Atoh1 is required for the formation of lateral line electroreceptors and hair cells, whereas Foxg1 represses an electrosensory fate
- University of Cambridge, United Kingdom
- University of South Bohemia in České Budějovice, Czech Republic
Abstract
In electroreceptive jawed fishes and amphibians, individual lateral line placodes form lines of neuromasts on the head containing mechanosensory hair cells, flanked by fields of ampullary organs containing electroreceptors - modified hair cells that respond to weak electric fields. Extensively shared gene expression between neuromasts and ampullary organs suggests that conserved molecular mechanisms are involved in their development, but a few transcription factor genes are restricted either to the developing electrosensory or mechanosensory lateral line. Here, we used CRISPR/Cas9-mediated mutagenesis in G0-injected sterlet embryos (Acipenser ruthenus, a sturgeon) to test the function of three such genes. We found that the 'hair cell' transcription factor gene Atoh1 is required for both hair cell and electroreceptor differentiation in sterlet, and for Pou4f3 and Gfi1 expression in both neuromasts and ampullary organs. These data support the conservation of developmental mechanisms between hair cells and electroreceptors. Targeting ampullary organ-restricted Neurod4 did not yield any phenotype, potentially owing to redundancy with other Neurod genes that we found to be expressed in sterlet ampullary organs. After targeting mechanosensory-restricted Foxg1, ampullary organs formed within neuromast lines, suggesting that Foxg1 normally represses their development, whether directly or indirectly. We speculate that electrosensory organs may be the 'default' developmental fate of lateral line primordia in electroreceptive vertebrates.
Data availability
The original data required to reproduce the claims of the paper are provided in the manuscript and supplementary figures, together with additional image files deposited into the Dryad database (DOI: 10.5061/dryad.fqz612k3s). Previously published sterlet transcriptome assemblies (from pooled yolk-sac larvae at stages 40-45; Minařík et al., 2024) are available at DDBJ/EMBL/GenBank under the accessions GKLU00000000 (https://www.ncbi.nlm.nih.gov/nuccore/GKLU00000000) and GKEF01000000 (https://www.ncbi.nlm.nih.gov/nuccore/GKEF00000000.1). Previously published paddlefish RNA-seq data (from pooled paddlefish opercula and fin tissue at stage 46; Modrell et al., 2017a) are available via the NCBI Gene Expression Omnibus (GEO) database (https://www.ncbi.nlm.nih.gov/geo/) under accession code GSE92470.
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Data from: Atoh1 is required for the formation of lateral line electroreceptors and hair cells, whereas Foxg1 represses an electrosensory fateDryad Digital Repository, doi:10.5061/dryad.fqz612k3s.
Article and author information
Author details
Alexander S Campbell
Funding
Biotechnology and Biological Sciences Research Council (BB/P001947/1)
- Clare VH Baker
Isaac Newton Trust (Grant 20.07(c))
- Clare VH Baker
Anatomical Society (Research Studentship)
- Alexander S Campbell
- Clare VH Baker
Cambridge Philosophical Society (Research Studentship)
- Alexander S Campbell
School of the Biological Sciences, University of Cambridge
- Martin Minařík
Ministry of Education, Youth and Sports of the Czech Republic (Projects CENAKVA (LM2018099) and Biodiversity (CZ.02.1.01/0.0/0.0/16_025/0007370))
- Roman Franěk
- Michaela Vazačová
- Martin Pšenička
Czech Science Foundation (Project 22-31141J)
- Roman Franěk
- Michaela Vazačová
- Martin Pšenička
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Sterlet animal work was reviewed and approved by The Animal Research Committee of Research Institute of Fish Culture and Hydrobiology, Faculty of Fisheries and Protection of Waters, University of South Bohemia in České Budějovice, Vodňany, Czech Republic and Ministry of Agriculture of the Czech Republic (MSMT-12550/2016-3). Experimental fish were maintained according to the principles of the European Union (EU) Harmonized Animal Welfare Act of the Czech Republic, and Principles of Laboratory Animal Care and National Laws 246/1992 "Animal Welfare" on the protection of animals.
Copyright
© 2025, Minařík et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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Atoh1 is required for the formation of lateral line electroreceptors and hair cells, whereas Foxg1 represses an electrosensory fate
eLife 14:e96285.
https://doi.org/10.7554/eLife.96285
