Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

  1. Ethan Ozment
  2. Arianna N Tamvacakis
  3. Jianhong Zhou
  4. Pablo Yamild Rosiles-Loeza
  5. Esteban Elías Escobar-Hernandez
  6. Selene L Fernandez-Valverde
  7. Nagayasu Nakanishi  Is a corresponding author
  1. University of Arkansas, United States
  2. 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.

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

Article and author information

Author details

  1. Ethan Ozment

    Department of Biological Sciences, University of Arkansas, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Arianna N Tamvacakis

    Department of Biological Sciences, University of Arkansas, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jianhong Zhou

    Department of Biological Sciences, University of Arkansas, Fayetteville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Pablo Yamild Rosiles-Loeza

    Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4569-9076
  5. Esteban Elías Escobar-Hernandez

    Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8892-5141
  6. Selene L Fernandez-Valverde

    Unidad de Genómica Avanzada (Langebio), Centro de Investigación y de Estudios Avanzados del IPN, Irapuato, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  7. Nagayasu Nakanishi

    Department of Biological Sciences, University of Arkansas, Fayetteville, United States
    For correspondence
    nnakanis@uark.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7516-5078

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

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Version history

  1. Received: September 30, 2021
  2. Preprint posted: October 14, 2021 (view preprint)
  3. Accepted: December 22, 2021
  4. Accepted Manuscript published: December 23, 2021 (version 1)
  5. Version of Record published: February 15, 2022 (version 2)
  6. 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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  1. Ethan Ozment
  2. Arianna N Tamvacakis
  3. Jianhong Zhou
  4. Pablo Yamild Rosiles-Loeza
  5. Esteban Elías Escobar-Hernandez
  6. Selene L Fernandez-Valverde
  7. Nagayasu Nakanishi
(2021)
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

Share this article

https://doi.org/10.7554/eLife.74336

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