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.
Reviewing Editor
- Claude Desplan, New York University, United States
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
Version history
- Received: December 30, 2020
- Preprint posted: January 12, 2021 (view preprint)
- Accepted: August 4, 2021
- Accepted Manuscript published: August 5, 2021 (version 1)
- Version of Record published: August 16, 2021 (version 2)
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
-
- 1,118
- views
-
- 141
- downloads
-
- 10
- 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
-
- Chromosomes and Gene Expression
- Developmental Biology
Developmental programming involves the accurate conversion of signalling levels and dynamics to transcriptional outputs. The transcriptional relay in the Notch pathway relies on nuclear complexes containing the co-activator Mastermind (Mam). By tracking these complexes in real time, we reveal that they promote the formation of a dynamic transcription hub in Notch ON nuclei which concentrates key factors including the Mediator CDK module. The composition of the hub is labile and persists after Notch withdrawal conferring a memory that enables rapid reformation. Surprisingly, only a third of Notch ON hubs progress to a state with nascent transcription, which correlates with polymerase II and core Mediator recruitment. This probability is increased by a second signal. The discovery that target-gene transcription is probabilistic has far-reaching implications because it implies that stochastic differences in Notch pathway output can arise downstream of receptor activation.
-
- Developmental Biology
Large-scale cell flow characterizes gastrulation in animal development. In amniote gastrulation, particularly in avian gastrula, a bilateral vortex-like counter-rotating cell flow, called ‘polonaise movements’, appears along the midline. Here, through experimental manipulations, we addressed relationships between the polonaise movements and morphogenesis of the primitive streak, the earliest midline structure in amniotes. Suppression of the Wnt/planar cell polarity (PCP) signaling pathway maintains the polonaise movements along a deformed primitive streak. Mitotic arrest leads to diminished extension and development of the primitive streak and maintains the early phase of the polonaise movements. Ectopically induced Vg1, an axis-inducing morphogen, generates the polonaise movements, aligned to the induced midline, but disturbs the stereotypical cell flow pattern at the authentic midline. Despite the altered cell flow, induction and extension of the primitive streak are preserved along both authentic and induced midlines. Finally, we show that ectopic axis-inducing morphogen, Vg1, is capable of initiating the polonaise movements without concomitant PS extension under mitotic arrest conditions. These results are consistent with a model wherein primitive streak morphogenesis is required for the maintenance of the polonaise movements, but the polonaise movements are not necessarily responsible for primitive streak morphogenesis. Our data describe a previously undefined relationship between the large-scale cell flow and midline morphogenesis in gastrulation.
