Evolutionary history of teleost intron-containing and intron-less rhodopsin genes

Abstract

Recent progress in whole genome sequencing has revealed that animals have various kinds of opsin genes for photoreception. Among them, most opsin genes have introns in their coding regions. However, it has been known for a long time that teleost retinas express intron-less rhodopsin genes, which are presumed to have been formed by retroduplication from an ancestral intron-containing rhodopsin gene. In addition, teleosts have an intron-containing rhodopsin gene (exo-rhodopsin) exclusively for pineal photoreception. In this study, to unravel the evolutionary origin of the two teleost rhodopsin genes, we analyzed the rhodopsin genes of non-teleost fishes in the Actinopterygii. The phylogenetic analysis of full-length sequences of bichir, sturgeon and gar rhodopsins revealed that retroduplication of the rhodopsin gene occurred after branching of the bichir lineage. In addition, analysis of the tissue distribution and the molecular properties of bichir, sturgeon and gar rhodopsins showed that the abundant and exclusive expression of intron-containing rhodopsin in the pineal gland and the short lifetime of its meta II intermediate, which leads to optimization for pineal photoreception, were achieved after branching of the gar lineage. Based on these results, we propose a stepwise evolutionary model of teleost intron-containing and intron-less rhodopsin genes.

The Visual Opsin Gene Repertoires of Teleost Fishes: Evolution, Ecology, and Function

“…Gene duplication may also occur via retrotransposition, whereby mature messenger RNA post splicing is retrotranscribed and re-inserted into the genome. Two such cases have been documented in fish: The first involves RH1, which is a single-exon gene in all ray-finned fishes but bichirs (Fujiyabu et al 2019) and has originated from the retrotransposition of its common ancestor with the extraocular rhodopsin (exo-rhodopsin) (Bellingham et al 2003) (Figure 2a). While the new intron-less copy retained the ancestral function in vision, exo-rhodopsin expression mainly became restricted to the pineal gland in extant fishes, where it is involved in circadian regulation (Mano et al 1999;Pierce et al 2008).…”

Diversification processes of teleost intron-less opsin genes

“…In our previous study, we obtained the rhodopsin clones from several non-teleost fishes in the Actinopterygii and proposed a stepwise evolutionary model of teleost intron-containing and intron-less rhodopsin genes, that is, the intron-less rhodopsin gene was retroduplicated from an ancestral intron-containing rhodopsin gene after the branching of the Polypteriformes and subsequently the molecular property and tissue distribution of the ancestral intron-containing rhodopsin gene changed to be exclusively utilized for pineal photoreception in teleosts ( 13 ). After our analysis, the whole genome assemblies of gray bichir ( Polypterus senegalus ) and reedfish ( Erpetoichthys calabaricus ) in the Polypteriformes and sterlet ( Acipenser ruthenus ) and paddlefish ( Polyodon spathula ) in the Acipenseriformes were published in the public databases ( 21 , 22 ).…”

“…The intron-containing rhodopsin gene ( Rh1-1 ) was lost in the Acipenseriformes. The ancestor of the Teleostei duplicated the intron-less rhodopsin gene ( Rh1-2 , Rh1 ) by a whole genome duplication and changed the expression pattern of the intron-containing rhodopsin gene ( Exorh ( Rh1-1 )) for pineal photoreception ( 13 ). The nomenclature of rhodopsin genes we use refers to that in the previous studies ( 36 , 49 , 50 , 51 ).…”

“…In vertebrates, several intron-less opsin genes have been found in fish genomes. In a previous study, we analyzed the evolutionary process of the teleost intron-less rhodopsin gene ( 13 ). In general, vertebrates have a single intron-containing rhodopsin gene in their genomes and utilize it in rod cells for visual photoreception.…”

Decoupled spectral tuning and eye size diversification patterns in an Antarctic adaptive radiation

“…As several available notothenioid genomes were sequenced with low (10x) coverage, instances of fragmented opsin genes within scaffolds were excluded from analysis as meaningful tuning site comparisons would not be possible. Additionally, non-visual extra-ocular rhodopsin, (exo-rh1) sequences, which are similar to Rh1 but expressed in the pineal gland (Chen et al 2018; Fujiyabu et al 2019), were excluded from this study.…”