A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells

Development ◽  
1997 ◽  
Vol 124 (9) ◽  
pp. 1665-1673 ◽  
Author(s):  
D. Papatsenko ◽  
G. Sheng ◽  
C. Desplan

The photoreceptor cells of the Drosophila compound eye are precisely organized in elementary units called ommatidia. The outer (R1-R6) and inner (R7, R8) photoreceptors represent two physiologically distinct systems with two different projection targets in the brain (for review see Hardie, 1985). All cells of the primary system, R1-R6, express the same rhodopsin and are functionally identical. In contrast, the R7 and R8 photoreceptors are different from each other. They occupy anatomically precise positions, with R7 on top of R8. In fact, there are several classes of R7/R8 pairs, which differ morphologically and functionally and are characterized by the expression of one of two R7-specific opsins, rh3 or rh4. Here, we describe the identification of a new opsin gene, rhodopsin 5, expressed in one subclass of R8 cells. Interestingly, this subclass represents R8 cells that are directly underneath the R7 photoreceptors expressing rh3, but are never under those expressing rh4. These results confirm the existence of two subpopulations of R7 and R8 cells, which coordinate the expression of their respective rh genes. Thus, developmental signaling pathways between R7 and R8 lead to the exclusive expression of a single rhodopsin gene per cell and to the coordinate expression of another one in the neighboring cell. Consistent with this, rh5 expression in R8 disappears when R7 cells are absent (in sevenless mutant). We propose a model for the concerted evolution of opsin genes and the elaboration of the architecture of the retina.

Author(s):  
Zuzana Musilova ◽  
Walter Salzburger ◽  
Fabio Cortesi

Visual opsin genes expressed in the rod and cone photoreceptor cells of the retina are core components of the visual sensory system of vertebrates. Here, we provide an overview of the dynamic evolution of visual opsin genes in the most species-rich group of vertebrates, teleost fishes. The examination of the rich genomic resources now available for this group reveals that fish genomes contain more copies of visual opsin genes than are present in the genomes of amphibians, reptiles, birds, and mammals. The expansion of opsin genes in fishes is due primarily to a combination of ancestral and lineage-specific gene duplications. Following their duplication, the visual opsin genes of fishes repeatedly diversified at the same key spectral-tuning sites, generating arrays of visual pigments sensitive from the ultraviolet to the red spectrum of the light. Species-specific opsin gene repertoires correlate strongly with underwater light habitats, ecology, and color-based sexual selection. Expected final online publication date for the Annual Review of Cell and Developmental Biology, Volume 37 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.


Development ◽  
1999 ◽  
Vol 126 (4) ◽  
pp. 607-616 ◽  
Author(s):  
W.H. Chou ◽  
A. Huber ◽  
J. Bentrop ◽  
S. Schulz ◽  
K. Schwab ◽  
...  

Opsin gene expression in the R7 and R8 photoreceptor cells of the Drosophila compound eye is highly coordinated. We have found that the R8 cell specific Rh5 and Rh6 opsins are expressed in non-overlapping sets of R8 cells, in a precise pairwise fashion with Rh3 and Rh4 in the R7 cells of individual ommatidia. Removal of the R7 cells in sevenless, boss or sina mutants, disrupts Rh5 expression and dramatically increases the number of Rh6-expressing R8 cells. This suggests that the expression of Rh5 may be induced by an Rh3-expressing R7 cell, whereas Rh6 expression is most likely a default state of the R8 cell. We found that the paired expression of opsin genes in the R7 and R8 cells occurs in a sevenless and boss independent manner. Furthermore, we found that the generation of both Rh3- and Rh4-expressing R7 cells can occur in the absence of an R8 cell. These results suggest that the specification of opsin expression in the R7 cells may occur autonomously, whereas the R7 photoreceptor cell may be responsible for regulating a binary developmental switch between induced and default cell-fates in the R8 cell.


2021 ◽  
Author(s):  
Yohey Ogawa ◽  
Tomoya Shiraki ◽  
Yoshitaka Fukada ◽  
Daisuke Kojima

In vertebrates, daylight vision is mediated by a combination of spectrally distinct cone photoreceptor cells. Most vertebrate lineages retain a tetrachromatic cone system in which each cone photoreceptor subtype expresses one of four cone opsins: UV- (SWS1), blue- (SWS2), green- (RH2), and red-sensitive (LWS) opsins. Each cone subtype identity is established by a transcriptional network directing selective opsin gene expression in single photoreceptors. Our knowledge is limited regarding gene expression mechanisms for the middle wavelength-sensitive opsin genes, sws2 and rh2, because they are absent in mammalian species such as mouse, whose visual system has been extensively studied. Our previous studies identified homeobox transcription factors, Six6 and Six7, as crucial regulators of both sws2 and rh2 gene expression in zebrafish. Yet it remains unclear how these two opsin genes are selectively expressed in a cone subtype-specific manner. Here we pursued loss-of-function studies on transcription factors expressed predominantly in zebrafish cone photoreceptors and found that sws2 expression requires a forkhead box transcription factor, Foxq2, which is retained in many vertebrates having sws2 gene. A quantitative gene expression analysis using purified pools of the four cone subtypes revealed that foxq2 was expressed only in SWS2 cone subtype. foxq2 expression was abrogated in six6a/six6b/six7 knock-out zebrafish, which is deficient in SWS2 cone subtype. Forced expression of foxq2 fully restored sws2 expression in six7 knock-out fish without affecting rh2 expression. We propose a core transcriptional network that determines SWS2 cone subtype identity in the tetrachromatic vertebrate.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Quentin Guignard ◽  
Johannes Spaethe ◽  
Bernard Slippers ◽  
Martin Strube-Bloss ◽  
Jeremy D. Allison

AbstractA precondition for colour vision is the presence of at least two spectral types of photoreceptors in the eye. The order Hymenoptera is traditionally divided into the Apocrita (ants, bees, wasps) and the Symphyta (sawflies, woodwasps, horntails). Most apocritan species possess three different photoreceptor types. In contrast, physiological studies in the Symphyta have reported one to four photoreceptor types. To better understand the evolution of photoreceptor diversity in the Hymenoptera, we studied the Symphyta Sirex noctilio, which belongs to the superfamily Siricoidea, a closely related group of the Apocrita suborder. Our aim was to (i) identify the photoreceptor types of the compound eye by electroretinography (ERG), (ii) characterise the visual opsin genes of S. noctilio by genomic comparisons and phylogenetic analyses and (iii) analyse opsin mRNA expression. ERG measurements revealed two photoreceptor types in the compound eye, maximally sensitive to 527 and 364 nm. In addition, we identified three opsins in the genome, homologous to the hymenopteran green or long-wavelength sensitive (LW) LW1, LW2 and ultra-violet sensitive (UV) opsin genes. The LW1 and UV opsins were found to be expressed in the compound eyes, and LW2 and UV opsins in the ocelli. The lack of a blue or short-wavelength sensitive (SW) homologous opsin gene and a corresponding receptor suggests that S. noctilio is a UV-green dichromate.


2021 ◽  
Author(s):  
Quentin Guignard ◽  
Johannes Spaethe ◽  
Bernard Slippers ◽  
Martin Strube-Bloss ◽  
Jeremy D. Allison

Abstract A precondition for colour vision is the presence of at least two spectral types of photoreceptors in the eye. The order Hymenoptera is traditionally divided into the Apocrita (ants, bees, wasps) and the Symphyta (sawflies, woodwasps, horntails). Most apocritan species possess three different photoreceptor types. In contrast, physiological studies in the Symphyta have reported one to four photoreceptor types. To better understand the evolution of photoreceptor diversity in the Hymenoptera, we studied Sirex noctilio, which belongs to the superfamily Siricoidea, a sister group of the Apocrita. Our aim was to i) identify the photoreceptor types of the compound eye by electroretinography (ERG), ii) characterise the visual opsins genes of S. noctilio by genomic comparisons and phylogenetic analyses and iii) analyse opsin mRNA expression. ERG measurements revealed two photoreceptor types in the compound eye, maximally sensitive to 527 and 364 nm. In addition, we identified three opsins in the genome, homologous to the hymenopteran LW1, LW2 and UV opsin genes. The LW1 and UV opsins were found to be expressed in the compound eyes, and LW2 and UV opsins in the ocelli. The lack of a SW-homologous opsin gene and a corresponding receptor suggests that S. noctilio is a UV-green dichromate.


Development ◽  
1992 ◽  
Vol 114 (2) ◽  
pp. 355-366 ◽  
Author(s):  
A.R. Campos ◽  
K.F. Fischbach ◽  
H. Steller

The importance of retinal innervation for the normal development of the optic ganglia in Drosophila is well documented. However, little is known about retrograde effects of the optic lobe on the adult photoreceptor cells (R-cells). We addressed this question by examining the survival of R-cells in mutant flies where R-cells do not connect to the brain. Although imaginal R-cells develop normally in the absence of connections to the optic lobes, we find that their continued survival requires these connections. Genetic mosaic studies with the disconnected (disco) mutation demonstrate that survival of R-cells does not depend on the genotype of the eye, but is correlated with the presence of connections to the optic ganglia. These results suggest the existence of retrograde interactions in the Drosophila visual system reminiscent of trophic interactions found in vertebrates.


Author(s):  
Matti Järvilehto ◽  
Riitta Harjula

The photoreceptor cells in the compound eyes of higher diptera are clustered in groups (ommatidia) of eight receptor cells. The cells from six adjacent ommatidia are organized into optical units, neuro-ommatia sharing the same visual field. In those ommatidia the optical axes of the photopigment containing structures (rhabdomeres) are parallel. The rhabdomeres of the photoreceptor cells are separated from each other by an interstitial i.e innerommatidial space (IOS). In the photoreceptor cell body, besides of the normal cell organelles, a cellular matrix is a structurally apparent component. Similar kind of reticular formation is also found in the IOS containing some unidentified filamentary substance, of which composition and functional significance for optical properties of vision is the aim of this report.The prefixed (2% PA + 0.2% GA in 0.1-n phosphate buffer, pH 7.4, for 1h), frozen section blocks of the compound eye of the blowfly (Calliphora erythrocephala) were prepared by immuno-cryo-techniques. The ultrathin cryosections were incubated with antibodies of monoclonal α-tubulin and polyclonal smooth muscle actin. Control labelings of excess of antigen, non-immune serum and non-present antibody were perforated.


1992 ◽  
Vol 101 (1) ◽  
pp. 247-254 ◽  
Author(s):  
J.L. Hicks ◽  
D.S. Williams

The Drosophila ninaC gene encodes for two head-specific proteins of 132 kDa and 174 kDa. Their predicted amino acid sequences indicate that they may have myosin I and kinase properties. We have: (1) determined the cellular and subcellular distributions of the ninaC proteins in the Drosophila retina by electron microscopic immunocytochemistry with an antibody specific for epitopes shared by both proteins; (2) characterized the ultrastructure of the mutant phenotype. The proteins were detected only in the photoreceptor cells, but were detected in all classes of the compound eye photoreceptors. Within the photoreceptors, they were found in the rhabdomeral microvilli and the cytoplasm adjacent to the rhabdomeres. This distribution coincides with that shown previously for actin filaments. Immunolabelling of tissue from the ninaC P221 mutant, which lacks the 174 kDa protein, and two mutants whose rhabdomeres degenerate, suggests that the 132 kDa protein is present primarily in the cytoplasm adjacent to the rhabdomeres, and that the 174 kDa protein is concentrated in the rhabdomeres. Our ultrastructural analysis showed that the axial cytoskeleton of the rhabdomeral microvilli (which contains filamentous actin) was absent in both the null and P221 mutants. In the photoreceptor cell cytoplasm, the number of multivesicular bodies in the null mutant, but not the P221 mutant, was 3-fold greater in comparison with wild-type.(ABSTRACT TRUNCATED AT 250 WORDS)


The axons of the primary photoreceptor cells of the compound eye of the fly interweave in a complex but definite pattern before they terminate upon the second-order neurons. Of approximately 650 short retinula axons from behind 120 facets of the eye none terminated at an incorrect lamina cartridge. Six, seven, or eight first-order terminals upon one pair of second-order cells are arranged in a rotational sequence that is related to the positions of the retinula cells within the ommatidia. Errors in location of the terminal among its neighbours occurred only ten times. The asymmetry of the receptor pattern in the dorsal half of the eye has a mirror image in the ventral half. Along the equator of the eye is a plane of symmetry which many axons necessarily cross in maintaining the appropriate connexions of their receptors. Axons which cross this plane of symmetry have somehow found their appropriate second-order cells, although to do so they must have grown through a milieu which is the mirror image of that in their own half of the eye. Each pair of second-order axons proceeding from the lamina forms a small bundle with the axons of the two long retinula cells that have the same visual axis. Between the lamina and the medulla is a chiasma (with the crossing in the horizontal plane) through which bundles from the lamina pass to project in exactly reverse order upon the medulla. No errors of projection have been found at the single neuron level in this chiasma.


1997 ◽  
Vol 3 (S2) ◽  
pp. 1129-1130
Author(s):  
John Archie Pollock ◽  
Bejon T. Maneckshana ◽  
Teresa E. Leonardo

The compound eye of the fruit fly, Drosophila melanogaster, is composed of a highly ordered array of facets (FIG. 1), each containing a precise set of neurons and supporting cells. The eye arises during the third larval instar from an undifferentiated epithelium, the eye imaginai disc, which is connected to the brain via the optic stalk (FIG. 2). During eye development, movement of the morphogenetic furrow, progressive recruitment of specific cell types and the growth of photoreceptor axons into the brain are each dynamic processes that are routinely studied indirectly in fixed tissues. While stereotyped development and the ‘crystalline’ like structure of the eye facilitates this analysis, certain experiments are hindered by the inability to observe developmental processes as they occur. To overcome this limitation, we have combined organ culture with advanced microscopy tools to enable the observation of eye development in living tissue.


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