Abstract
Ciliary and rhabdomeric opsins are employed by different kinds of photoreceptor cells, such as ciliary vertebrate rods and cones or protostome microvillar eye photoreceptors, that have specialized structures and molecular physiologies. We report unprecedented cellular co-expression of rhabdomeric opsin and a visual pigment of the recently described xenopsins in larval eyes of a mollusk. The photoreceptors bear both microvilli and cilia and express proteins that are orthologous to transporters in microvillar and ciliary opsin trafficking. Highly conserved but distinct gene structures suggest that xenopsins and ciliary opsins are of independent origin, irrespective of their mutually exclusive distribution in animals. Furthermore, we propose that frequent opsin gene loss had a large influence on the evolution, organization and function of brain and eye photoreceptor cells in bilaterian animals. The presence of xenopsin in eyes of even different design might be due to a common origin and initial employment of this protein in a highly plastic photoreceptor cell type of mixed microvillar/ciliary organization.
Highlights
Animal eyes are amongst the best-investigated sensory organs and are subject to studies in sensory biology, and in general molecular, developmental and evolutionary biology
We searched for indicators of cilia development in the photoreceptor cells (PRCs) of L. asellus by means of in-situ hybridization, i.e. we looked for the transcription factors Foxj1 and RFX, which are involved in ciliary development in xenopsin r-opsin
C-opsins drive the important process of vision, as they constitute the visual pigments of the retinal rods and cones and they serve additional functions when expressed in the pineal or in deep brain PRCs
Summary
Animal eyes are amongst the best-investigated sensory organs and are subject to studies in sensory biology, and in general molecular, developmental and evolutionary biology. The integrative data sets on eyes and their cellular components has had considerable impact on the characterization of different kinds of light-detecting cells, and on concepts how to trace their evolution and that of the organs they constitute (Arendt, 2003; Arendt et al, 2016; Oakley and Speiser, 2015; Wagner, 2014). These studies have dealt with the general question of whether gradual change or rather integration and reshuffling of modules that exist elsewhere is the main driving force in the evolution of light-detecting cell types. These findings initiated a wealth of comparative studies and resulted in pro-longed debates on whether a few conserved lineages of animal eye PRCs exist or whether both those PRCs andwhole eyes evolved multiple times independently (Eakin, 1982; von Salvini-Plawen, 1982; Vanfleteren, 1982)
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