Co-expression of xenopsin and rhabdomeric opsin in photoreceptors bearing microvilli and cilia

Abstract

Ciliary and rhabdomeric opsins are employed by cells differing fundamentally in structure and molecular physiology, such as ciliary vertebrate rods and cones and protostome microvillar eye photoreceptors. We report unprecedented cellular co-expression of rhabdomeric opsin and a visual pigment of the recently described xenopsins in larval eyes of a mollusk. The photoreceptors bear both microvilli and cilia and express orthologs to transporters for microvillar and ciliary opsin trafficking. Highly conserved but distinct gene structures suggest that xenopsins and ciliary opsins are of independent origin, irrespective of their mutually exclusive distribution in animals.Furthermore, we propose that frequent opsin gene loss had big influence on evolution, organization and function of brain and eye photoreceptor cells in bilaterian animals. Presence of xenopsin in eyes of even different design might be due to common origin and initial employment in a highly plastic photoreceptor cell type of mixed microvillar/ciliary organization.

Data availability

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Oliver Vöcking

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    For correspondence
    voecking@pitt.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Ioannis Kourtesis

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  3. Sharat Chandra Tumu

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  4. Harald Hausen

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    For correspondence
    harald.hausen@uib.no
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2788-2835

Funding

Universitetet i Bergen

  • Harald Hausen

Norges Forskningsråd

  • Harald Hausen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Russ Fernald, Stanford University, United States

Version history

  1. Received: November 22, 2016
  2. Accepted: September 1, 2017
  3. Accepted Manuscript published: September 6, 2017 (version 1)
  4. Version of Record published: October 19, 2017 (version 2)

Copyright

© 2017, Vöcking et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,474
    views
  • 546
    downloads
  • 51
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Oliver Vöcking
  2. Ioannis Kourtesis
  3. Sharat Chandra Tumu
  4. Harald Hausen
(2017)
Co-expression of xenopsin and rhabdomeric opsin in photoreceptors bearing microvilli and cilia
eLife 6:e23435.
https://doi.org/10.7554/eLife.23435

Share this article

https://doi.org/10.7554/eLife.23435

Further reading

    1. Genetics and Genomics
    Can Hu, Xue-Ting Zhu ... Jin-Qiu Zhou
    Research Article

    Telomeres, which are chromosomal end structures, play a crucial role in maintaining genome stability and integrity in eukaryotes. In the baker’s yeast Saccharomyces cerevisiae, the X- and Y’-elements are subtelomeric repetitive sequences found in all 32 and 17 telomeres, respectively. While the Y’-elements serve as a backup for telomere functions in cells lacking telomerase, the function of the X-elements remains unclear. This study utilized the S. cerevisiae strain SY12, which has three chromosomes and six telomeres, to investigate the role of X-elements (as well as Y’-elements) in telomere maintenance. Deletion of Y’-elements (SY12), X-elements (SY12XYΔ+Y), or both X- and Y’-elements (SY12XYΔ) did not impact the length of the terminal TG1-3 tracks or telomere silencing. However, inactivation of telomerase in SY12, SY12XYΔ+Y, and SY12XYΔ cells resulted in cellular senescence and the generation of survivors. These survivors either maintained their telomeres through homologous recombination-dependent TG1-3 track elongation or underwent microhomology-mediated intra-chromosomal end-to-end joining. Our findings indicate the non-essential role of subtelomeric X- and Y’-elements in telomere regulation in both telomerase-proficient and telomerase-null cells and suggest that these elements may represent remnants of S. cerevisiae genome evolution. Furthermore, strains with fewer or no subtelomeric elements exhibit more concise telomere structures and offer potential models for future studies in telomere biology.

    1. Genetics and Genomics
    2. Neuroscience
    Bohan Zhu, Richard I Ainsworth ... Javier González-Maeso
    Research Article

    Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.