Abstract
Microspectrophotometric (msp) studies have shown that the colour-vision system of many bird species is based on four pigments with absorption peaks in the red, green, blue and UV regions of the spectrum. The existence of a fourth pigment (UV) is the major difference between the trichromacy of humans and the tetrachromacy of such birds, and recent studies have shown that it may play a determining role in such diverse aspects of behaviour as mate selection and detection of food. Avian visual pigments are composed of an opsin protein covalently bound via a Schiff-base linkage to the chromophore 11-cis-retinal. Here we report the cDNA sequence of a UV opsin isolated from an avian species, Melopsittacus undulatus (budgerigar or small parakeet). This sequence has been expressed using the recombinant baculovirus system; the pigment generated from the expressed protein on addition of 11-cis-retinal yielded an absorption spectrum typical of a UV photopigment, with lambdamax 365+/-3 nm. This is the first UV opsin from an avian species to be sequenced and expressed in a heterologous system. In situ hybridization of this sequence to budgerigar retinas selectively labelled a sub-set of UV cones, representing approx. 9% of the total cone population, that are distributed in a semi-regular pattern across the entire retina.
Full Text
The Full Text of this article is available as a PDF (494.0 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baldwin J. M. The probable arrangement of the helices in G protein-coupled receptors. EMBO J. 1993 Apr;12(4):1693–1703. doi: 10.1002/j.1460-2075.1993.tb05814.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barthel L. K., Raymond P. A. Improved method for obtaining 3-microns cryosections for immunocytochemistry. J Histochem Cytochem. 1990 Sep;38(9):1383–1388. doi: 10.1177/38.9.2201738. [DOI] [PubMed] [Google Scholar]
- Bowmaker J. K., Heath L. A., Wilkie S. E., Hunt D. M. Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res. 1997 Aug;37(16):2183–2194. doi: 10.1016/s0042-6989(97)00026-6. [DOI] [PubMed] [Google Scholar]
- Bowmaker J. K., Thorpe A., Douglas R. H. Ultraviolet-sensitive cones in the goldfish. Vision Res. 1991;31(3):349–352. doi: 10.1016/0042-6989(91)90087-l. [DOI] [PubMed] [Google Scholar]
- Curcio C. A., Allen K. A., Sloan K. R., Lerea C. L., Hurley J. B., Klock I. B., Milam A. H. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J Comp Neurol. 1991 Oct 22;312(4):610–624. doi: 10.1002/cne.903120411. [DOI] [PubMed] [Google Scholar]
- Groenendijk G. W., De Grip W. J., Daemen F. J. Quantitative determination of retinals with complete retention of their geometric configuration. Biochim Biophys Acta. 1980 Mar 21;617(3):430–438. doi: 10.1016/0005-2760(80)90009-0. [DOI] [PubMed] [Google Scholar]
- Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
- Hisatomi O., Satoh T., Barthel L. K., Stenkamp D. L., Raymond P. A., Tokunaga F. Molecular cloning and characterization of the putative ultraviolet-sensitive visual pigment of goldfish. Vision Res. 1996 Apr;36(7):933–939. doi: 10.1016/0042-6989(95)00189-1. [DOI] [PubMed] [Google Scholar]
- Hárosi F. I. An analysis of two spectral properties of vertebrate visual pigments. Vision Res. 1994 Jun;34(11):1359–1367. doi: 10.1016/0042-6989(94)90134-1. [DOI] [PubMed] [Google Scholar]
- Jacobs G. H., Neitz J., Deegan J. F., 2nd Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature. 1991 Oct 17;353(6345):655–656. doi: 10.1038/353655a0. [DOI] [PubMed] [Google Scholar]
- Janssen J. J., Bovee-Geurts P. H., Merkx M., DeGrip W. J. Histidine tagging both allows convenient single-step purification of bovine rhodopsin and exerts ionic strength-dependent effects on its photochemistry. J Biol Chem. 1995 May 12;270(19):11222–11229. doi: 10.1074/jbc.270.19.11222. [DOI] [PubMed] [Google Scholar]
- Jeffery G., Williams A. Is abnormal retinal development in albinism only a mammalian problem? Normality of a hypopigmented avian retina. Exp Brain Res. 1994;100(1):47–57. doi: 10.1007/BF00227278. [DOI] [PubMed] [Google Scholar]
- Kawamura S., Yokoyama S. Phylogenetic relationships among short wavelength-sensitive opsins of American chameleon (Anolis carolinensis) and other vertebrates. Vision Res. 1996 Sep;36(18):2797–2804. doi: 10.1016/0042-6989(96)00034-x. [DOI] [PubMed] [Google Scholar]
- Loew E. R., Govardovskii V. I., Röhlich P., Szél A. Microspectrophotometric and immunocytochemical identification of ultraviolet photoreceptors in geckos. Vis Neurosci. 1996 Mar-Apr;13(2):247–256. doi: 10.1017/s0952523800007483. [DOI] [PubMed] [Google Scholar]
- Makino C. L., Dodd R. L. Multiple visual pigments in a photoreceptor of the salamander retina. J Gen Physiol. 1996 Jul;108(1):27–34. doi: 10.1085/jgp.108.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Merbs S. L., Nathans J. Role of hydroxyl-bearing amino acids in differentially tuning the absorption spectra of the human red and green cone pigments. Photochem Photobiol. 1993 Nov;58(5):706–710. doi: 10.1111/j.1751-1097.1993.tb04956.x. [DOI] [PubMed] [Google Scholar]
- Nathans J. Determinants of visual pigment absorbance: identification of the retinylidene Schiff's base counterion in bovine rhodopsin. Biochemistry. 1990 Oct 16;29(41):9746–9752. doi: 10.1021/bi00493a034. [DOI] [PubMed] [Google Scholar]
- Nathans J. Rhodopsin: structure, function, and genetics. Biochemistry. 1992 Jun 2;31(21):4923–4931. doi: 10.1021/bi00136a001. [DOI] [PubMed] [Google Scholar]
- Ohtsuka T. Fluorescence from colorless oil droplets: a new criterion for identification of cone photoreceptors. Neurosci Lett. 1984 Dec 21;52(3):241–245. doi: 10.1016/0304-3940(84)90168-x. [DOI] [PubMed] [Google Scholar]
- Okano T., Kojima D., Fukada Y., Shichida Y., Yoshizawa T. Primary structures of chicken cone visual pigments: vertebrate rhodopsins have evolved out of cone visual pigments. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5932–5936. doi: 10.1073/pnas.89.13.5932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Partridge J. C., De Grip W. J. A new template for rhodopsin (vitamin A1 based) visual pigments. Vision Res. 1991;31(4):619–630. doi: 10.1016/0042-6989(91)90002-m. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Starace D. M., Knox B. E. Activation of transducin by a Xenopus short wavelength visual pigment. J Biol Chem. 1997 Jan 10;272(2):1095–1100. doi: 10.1074/jbc.272.2.1095. [DOI] [PubMed] [Google Scholar]
- Stenkamp D. L., Hisatomi O., Barthel L. K., Tokunaga F., Raymond P. A. Temporal expression of rod and cone opsins in embryonic goldfish retina predicts the spatial organization of the cone mosaic. Invest Ophthalmol Vis Sci. 1996 Feb;37(2):363–376. [PubMed] [Google Scholar]
- Szél A., Röhlich P., Caffé A. R., Juliusson B., Aguirre G., Van Veen T. Unique topographic separation of two spectral classes of cones in the mouse retina. J Comp Neurol. 1992 Nov 15;325(3):327–342. doi: 10.1002/cne.903250302. [DOI] [PubMed] [Google Scholar]
- Vissers P. M., DeGrip W. J. Functional expression of human cone pigments using recombinant baculovirus: compatibility with histidine tagging and evidence for N-glycosylation. FEBS Lett. 1996 Oct 28;396(1):26–30. doi: 10.1016/0014-5793(96)01064-2. [DOI] [PubMed] [Google Scholar]