Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
- University of Arkansas, United States
- Centro de Investigación y de Estudios Avanzados del IPN, Mexico
Abstract
Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosensory cell types - a lineage-specific sensory-effector known as the cnidocyte, and a classical mechanosensory neuron referred to as the hair cell. While developmental genetics of cnidocytes is increasingly understood, genes essential for cnidarian hair cell development are unknown. Here we show that the class IV POU homeodomain transcription factor (POU-IV) - an indispensable regulator of mechanosensory cell differentiation in Bilateria and cnidocyte differentiation in Cnidaria - controls hair cell development in the sea anemone cnidarian Nematostella vectensis. N. vectensis POU-IV is postmitotically expressed in tentacular hair cells, and is necessary for development of the apical mechanosensory apparatus, but not of neurites, in hair cells. Moreover, it binds to deeply conserved DNA recognition elements, and turns on a unique set of effector genes - including the transmembrane-receptor-encoding gene polycystin 1 - specifically in hair cells. Our results suggest that POU-IV directs differentiation of cnidarian hair cells and cnidocytes via distinct gene regulatory mechanisms, and support an evolutionarily ancient role for POU-IV in defining the mature state of mechanosensory neurons.
Data availability
Sequencing data have been deposited in GenBank under an accession number OK338071, and in BioProject database under an accession number PRJNA767103.The scripts for RNA-Seq and ChIP-seq analysis are publicly available at https://github.com/pyrosilesl97/POU-IV_analysis.
Article and author information
Author details
Pablo Yamild Rosiles-Loeza
Esteban Elías Escobar-Hernandez
Nagayasu Nakanishi
Funding
National Science Foundation (1931154)
- Nagayasu Nakanishi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Kristin Tessmar-Raible, University of Vienna, Austria
Version history
- Received: September 30, 2021
- Preprint posted: October 14, 2021 (view preprint)
- Accepted: December 22, 2021
- Accepted Manuscript published: December 23, 2021 (version 1)
- Version of Record published: February 15, 2022 (version 2)
- Version of Record updated: February 16, 2022 (version 3)
Copyright
© 2021, Ozment 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.
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Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
eLife 10:e74336.
https://doi.org/10.7554/eLife.74336
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