C.D.B. (1972). The rhodopsin-porphyropsin visual system. In Handbook of Sensory Physiology, Vol. VII, ed. Dartnall, H.J., pp. 417–480. 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, 79–106.Google Scholar
Cameron, D.A. (2002). Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Visual Neuroscience 19, 365–372.Google Scholar
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, 1540–1550.Google Scholar
Chinen, A., Hamaoka, T., Yamada, Y., & Kawamura, S. (2003). Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics 163, 663–675.Google Scholar
Connaughton, V.P. & Dowling, J.E. (1998). Comparative morphology of distal neurons in larval and adult zebrafish retinas. Vision Research 38, 13–18.Google Scholar
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, 400–412.Google Scholar
Dartnall, H.J. & Lythgoe, J.N. (1965). The spectral clustering of visual pigments. Vision Research 5, 81–100.Google Scholar
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, 11–18.Google Scholar
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G., & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509–528.Google Scholar
Harosi, F.I. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 1359–1367.Google Scholar
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, 2431–2438.Google Scholar
Hisatomi, O., Satoh, T., & Tokunaga, F. (1997). The primary structure and distribution of killifish visual pigments. Vision Research 37, 3089–3096.Google Scholar
Hunt, D.M., Wilkie, S.E., Bowmaker, J.K., & Poopalasundaram, S. (2001). Vision in the ultraviolet. Cellular and Molecular Life Sciences 58, 1583–1598.Google Scholar
Kennedy, D. (1957). A comparative study of spectral sensitivity in tadpoles and adult frogs. Journal of Cellular and Comparative Physiology 50, 155–165.Google Scholar
Koskelainen, A., Ala-Laurila, P., Fyhrquist, N., & Donner, K. (2000). Measurement of thermal contribution to photoreceptor sensitivity. Nature 403, 220–223.Google Scholar
Krauss, A. & Neumeyer, C. (2003). Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vision Research 43, 1273–1282.Google Scholar
Kusmic, C. & Gualtieri, P. (2000). Morphology and spectral sensitivities of retinal and extraretinal photoreceptors in freshwater teleosts. Micron 31, 183–200.Google Scholar
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, 95–131.Google Scholar
Li, L. (2001). Zebrafish mutants: Behavioral genetic studies of visual system defects. Developmental Dynamics 221, 365–372.Google Scholar
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. 57–77. 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, 891–896.Google Scholar
Nawrocki, L., BreMiller, R., Streisinger, G., & Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Research 25, 1569–1576.Google Scholar
Neuhauss, S.C. (2003). Behavioral genetic approaches to visual system development and function in zebrafish. Journal of Neurobiology 54, 148–160.Google Scholar
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, 8603–8615.Google Scholar
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, 411–421.Google Scholar
Parry, J.W. & Bowmaker, J.K. (2000). Visual pigment reconstitution in intact goldfish retina using synthetic retinaldehyde isomers. Vision Research 40, 2241–2247.Google Scholar
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, 1161–1174.Google Scholar
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, 948–950.Google Scholar
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, 6009–6012.Google Scholar
Saszik, S. & Bilotta, J. (1999). The effects of temperature on the dark-adapted spectral sensitivity function of the adult zebrafish. Vision Research 39, 1051–1058.Google Scholar
Schwanzara, S.A. (1967). The visual pigments of freshwater fishes. Vision Research 7, 121–148.Google Scholar
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, 536–557.Google Scholar
Tsin, A.T. & Beatty, D.D. (1978). Goldfish rhodopsin: P499. Vision Research 18, 1453–1455.Google Scholar
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, 15–26.Google Scholar
Tsin, A.T., Liebman, P.A., Beatty, D.D., & Drzymala, R. (1981). Rod and cone visual pigments in the goldfish. Vision Research 21, 943–946.Google Scholar
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, 868–874.Google Scholar
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, 571–585.Google Scholar
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, 103–115.Google Scholar
Yokoyama, S. & Radlwimmer, F.B. (2001). The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158, 1697–1710.Google Scholar