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

Ethan Ozment,Nagayasu Nakanishi,Jianhong Zhou,Selene L Fernandez-Valverde,Esteban Elías Escobar-Hernandez,Pablo Yamild Rosiles-Loeza,Arianna N Tamvacakis

doi:10.7554/elife.74336

Ethan Ozment, Nagayasu Nakanishi + Show 5 more

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

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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.

Highlights

One of the most fundamental sensory cell types that emerged in animal evolution is the mechanosensory cell – the specialized sensory epithelial cell that transduces mechanical stimuli into internal signals
A previous study has shown that the class IV POU homeodomain transcription factor (POU-IV or Brn-3)-encoding gene is expressed in the hair-cell-bearing mechanosensory organ called the touch plate in moon jellyfish Aurelia sp.1 (Nakanishi et al, 2010), consistent with a role in cnidarian hair cell development
Using the starlet sea anemone Nematostella vectensis, we have shown that POU-IV is postmitotically expressed in hair cells in the ectodermal epithelium of feeding tentacles during development

Summary

Introduction

One of the most fundamental sensory cell types that emerged in animal evolution is the mechanosensory cell – the specialized sensory epithelial cell that transduces mechanical stimuli (e.g. water vibration) into internal signals. Relatively little is known about the genetics of mechanoreceptor development in non-bilaterian, early-evolving animal groups such as Cnidaria (e.g. jellyfish, corals and sea anemones), Ctenophora (combjellies), Placozoa and Porifera (sponges), the knowledge of which is key to defining the ancestral conditions for mechanoreceptor development basal to Bilateria. A previous study has shown that the class IV POU homeodomain transcription factor (POU-IV or Brn-3)-encoding gene is expressed in the hair-cell-bearing mechanosensory organ called the touch plate in moon jellyfish Aurelia sp. (Nakanishi et al, 2010), consistent with a role in cnidarian hair cell development. The apical sensory apparatus, or the hair bundle, of the mechanoreceptor consists of the cilium and stereovilli of the central hair cell and the peripheral stereovilli/microvilli of support cells (Mire and Watson, 1997). We provide evidence that POU-IV regulates postmitotic differentiation of hair cells by directly activating effector genes that define mature cell identity

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Materials and Methods