The retinal mosaics of opsin expression in invertebrates and vertebrates

Abstract

Colour vision is found in many invertebrate and vertebrate species. It is the ability to discriminate objects based on the wavelength of emitted light independent of intensity. As it requires the comparison of at least two photoreceptor types with different spectral sensitivities, this process is often mediated by a mosaic made of several photoreceptor types. In this review, we summarize the current knowledge about the formation of retinal mosaics and the regulation of photopigment (opsin) expression in the fly, mouse and human retina. Despite distinct evolutionary origins, as well as major differences in morphology and phototransduction machineries, there are significant similarities in the stepwise cell-fate decisions that lead from progenitor cells to terminally differentiated photoreceptors that express a particular opsin. Common themes include i) the use of binary transcriptional switches that distinguish classes of photoreceptors, ii) the use of gradients of signaling molecules for regional specializations, iii) stochastic choices that pattern the retina and iv) the use of permissive factors with multiple roles in different photoreceptor types.

So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice

“…The expression of different Rhodopsin (Rh) genes in ''inner photoreceptors'' R7 and R8, the equivalent of vertebrate cone cells, defines at least four distinct ommatidial subtypes ( Fig. 2A; Rister and Desplan 2011). One subtype forms a narrow band of morphologically distinct ommatidia in the ''dorsal rim area'' (DRA) of the retina (Tomlinson 2003;Wernet et al 2003), where it measures the vector of polarized light emanating from the sky for navigation (Wolf et al 1980;Weir and Dickinson 2012;Wernet et al 2012).…”

“…A considerable body of work has focused on the specification of cell types of the retina; for instance, the designation of different classes of photoreceptors with distinct spectral sensitivities in the Drosophila retina (Rister and Desplan 2011) and the establishment of the various cell types that comprise the vertebrate retina: photoreceptors, Muller glia, interneurons (horizontal, amacrine, and bipolar cells), and retinal ganglion cells (RGCs) (Livesey and Cepko 2001;Mu et al 2004; Poch e and Reese 2006). With that knowledge in hand, focus in recent years has expanded to understanding how the circuits formed by these retinal cells are linked to the staggering number of diverse visual neurons in the brain, which in turn enables sophisticated and diverse computational tasks.…”

Establishing and maintaining gene expression patterns: insights from sensory receptor patterning

“…To achieve this, the visual and olfactory systems deploy large numbers of sensory receptors (SRs). For example, five Rhodopsin genes are differentially expressed in the fly retina (Rister and Desplan, 2011), while over 1200 olfactory receptor genes are expressed in the nose of the mouse (Buck and Axel, 1991). In sensory systems of high discriminatory power, each sensory neuron generally expresses only one or very few SR gene(s), excluding all others (Mazzoni et al, 2004;Mombaerts, 2004;Serizawa et al, 2004).…”

“…Five Rh proteins -Rh1 (NinaE -FlyBase), Rh3, Rh4, Rh5 and Rh6 -with different spectral sensitivities are expressed in two classes of PRs in the Drosophila retina (Rister and Desplan, 2011). The 'outer' PRs (R1-R6) span the length of the ommatidium and express Rh1, which has a broad sensitivity to blue-green wavelengths ( Fig.…”

“…These TFs play a part in controlling terminal PR differentiation by restricting the Rh genes that each PR can express (reviewed by Rister and Desplan, 2011). As summarized above, the outer PRs R1-R6 exclusively express Rh1, whereas R7s can express Rh3 and/or Rh4, and R8s can express either Rh5 or Rh6 (Mollereau et al, 2001;Cook et al, 2003;Tahayato et al, 2003;Johnston et al, 2011).…”