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Diurnal rhythm of cone opsin expression in the teleost fish Haplochromis burtoni

Published online by Cambridge University Press:  02 June 2005

SVEN HALSTENBERG ,
KRISTIN M. LINDGREN ,
SANJUM P. S. SAMAGH ,
MIREYA NADAL-VICENS ,
STEVE BALT,  and
RUSSELL D. FERNALD
SVEN HALSTENBERG
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford Present address: Institute of Pathology, Johannes Gutenberg University, Langenbeckstrasse 1, D-55101 Mainz, Germany
KRISTIN M. LINDGREN
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford
SANJUM P. S. SAMAGH
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford
MIREYA NADAL-VICENS
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford Present address: Program of Neurosciences, Harvard University, Harvard Medical School, Boston, MA 02115, USA
STEVE BALT,
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford Present address: Department of Psychiatry, Stanford University, Stanford, CA 94305, USA
RUSSELL D. FERNALD
Affiliation:
Department of Biological Sciences and Neuroscience Program, Stanford University, Stanford
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Abstract

The biochemical and morphological specializations of rod and cone photoreceptors reflect their roles in sight. The apoprotein opsin, which converts photons into chemical signals, functions at one end of these highly polarized cells, in the outer segment. Previous work has shown that the mRNA of rod opsin, the opsin specific to rods, is renewed in the outer segment with a diurnal rhythm in the retina of the teleost fish Haplochromis burtoni. Here we show that in the same species, all three cone opsin mRNAs (blue, green, and red) also have a diurnal rhythm of expression. Quantitative real-time polymerase chain reaction (PCR) with primer pairs specific for the cone photoreceptor opsin subtypes was used to detect opsin mRNA abundance in animals sacrificed at 3-h intervals around the clock. All three cone opsins were expressed with diurnal rhythms similar to each other but out of phase with the rod opsin rhythm. Specifically, cone opsin expression occurs at a higher level near the onset of the dark period, when cones are not used for vision. Finally, we found that the rhythm of cone opsin expression in fish appears to be light dependent, as prolonged darkness changes normal diurnal expression patterns.

Keywords

Cone photoreceptorOpsinDiurnal rhythmTemporal regulationHaplochromis (Astatotilapia) burtoni
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 2 , March 2005 , pp. 135 - 141
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Besharse, J.C., Hollyfield, J.G., & Rayborn, M.E. (1977). Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light. Journal of Cell Biology 75, 507–527.Google Scholar
Burnside, B. (1976). Microtubules and actin filaments in teleost visual cone elongation and contraction. Journal of Supramolecular Structure 5, 257–275.CrossRefGoogle Scholar
Cahill, G.M. & Besharse, J.C. (1993). Circadian clock functions localized in xenopus retinal photoreceptors. Neuron 10, 573–577.CrossRefGoogle 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.CrossRefGoogle Scholar
Chiu, J.F., Mack, A.F., & Fernald, R.D. (1995). Daily rhythm of cell proliferation in the teleost retina. Brain Research 673, 119–125.CrossRefGoogle Scholar
Fernald, R.D. (1977). Quantitative behavioral observations of Haplochromis burtoni under semi-natural conditions. Animal Behavior 25, 643–653.CrossRefGoogle Scholar
Fernald, R.D. (1990). Haplochromis burtoni: A case study. In The Visual System of Fish, ed. Douglas, R.H. & Djamgoz, M.B., pp. 443–464. New York: Croon Helm Ltd.CrossRef
Fernald, R.D. (1991). Principles of sensory regeneration. In Regeneration of Vertebrate Sensory Receptor Cells, Vol. 160, ed. Bock, G.R., Marsh, J. & Whelan, J., pp. 318–329. New York: Wiley.
Fernald, R.D. & Hirata, N. (1977a). Field study of Haplochromis burtoni: Quantitative behavioral observations. Animal Behaviour 25, 964–975.Google Scholar
Fernald, R.D. & Hirata, N. (1977b). Field study of Haplochromis burtoni: Habitats and co-habitants. Environmental Biology 2, 299–308.Google Scholar
Fernald, R.D. & Liebman, P.A. (1980). Visual receptor pigments in the African cichlid fish Haplochromis burtoni. Vision Research 20, 857–864.CrossRefGoogle Scholar
Foster, R.G. & Bellingham, J. (2004). Inner retinal photoreceptors (IRPs) in mammals and teleost fish. Photochemistry and Photobiology Science 3, 617–627.CrossRefGoogle Scholar
Jacklet, J.W. (1989). Circadian neuronal oscillators. In Neuronal and Cellular Oscillators, ed. Jacklet, J., pp. 12–18. New York: Marcel Dekker.
Korenbrot, J.I. & Fernald, R.D. (1989). Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature 337, 454–457.CrossRefGoogle Scholar
Kroger, R.H., Campbell, M.C., & Fernald, R.D. (2001). The development of the crystalline lens is sensitive to visual input in the African cichlid fish, Haplochromis burtoni. Vision Research 41, 549–559.CrossRefGoogle Scholar
Land, M.F. & Fernald, R.D. (1992). The evolution of eyes. Annual Review of Neuroscience 15, 1–29.CrossRefGoogle Scholar
McFarland, W.N. & Munz, F.W. (1975). Part III: The evolution of photopic visual pigments in fishes. Vision Research 15, 1071–1080.CrossRefGoogle Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.CrossRefGoogle Scholar
Pierce, M.E., Sheshberadaran, H., Zhang, Z., Fox, L.E., Applebury, M.L., & Takahashi, J.S. (1993). Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron 10, 579–584.CrossRefGoogle Scholar
Puzzolo, D. (1989). [Morphological adaptations of the eyes of vertebrates: Retinal trophism and the response to environmental stimuli]. Italian Journal of Anatomy and Embryology 94, 317–378.Google Scholar
von Schantz, M., Lucas, R.J., & Foster, R.G. (1999). Circadian oscillation of photopigment transcript levels in the mouse retina. Brain Research Molecular Brain Research 72, 108–114.CrossRefGoogle Scholar
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 3390–3401.Google Scholar
Young, R.W. (1969). A difference between rods and cones in the renewal of outer segment protein. Investigative Ophthalmology 8, 222–231.Google Scholar
Young, R.W. (1976). Visual cells and the concept of renewal. Investigative Ophthalmology and Visual Science 15, 700–725.Google Scholar
Young, R.W. (1978). The daily rhythm of shedding and degradation of rod and cone outer segment membranes in the chick retina. Investigative Ophthalmology and Visual Science 17, 105–116.Google Scholar
Young, R.W. & Bok, D. (1969). Participation of the retinal pigment epithelium in the rod outer segment renewal process. Journal of Cell Biology 42, 392–403.CrossRefGoogle Scholar