Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution
- University of Vienna, Austria
- University of Manchester, United Kingdom
- CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Medical University of Vienna, Austria
Abstract
Rhabdomeric opsins (r-opsins) are light-sensors in cephalic eye photoreceptors, but also function in additional sensory organs. This has prompted questions on the evolutionary relationship of these cell types, and if ancient r-opsins were non-photosensory. A molecular profiling approach in the marine bristleworm Platynereis dumerilii revealed shared and distinct features of cephalic and non-cephalic of r-opsin1-expressing cells. Non-cephalic cells possess a full set of phototransduction components, but also a mechanosensory signature. Prompted by the latter, we investigated Platynereis putative mechanotransducer, and found nompc and pkd2.1 co-expressed with r-opsin1 in TRE cells by HCR RNA-FISH. To further assess the role of r-Opsin1 in these cells, we studied its signaling properties and unraveled that r-Opsin1 is a Gαq-coupled blue-light receptor. Profiling of cells from r-opsin1 mutants versus wild-types, and a comparison under different light conditions reveals that in the non-cephalic cells, light - mediated by r-Opsin1 - adjusts the expression level of a calcium transporter relevant for auditory mechanosensation in vertebrates. We establish a deep learning-based quantitative behavioral analysis for animal trunk movements, and identify a light- and r-Opsin-1-dependent fine-tuning of the worm's undulatory movements in headless trunks, which are known to require mechanosensory feedback. Our results provide new data on peripheral cell types of likely light-sensory/mechanosensory nature. These results point towards a concept in which such a multisensory cell type evolved to allow for fine-tuning of mechanosensation by light. This implies that light-independent mechanosensory roles of r-opsins may have evolved secondarily.
Data availability
All metadata and source files are available for download from Dryad (doi:10.5061/dryad.m63xsj416).This includes raw data, scripts, and the newly assembled and size-filtered transcriptome, used for quantitative mapping (cf. section on Transcriptome profiling).
-
Metadata for the characterization of Platynereis dumerilii cephalic and non-cephalic sensory cell typeshttps://creativecommons.org/publicdomain/zero/1.0/.
-
Metadata for the characterization of Platynereis dumerilii cephalic and non-cephalic sensory cell typeshttps://creativecommons.org/publicdomain/zero/1.0/.
Article and author information
Author details
Vinoth Babu Veedin Rajan
Kristin Tessmar-Raible
Funding
FP7 Ideas: European Research Council (FP7/2007-2013)/ERC Grant Agreement 260304)
- Florian Raible
Austrian Science Fund (P30035)
- Florian Raible
FP7 Ideas: European Research Council (ERC Grant Agreement 337011)
- Kristin Tessmar-Raible
H2020 European Research Council (ERC Grant Agreement 819952)
- Kristin Tessmar-Raible
Universität Wien (Research Platform Rhythms of Life"")
- Florian Raible
- Kristin Tessmar-Raible
Universität Wien (Research Platform Single-cell genomics of stem cells"")
- Florian Raible
Austrian Science Fund (START award,project Y413)
- Kristin Tessmar-Raible
Austrian Science Fund (P28970)
- Kristin Tessmar-Raible
Austrian Science Fund (I2972)
- Florian Raible
Austrian Science Fund (SFB F78)
- Florian Raible
- Kristin Tessmar-Raible
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All animal research and husbandry was conducted according to Austrian and European guidelines for animal research (fish maintenance and care approved under: BMWFW-66.006/0012-WF/II/3b/2014, experiments approved under: BMWFW-66.006/0003-WF/V/3b/2016
Copyright
© 2021, Revilla-i-Domingo 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
-
- 1,241
- views
-
- 151
- downloads
-
- 11
- 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)
Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution
eLife 10:e66144.
https://doi.org/10.7554/eLife.66144
Further reading
-
- Developmental Biology
The articles in this special issue highlight the diversity and complexity of research into reproductive health, including the need for a better understanding of the fundamental biology of reproduction and for new treatments for a range of reproductive disorders.
-
- Developmental Biology
During the trunk to tail transition the mammalian embryo builds the outlets for the intestinal and urogenital tracts, lays down the primordia for the hindlimb and external genitalia, and switches from the epiblast/primitive streak (PS) to the tail bud as the driver of axial extension. Genetic and molecular data indicate that Tgfbr1 is a key regulator of the trunk to tail transition. Tgfbr1 has been shown to control the switch of the neuromesodermal competent cells from the epiblast to the chordoneural hinge to generate the tail bud. We now show that in mouse embryos Tgfbr1 signaling also controls the remodeling of the lateral plate mesoderm (LPM) and of the embryonic endoderm associated with the trunk to tail transition. In the absence of Tgfbr1, the two LPM layers do not converge at the end of the trunk, extending instead as separate layers until the caudal embryonic extremity, and failing to activate markers of primordia for the hindlimb and external genitalia. The vascular remodeling involving the dorsal aorta and the umbilical artery leading to the connection between embryonic and extraembryonic circulation was also affected in the Tgfbr1 mutant embryos. Similar alterations in the LPM and vascular system were also observed in Isl1 null mutants, indicating that this factor acts in the regulatory cascade downstream of Tgfbr1 in LPM-derived tissues. In addition, in the absence of Tgfbr1 the embryonic endoderm fails to expand to form the endodermal cloaca and to extend posteriorly to generate the tail gut. We present evidence suggesting that the remodeling activity of Tgfbr1 in the LPM and endoderm results from the control of the posterior PS fate after its regression during the trunk to tail transition. Our data, together with previously reported observations, place Tgfbr1 at the top of the regulatory processes controlling the trunk to tail transition.
