1. Developmental Biology
  2. Evolutionary Biology

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
https://doi.org/10.7554/eLife.74336
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 2,955
    views
  • 404
    downloads
  • 12
    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)

  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

Categories and tags

Further reading

    1. Developmental Biology
    2. Stem Cells and Regenerative Medicine

    Single-cell RNA sequencing of the holothurian regenerating intestine reveals the pluripotency of the coelomic epithelium

    Joshua G Medina-Feliciano, Griselle Valentín-Tirado ... José E Garcia-Arraras
    Research Article

    In holothurians, the regenerative process following evisceration involves the development of a ‘rudiment’ or ‘anlage’ at the injured end of the mesentery. This regenerating anlage plays a pivotal role in the formation of a new intestine. Despite its significance, our understanding of the molecular characteristics inherent to the constituent cells of this structure has remained limited. To address this gap, we employed state-of-the-art scRNA-seq and hybridization chain reaction fluorescent in situ hybridization analyses to discern the distinct cellular populations associated with the regeneration anlage. Through this approach, we successfully identified 13 distinct cell clusters. Among these, two clusters exhibit characteristics consistent with putative mesenchymal cells, while another four show features akin to coelomocyte cell populations. The remaining seven cell clusters collectively form a large group encompassing the coelomic epithelium of the regenerating anlage and mesentery. Within this large group of clusters, we recognized previously documented cell populations such as muscle precursors, neuroepithelial cells, and actively proliferating cells. Strikingly, our analysis provides data for identifying at least four other cellular populations that we define as the precursor cells of the growing anlage. Consequently, our findings strengthen the hypothesis that the coelomic epithelium of the anlage is a pluripotent tissue that gives rise to diverse cell types of the regenerating intestinal organ. Moreover, our results provide the initial view into the transcriptomic analysis of cell populations responsible for the amazing regenerative capabilities of echinoderms.

    1. Cell Biology
    2. Developmental Biology

    Ovarian Biology: Revisiting the rete ovarii

    Yan Zhang, Hua Zhang
    Insight

    Long thought to have little relevance to ovarian physiology, the rete ovarii may have a role in follicular dynamics and reproductive health.

    1. Cell Biology
    2. Developmental Biology

    Rediscovering the rete ovarii, a secreting auxiliary structure to the ovary

    Dilara N Anbarci, Jennifer McKey ... Blanche Capel
    Research Article

    The rete ovarii (RO) is an appendage of the ovary that has been given little attention. Although the RO appears in drawings of the ovary in early versions of Gray’s Anatomy, it disappeared from recent textbooks, and is often dismissed as a functionless vestige in the adult ovary. Using PAX8 immunostaining and confocal microscopy, we characterized the fetal development of the RO in the context of the mouse ovary. The RO consists of three distinct regions that persist in adult life, the intraovarian rete (IOR), the extraovarian rete (EOR), and the connecting rete (CR). While the cells of the IOR appear to form solid cords within the ovary, the EOR rapidly develops into a convoluted tubular epithelium ending in a distal dilated tip. Cells of the EOR are ciliated and exhibit cellular trafficking capabilities. The CR, connecting the EOR to the IOR, gradually acquires tubular epithelial characteristics by birth. Using microinjections into the distal dilated tip of the EOR, we found that luminal contents flow toward the ovary. Mass spectrometry revealed that the EOR lumen contains secreted proteins potentially important for ovarian function. We show that the cells of the EOR are closely associated with vasculature and macrophages, and are contacted by neuronal projections, consistent with a role as a sensory appendage of the ovary. The direct proximity of the RO to the ovary and its integration with the extraovarian landscape suggest that it plays an important role in ovary development and homeostasis.