Elsevier

Gene

Volume 433, Issues 1–2, 15 March 2009, Pages 50-55
Gene

Cone visual pigments in two species of South American marsupials

https://doi.org/10.1016/j.gene.2008.12.006Get rights and content

Abstract

Marsupials are largely confined to Australasia and to Central and South America. The visual pigments that underlie the photosensitivity of the retina have been examined in a number of species from the former group where evidence for trichromatic colour vision has been found, but none from the latter. In this paper, we report the cone opsin sequences from two nocturnal South American marsupial species, the gray short-tailed opossum, Monodelphis domestica, and the big-eared opossum, Didelphis aurita. Both are members of the Order Didelphimorphia (American opossums). For both species, only two classes of cone opsin were found, an SWS1 and an LWS sequence, and in vitro expression showed that the peak sensitivity of the SWS1 pigment is in the UV. Analysis of the Monodelphis genome confirms the absence of other classes of cone visual pigment genes. The SWS1 and LWS genes with 4 and 5 introns respectively, show the same exon–intron structure as found for these genes in all other vertebrates. The SWS1 gene shows a conserved synteny with flanking genes. The LWS gene is X-linked, as in all therian mammals so far examined, with a locus control region 1.54 kb upstream.

Introduction

Visual pigments belong to the large family of G protein-coupled receptors that share a common structure of seven α-helical transmembrane regions joined by cytoplasmic and luminal loops. They form a group of closely-related proteins (opsins) that bind retinal, a derivative of vitamin A. Five classes of pigment are present in vertebrates, a rod class and four different cone classes distinguished on the basis of spectral sensitivity and amino acid sequence of their respective opsins: LWS with λmax 500–570 nm, MWS with λmax 480–530 nm, and two SWS classes, SWS2 with λmax 400–470 nm, and SWS1 with λmax 355–445 nm. Mammals however have lost two of the four classes of cone visual pigments and are therefore most probably dichromats. Eutherian amd metatherian mammals retain the LWS gene along with the SWS1 gene (reviewed in Hunt et al., 2001b) whereas the protheria or egg-laying monotremes retain the LWS gene along with the SWS2 gene (Davies et al., 2007, Wakefield, 2008). Where trichromacy is present, as in primates, this is based either on a polymorphic LWS gene with alleles that encode pigments of differing λmax values (Neitz et al., 1991, Williams et al., 1992, Jacobs and Deegan, 2003) or on a duplication of the LWS gene, with the duplicated copies encoding pigments with λmax values around 535 nm (M variant) or 560 nm (L variant) (Nathans et al., 1986, Jacobs et al., 1996). In marsupials, there is also evidence for trichromacy, based on the presence of three classes of cones in some species (Arrese et al., 2002) and behavioural colour vision tests with the fat-tailed dunnart (Arrese et al. 2006b), although a third cone pigment gene has not been found (Cowing et al., 2008).

Amongst the marsupials, the focus on visual pigment evolution has been almost entirely on Australian species, with studies on both polyprotodonts (fat-tailed dunnart, numbat, quenda) and diprotodonts (honey possum, pygmy possum, quokka, Tamar wallaby, quokka) (Deeb et al., 2003, Arrese et al., 2002, 2005Arrese et al., 2006a, Cowing et al., 2008). However, marsupials are also found in Central and South America, with isolation occurring when Australia separated from Antarctica in the Eocene/Paleocene about 60 Myr ago. Photoreceptor studies are limited so far to the South American big-eared opossum, Didelphis aurita, where four subtypes of cones in a rod dominated retina have been identified (Ahnelt et al., 1995). The COS-1 antibody labeled the outer segments of three of the cone subtypes, a double cone with a principal member containing a colorless oil droplet, a single cone with an oil droplet, and another without, whereas the OS-2 antibody labeled a second group of single cones lacking oil droplets. COS-1 antibodies are known to target M and L cones expressing either the M or L variants of the LWS gene and OS-2 antibodies target S cones expressing the SWS1 gene (Rohlich and Szel, 1993). As found for Australian marsupials (Arrese et al., 2002, 2005), multiple sub-types of L/M cones are therefore present, with the possibility that more than two cone pigments may be present. In this paper, we report the cone opsin sequences from D. aurita and the related gray short-tailed opossum, Monodelphis domestica. Both are members of the Order Didelphimorphia (American opossums). No spectral data are available for the visual pigments present in these species.

Section snippets

Retinal RNA preparation

M. domestica retinal tissue was obtained from a colony established at the University of Melbourne, Victoria, Australia, and D. aurita retinal tissue from the University of Rio de Janeiro, Brazil. The study was approved by the Animal Ethics and Experimentation Committee of the University of Western Australia.

Total RNA was extracted either from freshly dissected retinae or from retinae that had been stored in RNAlater (Ambion, Austin, Texas, USA) using the EpiCentre MasterPure RNA Purification

Results and discussion

For ease of comparison, the numbering of all opsin amino acid sequences follows the bovine rod opsin numbering. For actual residue number, subtract 5 for the Monodelphis SWS1 sequence and add 16 for the Monodelphis LWS sequence.

Acknowledgments

This research was supported by grants from the Australian Research Council to CAA, LDB and DMH (35322000), and the Leverhulme Trust to DMH (F/07 134/AX). We are grateful to Professor Rosalie Crouch of the Storm Eye Institute, Medical University of South Carolina, USA for the provision of 11-cis-retinal, and to Professor Norman Saunders, University of Melbourne, Australia for the supply of Monodelphis retinal tissue.

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