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Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis

Cnidarians are the only non-bilaterian group to evolve ciliated larvae with an apical sensory organ, which is possibly homologous to the apical organs of bilaterian primary larvae. Here, we generated transcriptomes of the apical tissue in the sea anemone Nematostella vectensis and showed that it has...

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Autores principales: Gilbert, Eleanor, Teeling, Callum, Lebedeva, Tatiana, Pedersen, Siffreya, Chrismas, Nathan, Genikhovich, Grigory, Modepalli, Vengamanaidu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481973/
https://www.ncbi.nlm.nih.gov/pubmed/36000354
http://dx.doi.org/10.1242/dev.200833
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author Gilbert, Eleanor
Teeling, Callum
Lebedeva, Tatiana
Pedersen, Siffreya
Chrismas, Nathan
Genikhovich, Grigory
Modepalli, Vengamanaidu
author_facet Gilbert, Eleanor
Teeling, Callum
Lebedeva, Tatiana
Pedersen, Siffreya
Chrismas, Nathan
Genikhovich, Grigory
Modepalli, Vengamanaidu
author_sort Gilbert, Eleanor
collection PubMed
description Cnidarians are the only non-bilaterian group to evolve ciliated larvae with an apical sensory organ, which is possibly homologous to the apical organs of bilaterian primary larvae. Here, we generated transcriptomes of the apical tissue in the sea anemone Nematostella vectensis and showed that it has a unique neuronal signature. By integrating previously published larval single-cell data with our apical transcriptomes, we discovered that the apical domain comprises a minimum of six distinct cell types. We show that the apical organ is compartmentalised into apical tuft cells (spot) and larval-specific neurons (ring). Finally, we identify ISX-like (NVE14554), a PRD class homeobox gene specifically expressed in apical tuft cells, as an FGF signalling-dependent transcription factor responsible for the formation of the apical tuft domain via repression of the neural ring fate in apical cells. With this study, we contribute a comparison of the molecular anatomy of apical organs, which must be carried out across phyla to determine whether this crucial larval structure evolved once or multiple times.
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spelling pubmed-94819732022-10-25 Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis Gilbert, Eleanor Teeling, Callum Lebedeva, Tatiana Pedersen, Siffreya Chrismas, Nathan Genikhovich, Grigory Modepalli, Vengamanaidu Development Research Article Cnidarians are the only non-bilaterian group to evolve ciliated larvae with an apical sensory organ, which is possibly homologous to the apical organs of bilaterian primary larvae. Here, we generated transcriptomes of the apical tissue in the sea anemone Nematostella vectensis and showed that it has a unique neuronal signature. By integrating previously published larval single-cell data with our apical transcriptomes, we discovered that the apical domain comprises a minimum of six distinct cell types. We show that the apical organ is compartmentalised into apical tuft cells (spot) and larval-specific neurons (ring). Finally, we identify ISX-like (NVE14554), a PRD class homeobox gene specifically expressed in apical tuft cells, as an FGF signalling-dependent transcription factor responsible for the formation of the apical tuft domain via repression of the neural ring fate in apical cells. With this study, we contribute a comparison of the molecular anatomy of apical organs, which must be carried out across phyla to determine whether this crucial larval structure evolved once or multiple times. The Company of Biologists Ltd 2022-08-24 /pmc/articles/PMC9481973/ /pubmed/36000354 http://dx.doi.org/10.1242/dev.200833 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Gilbert, Eleanor
Teeling, Callum
Lebedeva, Tatiana
Pedersen, Siffreya
Chrismas, Nathan
Genikhovich, Grigory
Modepalli, Vengamanaidu
Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title_full Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title_fullStr Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title_full_unstemmed Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title_short Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
title_sort molecular and cellular architecture of the larval sensory organ in the cnidarian nematostella vectensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481973/
https://www.ncbi.nlm.nih.gov/pubmed/36000354
http://dx.doi.org/10.1242/dev.200833
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