Article ; Online: Identification and cellular localization in Xenopus laevis photoreceptors of three Peripherin-2 family members, Prph2, Rom1 and Gp2l, which arose from gene duplication events in the common ancestors of jawed vertebrates.
2023 Volume 239, Page(s) 109760
Abstract: Rod and cone photoreceptors are named for the distinct morphologies of their outer segment organelles, which are either cylindrical or conical, respectively. The morphologies of the stacked disks that comprise the rod and cone outer segments also differ: ...
| Abstract | Rod and cone photoreceptors are named for the distinct morphologies of their outer segment organelles, which are either cylindrical or conical, respectively. The morphologies of the stacked disks that comprise the rod and cone outer segments also differ: rod disks are completely sealed and are discontinuous from the plasma membrane, while cone disks remain partially open to the extracellular space. These morphological differences between photoreceptor types are more prominent in non-mammalian vertebrates, whose cones typically possess a greater proportion of open disks and are more tapered in shape. In mammals, the tetraspanin prph2 generates and maintains the highly curved disk rim regions by forming extended oligomeric structures with itself and a structurally similar paralog, rom1. Here we determined that in addition to these two proteins, there is a third Prph2 family paralog in most non-mammalian vertebrate species, including X. laevis: Glycoprotein 2-like protein or "Gp2l". A survey of multiple genome databases revealed a single invertebrate Prph2 'pro-ortholog' in Amphioxus, several echinoderms and in a diversity of protostomes indicating an ancient divergence from other tetraspanins. Based on phylogenetic analysis, duplication of the vertebrate predecessor likely gave rise to the Gp2l and Prph2/Rom1 clades, with a further duplication distinguishing the Prph2 and Rom1 clades. Mammals have lost Gp2l and their Rom1 has undergone a period of accelerated evolution such that it has lost several features that are retained in non-mammalian vertebrate Rom1. Specifically, Prph2, Gp2l and non-mammalian Rom1 encode proteins with consensus N-linked glycosylation and outer segment localization signals; mammalian rom1 lacks these motifs. We determined that X. laevis gp2l is expressed exclusively in cones and green rods, while X. laevis rom1 is expressed exclusively in rods, and prph2 is present in both rods and cones. The presence of three Prph2-related genes with distinct expression patterns as well as the rapid evolution of mammalian Rom1, may contribute to the more pronounced differences in morphology between rod and cone outer segments and rod and cone disks observed in non-mammalian versus mammalian vertebrates. |
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| MeSH term(s) | Animals ; Gene Duplication ; Mammals ; Peripherins/genetics ; Peripherins/metabolism ; Phylogeny ; Retinal Cone Photoreceptor Cells/metabolism ; Retinal Degeneration/metabolism ; Tetraspanins/genetics ; Xenopus laevis/genetics ; Xenopus laevis/metabolism |
| Chemical Substances | Peripherins ; Tetraspanins ; Prph2 protein, Xenopus |
| Language | English |
| Publishing date | 2023-12-28 |
| Publishing country | England |
| Document type | Journal Article |
| ZDB-ID | 80122-7 |
| ISSN | 1096-0007 ; 0014-4835 |
| ISSN (online) | 1096-0007 |
| ISSN | 0014-4835 |
| DOI | 10.1016/j.exer.2023.109760 |
| Database | MEDical Literature Analysis and Retrieval System OnLINE |
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