scholarly journals Six6 and Six7 coordinately regulate expression of middle-wavelength opsins in zebrafish

2019 ◽  
Vol 116 (10) ◽  
pp. 4651-4660 ◽  
Author(s):  
Yohey Ogawa ◽  
Tomoya Shiraki ◽  
Yoshimasa Asano ◽  
Akira Muto ◽  
Koichi Kawakami ◽  
...  

Color discrimination in the vertebrate retina is mediated by a combination of spectrally distinct cone photoreceptors, each expressing one of multiple cone opsins. The opsin genes diverged early in vertebrate evolution into four classes maximally sensitive to varying wavelengths of light: UV (SWS1), blue (SWS2), green (RH2), and red (LWS) opsins. Although the tetrachromatic cone system is retained in most nonmammalian vertebrate lineages, the transcriptional mechanism underlying gene expression of the cone opsins remains elusive, particularly for SWS2 and RH2 opsins, both of which have been lost in the mammalian lineage. In zebrafish, which have all four cone subtypes,rh2opsin gene expression depends on a homeobox transcription factor,sine oculishomeobox 7 (Six7). However, thesix7gene is found only in the ray-finned fish lineage, suggesting the existence of another evolutionarily conserved transcriptional factor(s) controllingrh2opsin expression in vertebrates. Here, we found that the reducedrh2expression caused bysix7deficiency was rescued by forced expression ofsix6b, which is asix7-related transcription factor conserved widely among vertebrates. The compensatory role ofsix6bwas reinforced by ChIP-sequencing analysis, which revealed a similar pattern of Six6b- and Six7-binding sites within and near the cone opsin genes. TAL effector nuclease-induced genetic ablation ofsix6bandsix7revealed that they coordinately regulate SWS2 opsin gene expression. Mutant larvae deficient for these transcription factors showed severely impaired visually driven foraging behavior. These results demonstrate that in zebrafish,six6bandsix7govern expression of the SWS2 and RH2 opsins responsible for middle-wavelength sensitivity, which would be physiologically important for daylight vision.

1999 ◽  
Vol 16 (3) ◽  
pp. 601-605 ◽  
Author(s):  
ELLEN A. SCHMITT ◽  
GEORGE A. HYATT ◽  
JOHN E. DOWLING

We report here a reexamination of the developmental expression of cone opsins in the zebrafish retina. The red- and blue-sensitive opsins appear at 51 h postfertilization (hpf) whereas ultraviolet (UV) opsin is not seen until after 55 hpf. More cells show red cone opsin expression than blue at 51 and 55 hpf, indicating the sequence of cone opsin expression in zebrafish is first red, then blue, and finally UV. Curiously, morphological development of the cones is in reverse order; UV cones appear quite mature by day 6–7 postfertilization (pf), but morphologically, red cones do not appear adult-like until 15–20 days pf.


2018 ◽  
Author(s):  
Fabio Cortesi ◽  
Karen M Cheney ◽  
Georgina M Cooke ◽  
Terry Ord

Evolutionary adaptations to life on land include changes to the physiology, morphology and behaviour of an animal in response to physical differences between water and air. The visual systems of amphibious species show pronounced morphological adaptations; yet, whether molecular changes also occur remains largely unknown. Here, we investigated the molecular evolution of visual pigment genes (opsins) in amphibious and terrestrial fishes belonging to the Salariini division of blennies (Blenniidae). We hypothesized that when conquering land, blenny opsins adapt, in terms of sequence variation and/or gene expression, to match both higher light intensities as well as the broader light spectrum. Using retinal transcriptomes in six species ranging from fully aquatic to fully terrestrial, we found very little variation in opsin gene sequences or gene expression between species. All blennies expressed a single rod opsin gene as well as two cone opsin genes sensitive to longer-wavelengths of light: RH2A-1 (green-sensitive) and LWS (red-sensitive). They also expressed one or two short-wavelength-sensitive cone opsin genes (SWS2Aα, SWS2Aβ; blue-sensitive) in a phylogenetically inert manner. However, based on amino acid predictions, both SWS2A proteins confer similar peak spectral sensitivities and differential expression is therefore unlikely to be ecologically significant. Red-sensitivity is likely beneficial for feeding on algae and detritus, the main food source of Salariini blennies, and could be co-adapted to perceive visual displays in terrestrial species, which often use red dorsal fins to signal during aggressive disputes and courtship. Our data suggests that on the molecular level, the visual systems that evolved in aquatic blennies have been retained in species that have transitioned onto land.


2020 ◽  
Author(s):  
Nik Lupše ◽  
Fabio Cortesi ◽  
Marko Freese ◽  
Lasse Marohn ◽  
Jan-Dag Pohlman ◽  
...  

AbstractDeep-sea fishes show extraordinary visual adaptations to an environment where every photon of light that is captured might make the difference between life and death. While considerable effort has been made in understanding how adult deep-sea fishes see their world, relatively little is known about vision in earlier life stages. Similar to most marine species, larval deep-sea fishes start their life in the well-lit epipelagic zone, where food is abundant and predation relatively low. In this study, we show major changes in visual gene expression between larval and adult deep-sea fishes from eight different orders (Argentiniformes, Aulopiformes, Beryciformes, Myctophiformes, Pempheriformes, Scombriformes, Stomiiformes and Trachichthyiformes). Comparison between 18 species revealed that while adults mostly rely on rod opsin(s) (RH1) for vision in dim-light, larvae mostly express green-sensitive cone opsin(s) (RH2) in their retinas. Adults of the scombriform and three aulopiform species also expressed low levels of RH2, with the latter using different copies of the gene between ontogenetic stages. Cone opsins in adult fishes are rather surprising as most deep-sea fishes have lost their cone photoreceptors in favour of a highly sensitive pure rod retina. The expression of RH2 in larvae, on the other hand, shows that even in species that might not have any cones as adults, the larval retina is likely to be cone dominated first, before rod photoreceptors are added through ontogeny. Our study therefore supports a conserved pathway for the cone-to-rod developmental sequence of the teleost or even vertebrate retina.


2016 ◽  
Vol 113 (27) ◽  
pp. E3911-E3920 ◽  
Author(s):  
Eden Kleiman ◽  
Haiqun Jia ◽  
Salvatore Loguercio ◽  
Andrew I. Su ◽  
Ann J. Feeney

Ying Yang 1 (YY1) is a ubiquitously expressed transcription factor shown to be essential for pro–B-cell development. However, the role of YY1 in other B-cell populations has never been investigated. Recent bioinformatics analysis data have implicated YY1 in the germinal center (GC) B-cell transcriptional program. In accord with this prediction, we demonstrated that deletion of YY1 by Cγ1-Cre completely prevented differentiation of GC B cells and plasma cells. To determine if YY1 was also required for the differentiation of other B-cell populations, we deleted YY1 with CD19-Cre and found that all peripheral B-cell subsets, including B1 B cells, require YY1 for their differentiation. Transitional 1 (T1) B cells were the most dependent upon YY1, being sensitive to even a half-dosage of YY1 and also to short-term YY1 deletion by tamoxifen-induced Cre. We show that YY1 exerts its effects, in part, by promoting B-cell survival and proliferation. ChIP-sequencing shows that YY1 predominantly binds to promoters, and pathway analysis of the genes that bind YY1 show enrichment in ribosomal functions, mitochondrial functions such as bioenergetics, and functions related to transcription such as mRNA splicing. By RNA-sequencing analysis of differentially expressed genes, we demonstrated that YY1 normally activates genes involved in mitochondrial bioenergetics, whereas it normally down-regulates genes involved in transcription, mRNA splicing, NF-κB signaling pathways, the AP-1 transcription factor network, chromatin remodeling, cytokine signaling pathways, cell adhesion, and cell proliferation. Our results show the crucial role that YY1 plays in regulating broad general processes throughout all stages of B-cell differentiation.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Daniel J Denman ◽  
Jennifer A Luviano ◽  
Douglas R Ollerenshaw ◽  
Sissy Cross ◽  
Derric Williams ◽  
...  

Mammalian visual behaviors, as well as responses in the neural systems underlying these behaviors, are driven by luminance and color contrast. With constantly improving tools for measuring activity in cell-type-specific populations in the mouse during visual behavior, it is important to define the extent of luminance and color information that is behaviorally accessible to the mouse. A non-uniform distribution of cone opsins in the mouse retina potentially complicates both luminance and color sensitivity; opposing gradients of short (UV-shifted) and middle (blue/green) cone opsins suggest that color discrimination and wavelength-specific luminance contrast sensitivity may differ with retinotopic location. Here we ask how well mice can discriminate color and wavelength-specific luminance changes across visuotopic space. We found that mice were able to discriminate color and were able to do so more broadly across visuotopic space than expected from the cone-opsin distribution. We also found wavelength-band-specific differences in luminance sensitivity.


2015 ◽  
Vol 282 (1812) ◽  
pp. 20150659 ◽  
Author(s):  
Yohey Ogawa ◽  
Tomoya Shiraki ◽  
Daisuke Kojima ◽  
Yoshitaka Fukada

Colour discrimination in vertebrates requires cone photoreceptor cells in the retina, and high-acuity colour vision is endowed by a set of four cone subtypes expressing UV-, blue-, green- and red-sensitive opsins. Previous studies identified transcription factors governing cone photoreceptor development in mice, although loss of blue and green opsin genes in the evolution of mammals make it difficult to understand how high-acuity colour vision was organized during evolution and development. Zebrafish ( Danio rerio ) represents a valuable vertebrate model for studying colour vision as it retains all the four ancestral vertebrate cone subtypes. Here, by RT-qPCR and in situ hybridization analysis, we found that sine oculis homeobox homolog 7 ( six7 ), a transcription factor widely conserved in ray-finned fish, is expressed predominantly in the cone photoreceptors in zebrafish at both the larval and the adult stages. TAL effector nuclease-based six7 knock-out revealed its roles in expression of green, red and blue cone opsin genes. Most prominently, the six7 deficiency caused a loss of expression of all the green opsins at both the larval and adult stages. six7 is indispensable for the development and/or maintenance of the green cones.


2006 ◽  
Vol 23 (3-4) ◽  
pp. 379-385 ◽  
Author(s):  
MAUREEN NEITZ ◽  
SHAWN D. BALDING ◽  
CARRIE MCMAHON ◽  
STACY A. SJOBERG ◽  
JAY NEITZ

The topographical distributions of the relative ratio of long- (L) and middle- (M) wavelength sensitive cone opsin messenger RNA (mRNA) in human and baboon retinas were mapped using real-time polymerase chain reaction. The L:M mRNA ratio increased in a central-to-peripheral gradient in both species, being quite pronounced for humans.


2016 ◽  
Vol 88 (3-4) ◽  
pp. 204-212 ◽  
Author(s):  
Da-Wei Liu ◽  
Ying Lu ◽  
Hong Young Yan ◽  
Harold H. Zakon

Losses of cone opsin genes are noted in animals that are nocturnal or rely on senses other than vision. We investigated the cone opsin repertoire of night-active South American weakly electric fish. We obtained opsin gene sequences from genomic DNA of 3 gymnotiforms (Eigenmannia virescens, Sternopygus macrurus, Apteronotus albifrons) and the assembled genome of the electric eel (Electrophorus electricus). We identified genes for long-wavelength-sensitive (LWS) and medium-wavelength-sensitive cone opsins (RH2) and rod opsins (RH1). Neither of the 2 short-wavelength-sensitive cone opsin genes were found and are presumed lost. The fact that Electrophorus has a complete repertoire of extraretinal opsin genes and conservation of synteny with the zebrafish (Danio rerio) for genes flanking the 2 short-wavelength-sensitive opsin genes supports the supposition of gene loss. With microspectrophotometry and electroretinograms we observed absorption spectra consistent with RH1 and LWS but not RH2 opsins in the retinal photoreceptors of E. virescens. This profile of opsin genes and their retinal expression is identical to the gymnotiform's sister group, the catfish, which are also nocturnally active and bear ampullary electroreceptors, suggesting that this pattern likely occurred in the common ancestor of gymnotiforms and catfish. Finally, we noted an unusual N-terminal motif lacking a conserved glycosylation consensus site in the RH2 opsin of gymnotiforms, a catfish and a characin (Astyanax mexicanus). Mutations at this site influence rhodopsin trafficking in mammalian photoreceptors and cause retinitis pigmentosa. We speculate that this unusual N terminus may be related to the absence of the RH2 opsin in the cones of gymnotiforms and catfish.


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