Partitioning of gene expression among zebrafish photoreceptor subtypes

Yohey Ogawa,Joseph C Corbo

doi:10.1038/s41598-021-96837-z

Yohey Ogawa, Joseph C Corbo

Open Access

https://doi.org/10.1038/s41598-021-96837-z

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Journal: Scientific Reports	Publication Date: Aug 30, 2021
Citations: 26	License type: open-access

Affiliation: Washington University in St. Louis

Abstract

Vertebrate photoreceptors are categorized into two broad classes, rods and cones, responsible for dim- and bright-light vision, respectively. While many molecular features that distinguish rods and cones are known, gene expression differences among cone subtypes remain poorly understood. Teleost fishes are renowned for the diversity of their photoreceptor systems. Here, we used single-cell RNA-seq to profile adult photoreceptors in zebrafish, a teleost. We found that in addition to the four canonical zebrafish cone types, there exist subpopulations of green and red cones (previously shown to be located in the ventral retina) that express red-shifted opsin paralogs (opn1mw4 or opn1lw1) as well as a unique combination of cone phototransduction genes. Furthermore, the expression of many paralogous phototransduction genes is partitioned among cone subtypes, analogous to the partitioning of the phototransduction paralogs between rods and cones seen across vertebrates. The partitioned cone-gene pairs arose via the teleost-specific whole-genome duplication or later clade-specific gene duplications. We also discovered that cone subtypes express distinct transcriptional regulators, including many factors not previously implicated in photoreceptor development or differentiation. Overall, our work suggests that partitioning of paralogous gene expression via the action of differentially expressed transcriptional regulators enables diversification of cone subtypes in teleosts.

Highlights

Prior studies showed differential expression of these green and red cone opsin paralogs across the retina and over developmental time[17], but the physiological role unique to each individual opsin paralog remains largely unknown
We discovered numerous transcriptional regulators associated with differential gene expression across zebrafish photoreceptor subtypes; many of these factors were not previously known to be associated with photoreceptor gene regulation
We identified a distinctive subpopulation of green and red cones concentrated in the ventral region of the retina, which expresses redshifted opsin paralogs and a unique complement of phototransduction genes

Summary

Introduction

Prior studies showed differential expression of these green and red cone opsin paralogs across the retina and over developmental time[17], but the physiological role unique to each individual opsin paralog remains largely unknown. Studies have begun to identify additional transcription factors required for the development of specific cone subtypes: tbx2b in UV c ones[30], foxq[2] in blue c ones[31], six6a, six6b, and six[7] in blue and green cones[32], and thrb in red c ones[33,34]. Despite these advances, the architecture of the transcriptional regulatory networks that govern photoreceptor diversification. We discovered numerous transcriptional regulators associated with differential gene expression across zebrafish photoreceptor subtypes; many of these factors were not previously known to be associated with photoreceptor gene regulation

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Conclusion