Dataset Information

Glass confers rhabdomeric photoreceptor identity in Drosophila, but not across all metazoans.

ABSTRACT: Across metazoans, visual systems employ different types of photoreceptor neurons (PRs) to detect light. These include rhabdomeric PRs, which exist in distantly related phyla and possess an evolutionarily conserved phototransduction cascade. While the development of rhabdomeric PRs has been thoroughly studied in the fruit fly Drosophila melanogaster, we still know very little about how they form in other species. To investigate this question, we tested whether the transcription factor Glass, which is crucial for instructing rhabdomeric PR formation in Drosophila, may play a similar role in other metazoans. Glass homologues exist throughout the animal kingdom, indicating that this protein evolved prior to the metazoan radiation. Interestingly, our work indicates that glass is not expressed in rhabdomeric photoreceptors in the planarian Schmidtea mediterranea nor in the annelid Platynereis dumerilii. Combined with a comparative analysis of the Glass DNA-binding domain, our data suggest that the fate of rhabdomeric PRs is controlled by Glass-dependent and Glass-independent mechanisms in different animal clades.

SUBMITTER: Bernardo-Garcia FJ

PROVIDER: S-EPMC6399963 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Glass confers rhabdomeric photoreceptor identity in <i>Drosophila</i>, but not across all metazoans.

Bernardo-Garcia F Javier FJ Syed Maryam M Jékely Gáspár G Sprecher Simon G SG

EvoDevo 20190305

Across metazoans, visual systems employ different types of photoreceptor neurons (PRs) to detect light. These include rhabdomeric PRs, which exist in distantly related phyla and possess an evolutionarily conserved phototransduction cascade. While the development of rhabdomeric PRs has been thoroughly studied in the fruit fly <i>Drosophila melanogaster</i>, we still know very little about how they form in other species. To investigate this question, we tested whether the transcription factor Glas ...[more]

PMID: 30873275

Similar Datasets

Project description:Phototransduction reactions in the rhabdomeric photoreceptor are profoundly stochastic due to the small number of participating molecules and small reaction space. The resulting quantum bumps (QBs) vary in their timing (latency), amplitudes and durations, and these variabilities within each cell are not correlated. Using modeling and electrophysiological recordings, we investigated how the QB properties depend on the cascade speed and how they influence signal transfer. Parametric analysis in the model supported by experimental data revealed that faster cascades elicit larger and narrower QBs with faster onsets and smaller variabilities than slower cascades. Latency dispersion was stronger affected by modification of upstream than downstream activation parameters. The variability caused by downstream modifications closely matched the experimental variability. Frequency response modeling showed that corner frequency is a reciprocal function of the characteristic duration of the multiphoton response, which, in turn, is a non-linear function of QB duration and latency dispersion. All QB variabilities contributed noise but only latency dispersion slowed and spread multiphoton responses, lowering the corner frequency. Using the discovered QB correlations, we evaluated transduction noise for dissimilar species and two extreme adaptation states, and compared it to photon noise. The noise emitted by the cascade was non-additive and depended non-linearly on the interaction between the QB duration and the three QB variabilities. Increased QB duration strongly suppressed both noise and corner frequency. This trade-off might be acceptable for nocturnal but not diurnal species because corner frequency is the principal determinant of information capacity. To offset the increase in noise accompanying the QB narrowing during light adaptation and the response-expanding effect of latency dispersion, the cascade accelerates. This explains the widespread evolutionary tendency of diurnal fliers to have fast phototransduction, especially after light adaptation, which thus appears to be a common adaptation to contain stochasticity, improve SNR and expand the bandwidth.

Project description:BackgroundRhabdomeric photoreceptors of eyes in the terrestrial slug Limax are the typical invertebrate-type but unique in that three visual opsins (Gq-coupled rhodopsin, xenopsin, Opn5A) and one retinochrome, all belonging to different groups, are co-expressed. However, molecular properties including spectral sensitivity and G protein selectivity of any of them are not determined, which prevents us from understanding an advantage of multiplicity of opsin properties in a single rhabdomeric photoreceptor. To gain insight into the functional role of the co-expression of multiple opsin species in a photoreceptor, we investigated the molecular properties of the visual opsins in the present study.ResultsFirst, we found that the fourth member of visual opsins, Opn5B, is also co-expressed in the rhabdomere of the photoreceptor together with previously identified three opsins. The photoreceptors were also demonstrated to express Gq and Go alpha subunits. We then determined the spectral sensitivity of the four visual opsins using biochemical and spectroscopic methods. Gq-coupled rhodopsin and xenopsin exhibit maximum sensitivity at ~ 456 and 475 nm, respectively, and Opn5A and Opn5B exhibit maximum sensitivity at ~ 500 and 470 nm, respectively, with significant UV sensitivity. Notably, in vitro experiments revealed that Go alpha was activated by all four visual opsins, in contrast to the specific activation of Gq alpha by Gq-coupled rhodopsin, suggesting that the eye photoreceptor of Limax uses complex G protein signaling pathways.ConclusionsThe eye photoreceptor in Limax expresses as many as four different visual opsin species belonging to three distinct classes. The combination of opsins with different spectral sensitivities and G protein selectivities may underlie physiological properties of the ocular photoreception, such as a shift in spectral sensitivity between dark- and light-adapted states. This may be allowed by adjustment of the relative contribution of the four opsins without neural networks, enabling a simple strategy for fine-tuning of vision.

Project description:IntroductionIn Annelida two types of photoreceptor cells (PRCs) are regarded as generally present, rhabdomeric and ciliary PRCs. In certain taxa, however, an additional type of PRC may occur, the so called phaosomal PRC. Whereas the former two types of PRCs are always organized as an epithelium with their sensory processes projecting into an extracellular cavity formed by the PRCs and (pigmented) supportive cells, phaosomes are seemingly intracellular vacuoles housing the sensory processes. Phaosomal PRCs are the only type of PRC found in one major annelid group, Clitellata. Several hypotheses have been put forward explaining the evolutionary origin of the clitellate phaosomes. To elucidate the evolution of clitellate PRC and eyes the leech Helobdella robusta, for which a sequenced genome is available, was chosen.ResultsTEM observations showed that extraocular and ocular PRCs are structurally identical. Bioinformatic analyses revealed predictions for four opsin genes, three of which could be amplified. All belong to the rhabdomeric opsin family and phylogenetic analyses showed them in a derived position within annelid opsins. Gene expression studies showed two of them expressed in the eye and in the extraocular PRCs. Polychaete eye-typic key enzymes for ommochromme and pterin shading pigments synthesis are not expressed in leech eyes.ConclusionsBy comparative gene-expression studies we herein provide strong evidence that the phaosomal PRCs typical of Clitellata are derived from the rhabdomeric PRCs characteristic for polychaete adult eyes. Thus, they represent a highly derived type of PRC that evolved in the stem lineage of Clitellata rather than another, primitive type of PRC in Metazoa. Evolution of these PRCs in Clitellata is related to a loss of the primary eyes and most of their photoreceptive elements except for the rhabdomeric PRCs. Most likely this happened while changing to an endobenthic mode of life. This hypothesis of PRC evolution is in accordance with a recently published phylogeny of Annelida based on phylogenomic data. The data provide a nice example how morphologically highly divergent light sensitive structures emerged from a standard type of photoreceptor cell.

Dataset Information

Glass confers rhabdomeric photoreceptor identity in Drosophila, but not across all metazoans.

Publications

Glass confers rhabdomeric photoreceptor identity in <i>Drosophila</i>, but not across all metazoans.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets