Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2003 Feb;163(2):663–675. doi: 10.1093/genetics/163.2.663

Gene duplication and spectral diversification of cone visual pigments of zebrafish.

Akito Chinen 1, Takanori Hamaoka 1, Yukihiro Yamada 1, Shoji Kawamura 1
PMCID: PMC1462461  PMID: 12618404

Abstract

Zebrafish is becoming a powerful animal model for the study of vision but the genomic organization and variation of its visual opsins have not been fully characterized. We show here that zebrafish has two red (LWS-1 and LWS-2), four green (RH2-1, RH2-2, RH2-3, and RH2-4), and single blue (SWS2) and ultraviolet (SWS1) opsin genes in the genome, among which LWS-2, RH2-2, and RH2-3 are novel. SWS2, LWS-1, and LWS-2 are located in tandem and RH2-1, RH2-2, RH2-3, and RH2-4 form another tandem gene cluster. The peak absorption spectra (lambdamax) of the reconstituted photopigments from the opsin cDNAs differed markedly among them: 558 nm (LWS-1), 548 nm (LWS-2), 467 nm (RH2-1), 476 nm (RH2-2), 488 nm (RH2-3), 505 nm (RH2-4), 355 nm (SWS1), 416 nm (SWS2), and 501 nm (RH1, rod opsin). The quantitative RT-PCR revealed a considerable difference among the opsin genes in the expression level in the retina. The expression of the two red opsin genes and of three green opsin genes, RH2-1, RH2-3, and RH2-4, is significantly lower than that of RH2-2, SWS1, and SWS2. These findings must contribute to our comprehensive understanding of visual capabilities of zebrafish and the evolution of the fish visual system and should become a basis of further studies on expression and developmental regulation of the opsin genes.

Full Text

The Full Text of this article is available as a PDF (506.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amores A., Force A., Yan Y. L., Joly L., Amemiya C., Fritz A., Ho R. K., Langeland J., Prince V., Wang Y. L. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998 Nov 27;282(5394):1711–1714. doi: 10.1126/science.282.5394.1711. [DOI] [PubMed] [Google Scholar]
  2. Archer S., Hope A., Partridge J. C. The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc Biol Sci. 1995 Dec 22;262(1365):289–295. doi: 10.1098/rspb.1995.0208. [DOI] [PubMed] [Google Scholar]
  3. Branchek T., Bremiller R. The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure. J Comp Neurol. 1984 Mar 20;224(1):107–115. doi: 10.1002/cne.902240109. [DOI] [PubMed] [Google Scholar]
  4. Cameron David A. Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Vis Neurosci. 2002 May-Jun;19(3):365–372. doi: 10.1017/s0952523802192121. [DOI] [PubMed] [Google Scholar]
  5. Carleton K. L., Kocher T. D. Cone opsin genes of african cichlid fishes: tuning spectral sensitivity by differential gene expression. Mol Biol Evol. 2001 Aug;18(8):1540–1550. doi: 10.1093/oxfordjournals.molbev.a003940. [DOI] [PubMed] [Google Scholar]
  6. Cowing Jill A., Poopalasundaram Subathra, Wilkie Susan E., Bowmaker James K., Hunt David M. Spectral tuning and evolution of short wave-sensitive cone pigments in cottoid fish from Lake Baikal. Biochemistry. 2002 May 14;41(19):6019–6025. doi: 10.1021/bi025656e. [DOI] [PubMed] [Google Scholar]
  7. Forsell J., Ekström P., Flamarique I. N., Holmqvist B. Expression of pineal ultraviolet- and green-like opsins in the pineal organ and retina of teleosts. J Exp Biol. 2001 Jul;204(Pt 14):2517–2525. doi: 10.1242/jeb.204.14.2517. [DOI] [PubMed] [Google Scholar]
  8. Hamaoka Takanori, Takechi Masaki, Chinen Akito, Nishiwaki Yuko, Kawamura Shoji. Visualization of rod photoreceptor development using GFP-transgenic zebrafish. Genesis. 2002 Nov;34(3):215–220. doi: 10.1002/gene.10155. [DOI] [PubMed] [Google Scholar]
  9. Hargrave P. A., McDowell J. H., Curtis D. R., Wang J. K., Juszczak E., Fong S. L., Rao J. K., Argos P. The structure of bovine rhodopsin. Biophys Struct Mech. 1983;9(4):235–244. doi: 10.1007/BF00535659. [DOI] [PubMed] [Google Scholar]
  10. Helvik J. V., Drivenes O., Naess T. H., Fjose A., Seo H. C. Molecular cloning and characterization of five opsin genes from the marine flatfish Atlantic halibut (Hippoglossus hippoglossus). Vis Neurosci. 2001 Sep-Oct;18(5):767–780. doi: 10.1017/s095252380118510x. [DOI] [PubMed] [Google Scholar]
  11. Hughes A., Saszik S., Bilotta J., Demarco P. J., Jr, Patterson W. F., 2nd Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Vis Neurosci. 1998 Nov-Dec;15(6):1029–1037. doi: 10.1017/s095252389815602x. [DOI] [PubMed] [Google Scholar]
  12. Ina Y. New methods for estimating the numbers of synonymous and nonsynonymous substitutions. J Mol Evol. 1995 Feb;40(2):190–226. doi: 10.1007/BF00167113. [DOI] [PubMed] [Google Scholar]
  13. Johnson R. L., Grant K. B., Zankel T. C., Boehm M. F., Merbs S. L., Nathans J., Nakanishi K. Cloning and expression of goldfish opsin sequences. Biochemistry. 1993 Jan 12;32(1):208–214. doi: 10.1021/bi00052a027. [DOI] [PubMed] [Google Scholar]
  14. Karnik S. S., Sakmar T. P., Chen H. B., Khorana H. G. Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8459–8463. doi: 10.1073/pnas.85.22.8459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kawamura S., Blow N. S., Yokoyama S. Genetic analyses of visual pigments of the pigeon (Columba livia). Genetics. 1999 Dec;153(4):1839–1850. doi: 10.1093/genetics/153.4.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kawamura S., Yokoyama S. Functional characterization of visual and nonvisual pigments of American chameleon (Anolis carolinensis). Vision Res. 1998 Jan;38(1):37–44. doi: 10.1016/s0042-6989(97)00160-0. [DOI] [PubMed] [Google Scholar]
  17. Kennedy B. N., Vihtelic T. S., Checkley L., Vaughan K. T., Hyde D. R. Isolation of a zebrafish rod opsin promoter to generate a transgenic zebrafish line expressing enhanced green fluorescent protein in rod photoreceptors. J Biol Chem. 2001 Jan 18;276(17):14037–14043. doi: 10.1074/jbc.M010490200. [DOI] [PubMed] [Google Scholar]
  18. Khorana H. G., Knox B. E., Nasi E., Swanson R., Thompson D. A. Expression of a bovine rhodopsin gene in Xenopus oocytes: demonstration of light-dependent ionic currents. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7917–7921. doi: 10.1073/pnas.85.21.7917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kito Y., Suzuki T., Azuma M., Sekoguti Y. Absorption spectrum of rhodopsin denatured with acid. Nature. 1968 Jun 8;218(5145):955–957. doi: 10.1038/218955a0. [DOI] [PubMed] [Google Scholar]
  20. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Levine J. S., MacNichol E. F., Jr Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sens Processes. 1979 Jun;3(2):95–131. [PubMed] [Google Scholar]
  22. Malicki J. Harnessing the power of forward genetics--analysis of neuronal diversity and patterning in the zebrafish retina. Trends Neurosci. 2000 Nov;23(11):531–541. doi: 10.1016/s0166-2236(00)01655-6. [DOI] [PubMed] [Google Scholar]
  23. Mano H., Kojima D., Fukada Y. Exo-rhodopsin: a novel rhodopsin expressed in the zebrafish pineal gland. Brain Res Mol Brain Res. 1999 Nov 10;73(1-2):110–118. doi: 10.1016/s0169-328x(99)00242-9. [DOI] [PubMed] [Google Scholar]
  24. Meyer A., Málaga-Trillo E. Vertebrate genomics: More fishy tales about Hox genes. Curr Biol. 1999 Mar 25;9(6):R210–R213. doi: 10.1016/s0960-9822(99)80131-6. [DOI] [PubMed] [Google Scholar]
  25. Molday R. S., MacKenzie D. Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry. 1983 Feb 1;22(3):653–660. doi: 10.1021/bi00272a020. [DOI] [PubMed] [Google Scholar]
  26. Nawrocki L., BreMiller R., Streisinger G., Kaplan M. Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Res. 1985;25(11):1569–1576. doi: 10.1016/0042-6989(85)90127-0. [DOI] [PubMed] [Google Scholar]
  27. Ohguro H., Johnson R. S., Ericsson L. H., Walsh K. A., Palczewski K. Control of rhodopsin multiple phosphorylation. Biochemistry. 1994 Feb 1;33(4):1023–1028. doi: 10.1021/bi00170a022. [DOI] [PubMed] [Google Scholar]
  28. Pierce M. E., Sheshberadaran H., Zhang Z., Fox L. E., Applebury M. L., Takahashi J. S. Circadian regulation of iodopsin gene expression in embryonic photoreceptors in retinal cell culture. Neuron. 1993 Apr;10(4):579–584. doi: 10.1016/0896-6273(93)90161-j. [DOI] [PubMed] [Google Scholar]
  29. Postlethwait J. H., Woods I. G., Ngo-Hazelett P., Yan Y. L., Kelly P. D., Chu F., Huang H., Hill-Force A., Talbot W. S. Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 2000 Dec;10(12):1890–1902. doi: 10.1101/gr.164800. [DOI] [PubMed] [Google Scholar]
  30. Rajendran R. R., Van Niel E. E., Stenkamp D. L., Cunningham L. L., Raymond P. A., Gonzalez-Fernandez F. Zebrafish interphotoreceptor retinoid-binding protein: differential circadian expression among cone subtypes. J Exp Biol. 1996 Dec;199(Pt 12):2775–2787. doi: 10.1242/jeb.199.12.2775. [DOI] [PubMed] [Google Scholar]
  31. Raymond P. A., Barthel L. K., Rounsifer M. E., Sullivan S. A., Knight J. K. Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Neuron. 1993 Jun;10(6):1161–1174. doi: 10.1016/0896-6273(93)90064-x. [DOI] [PubMed] [Google Scholar]
  32. Register E. A., Yokoyama R., Yokoyama S. Multiple origins of the green-sensitive opsin genes in fish. J Mol Evol. 1994 Sep;39(3):268–273. doi: 10.1007/BF00160150. [DOI] [PubMed] [Google Scholar]
  33. Robinson J., Schmitt E. A., Hárosi F. I., Reece R. J., Dowling J. E. Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6009–6012. doi: 10.1073/pnas.90.13.6009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  35. Sakmar T. P., Franke R. R., Khorana H. G. Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8309–8313. doi: 10.1073/pnas.86.21.8309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Saszik S., Bilotta J. The effects of temperature on the dark-adapted spectral sensitivity function of the adult zebrafish. Vision Res. 1999 Mar;39(6):1051–1058. doi: 10.1016/s0042-6989(98)00237-5. [DOI] [PubMed] [Google Scholar]
  37. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vihtelic T. S., Doro C. J., Hyde D. R. Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Vis Neurosci. 1999 May-Jun;16(3):571–585. doi: 10.1017/s0952523899163168. [DOI] [PubMed] [Google Scholar]
  39. Wang J. K., McDowell J. H., Hargrave P. A. Site of attachment of 11-cis-retinal in bovine rhodopsin. Biochemistry. 1980 Oct 28;19(22):5111–5117. doi: 10.1021/bi00563a027. [DOI] [PubMed] [Google Scholar]
  40. Yokoyama R., Yokoyama S. Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9315–9318. doi: 10.1073/pnas.87.23.9315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res. 2000 Jul;19(4):385–419. doi: 10.1016/s1350-9462(00)00002-1. [DOI] [PubMed] [Google Scholar]
  42. Yokoyama S., Radlwimmer F. B. The "five-sites" rule and the evolution of red and green color vision in mammals. Mol Biol Evol. 1998 May;15(5):560–567. doi: 10.1093/oxfordjournals.molbev.a025956. [DOI] [PubMed] [Google Scholar]
  43. Yokoyama S., Radlwimmer F. B. The molecular genetics and evolution of red and green color vision in vertebrates. Genetics. 2001 Aug;158(4):1697–1710. doi: 10.1093/genetics/158.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yokoyama S., Radlwimmer F. B. The molecular genetics of red and green color vision in mammals. Genetics. 1999 Oct;153(2):919–932. doi: 10.1093/genetics/153.2.919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yokoyama S., Zhang H., Radlwimmer F. B., Blow N. S. Adaptive evolution of color vision of the Comoran coelacanth (Latimeria chalumnae). Proc Natl Acad Sci U S A. 1999 May 25;96(11):6279–6284. doi: 10.1073/pnas.96.11.6279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zhang H., Futami K., Horie N., Okamura A., Utoh T., Mikawa N., Yamada Y., Tanaka S., Okamoto N. Molecular cloning of fresh water and deep-sea rod opsin genes from Japanese eel Anguilla japonica and expressional analyses during sexual maturation. FEBS Lett. 2000 Mar 3;469(1):39–43. doi: 10.1016/s0014-5793(00)01233-3. [DOI] [PubMed] [Google Scholar]
  47. Zhukovsky E. A., Oprian D. D. Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science. 1989 Nov 17;246(4932):928–930. doi: 10.1126/science.2573154. [DOI] [PubMed] [Google Scholar]
  48. von Schantz M., Lucas R. J., Foster R. G. Circadian oscillation of photopigment transcript levels in the mouse retina. Brain Res Mol Brain Res. 1999 Sep 8;72(1):108–114. doi: 10.1016/s0169-328x(99)00209-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES