Recruitment of Rod Photoreceptors from Short-Wavelength-Sensitive Cones during the Evolution of Nocturnal Vision in Mammals

Abstract

Summary Vertebrate ancestors had only cone-like photoreceptors. The duplex retina evolved in jawless vertebrates with the advent of highly photosensitive rod-like photoreceptors. Despite cones being the arbiters of high-resolution color vision, rods emerged as the dominant photoreceptor in mammals during a nocturnal phase early in their evolution. We investigated the evolutionary and developmental origins of rods in two divergent vertebrate retinae. In mice, we discovered genetic and epigenetic vestiges of short wavelength cones in developing rods and cell lineage tracing validated the genesis of rods from S-cones. Curiously, rods did not derive from S-cones in zebrafish. Our study illuminates several questions regarding the evolution of duplex retina and supports the hypothesis that, in mammals, the S-cone lineage was recruited via the Maf-family transcription factor NRL to augment rod photoreceptors. We propose that this developmental mechanism allowed the adaptive exploitation of scotopic niches during the nocturnal bottleneck early in mammalian evolution.

Melanopsin Retinal Ganglion Cells Regulate Cone Photoreceptor Lamination in the Mouse Retina

“…Among the significantly altered transcripts in P8 Opn4 DTA/DTA versus wild-type retinas, the dopamine receptor D 4 (Drd4) appeared to be a good candidate, showing significantly reduced expression (Figure 2B). DRD4 expression was confirmed to be expressed in cones in four separate transcriptional datasets (Hughes et al, 2017; Kim et al, 2016; Mo et al, 2016; Siegert et al, 2012). In the mature retina, ipRGCs are known to influence cone photoreceptor light adaptation by controlling dopamine (DA) release from dopaminergic amacrine cells (DACs) (Prigge et al, 2016; Zhang et al, 2008a), an effect dependent on the expression of DRD4 (Jackson et al, 2012).…”

Mechanisms of Photoreceptor Patterning in Vertebrates and Invertebrates

“…2D, Step 2 )(132, 152-154). Recent evolutionary studies suggest that mammalian S-cone and rod PRs may have similar lineages, and may temporally switch from S-cone precursors to rods(155). …”

Next generation sequencing technology and genomewide data analysis: Perspectives for retinal research

“…It is therefore imperative that we elucidate global profiles of transcriptome and epigenome, together with those of lncRNA, miRNA and other noncoding transcribed sequences, under normal (control) and abnormal (disease) conditions focusing on different cell types in the retina/eye and generate gene interaction networks. While a majority of reported NGS data in retina/eye originates from small number of samples and whole tissues (Farkas et al, 2013; Tian et al, 2015), several groups have initiated NGS studies on specific cell types (Macosko et al, 2015; Mo et al, 2016; Siegert et al, 2012)(Kim et al, 2016). An array of NGS data thus provides unprecedented opportunities to address fundamental questions related to gene/genome organization, function and regulation, which in turn would dramatically influence our understanding of cell physiology and pathogenic mechanisms.…”

“…However, whole tissue histone modification data might miss valuable epigenetic information on low expressed genes and those expressed in minor cell types, and such studies should be performed with purified cell types (Kim et al, 2016). New methods have been developed to perform single cell ChIP-seq experiments (Rotem et al, 2015).…”

“…Temporal transcriptome profiling of "normal" and "mutant" retina can help define how genetic changes lead to cellular dysfunction and elucidate gene networks associated with homeostasis and disease. Recent successes in generating expression profiles from single retinal cell types (Kim et al, 2016)(Siegert et al, 2012) or even from single cells (Macosko et al, 2015) are providing novel molecular insights into cell fate determination and disease mechanisms. Epigenetic changes are another major factor in influencing physiology and biological pathways.…”