Loss and gain of cone types in vertebrate ciliary photoreceptor evolution

Abstract

Ciliary photoreceptors are a diverse cell type family that comprises the rods and cones of the retina and other related cell types such as pineal photoreceptors. Ciliary photoreceptor evolution has been dynamic during vertebrate evolution with numerous gains and losses of opsin and phototransduction genes, and changes in their expression. For example, early mammals lost all but two cone opsins, indicating loss of cone receptor types in response to nocturnal lifestyle. Our review focuses on the comparison of specifying transcription factors and cell type-specific transcriptome data in vertebrate retinae to build and test hypotheses on ciliary photoreceptor evolution. Regarding cones, recent data reveal that a combination of factors specific for long-wavelength sensitive opsin (Lws)- cones in non-mammalian vertebrates (Thrb and Rxrg) is found across all differentiating cone photoreceptors in mice. This suggests that mammalian ancestors lost all but one ancestral cone type, the Lws-cone. We test this hypothesis by a correlation analysis of cone transcriptomes in mouse and chick, and find that, indeed, transcriptomes of all mouse cones are most highly correlated to avian Lws-cones. These findings underscore the importance of specifying transcription factors in tracking cell type evolution, and shed new light on the mechanisms of cell type loss and gain in retina evolution.

Tbx2amodulates switching of opsin gene expression

“…More recently, this possibility was further supported by a dataset from single cell transcriptomes of mouse retinal cells generated by Macosko et al (36). Reanalysis of this dataset revealed that none of the "pure" Sws1 cones expressed Tbx2, yet some of the cones co-expressing Sws1 and Lws did show Tbx2 expression (28,36). This pattern raises the possibility that the role of Tbx2a in promoting LWS expression could be conserved in even distantly related vertebrate lineages.…”

“…6). In this region we also identified predicted binding sites for six transcription factors that are known to play key roles in retinal development across vertebrates (28,29); Rxrg, Thrb, Sall3, Vsx1, Rax, and Vsx2 ( Fig. 6).…”

“…The Tbx2 class of transcription factors predates the vertebrate lineage and unlike the other T-box transcription factors, members of the Tbx2/3 class are known to act as repressors as well as activators (34). Musser and Arendt (28) showed that the Tbx2 class has played a strong role in photoreceptor development since well before the emergence of the mammalian lineage. While mammals have lost the RH2 class of opsins, they have maintained both LWS and TBX2.…”

“…The list was then reviewed for transcription factors known to play key roles in vertebrate photoreceptor development (28).…”

Ciliary photoreceptors in sea urchin larvae indicate pan-deuterostome cell type conservation

“…Comparative analyses have demonstrated considerable similarity among the ciliary photoreceptors and eyes within vertebrates [12,13]. At the morphological level, vertebrate eyes have a distinct position in respect to the brain, anterior and on the left and right side, and include rod and cone ciliary photoreceptors as well as neurons, pigment cells and other cell types.…”