Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells

In tunicates, the coronal organ represents a sentinel checking particle entrance into the pharynx. The organ differentiates from an anterior embryonic area considered a proto-placode. For their embryonic origin, morphological features and function, coronal sensory cells have been hypothesized to be...

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Main Authors: Rigon, F, Gasparini, F, Shimeld, S, Candiani, S, Manni, L
Format: Journal article
Published: Wiley 2017
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author Rigon, F
Gasparini, F
Shimeld, S
Candiani, S
Manni, L
author_facet Rigon, F
Gasparini, F
Shimeld, S
Candiani, S
Manni, L
author_sort Rigon, F
collection OXFORD
description In tunicates, the coronal organ represents a sentinel checking particle entrance into the pharynx. The organ differentiates from an anterior embryonic area considered a proto-placode. For their embryonic origin, morphological features and function, coronal sensory cells have been hypothesized to be homologues to vertebrate hair cells. However, vertebrate hair cells derive from a posterior placode. This contradicts one of the principle historical criteria for homology, similarity of position, which could be taken as evidence against coronal cells/hair cells homology. In the tunicates Ciona intestinalis and C. robusta, we found that the coronal organ expresses genes (Atoh, Notch, Delta-like, Hairy-b and Musashi) characterizing vertebrate neural and hair cell development. Moreover, coronal cells exhibit a complex synaptic connectivity pattern, and utilize neurotransmitters (Glu, ACh, GABA, 5-HT and catecholamines) involved in hair cell activity. Lastly, coronal cells express the Trpa gene, which encodes an ion channel expressed in hair cells. These data lead us to hypothesise a model in which competence to make secondary mechanoreceptors was primitively broadly distributed through placode territories, but has become confined to different placodes during the evolution of the vertebrate and tunicate lineages.
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spelling oxford-uuid:1aadb16e-02d8-4a3a-bbe6-4580b68ed1762022-03-26T10:56:13ZDevelopmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cellsJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:1aadb16e-02d8-4a3a-bbe6-4580b68ed176Symplectic Elements at OxfordWiley2017Rigon, FGasparini, FShimeld, SCandiani, SManni, LIn tunicates, the coronal organ represents a sentinel checking particle entrance into the pharynx. The organ differentiates from an anterior embryonic area considered a proto-placode. For their embryonic origin, morphological features and function, coronal sensory cells have been hypothesized to be homologues to vertebrate hair cells. However, vertebrate hair cells derive from a posterior placode. This contradicts one of the principle historical criteria for homology, similarity of position, which could be taken as evidence against coronal cells/hair cells homology. In the tunicates Ciona intestinalis and C. robusta, we found that the coronal organ expresses genes (Atoh, Notch, Delta-like, Hairy-b and Musashi) characterizing vertebrate neural and hair cell development. Moreover, coronal cells exhibit a complex synaptic connectivity pattern, and utilize neurotransmitters (Glu, ACh, GABA, 5-HT and catecholamines) involved in hair cell activity. Lastly, coronal cells express the Trpa gene, which encodes an ion channel expressed in hair cells. These data lead us to hypothesise a model in which competence to make secondary mechanoreceptors was primitively broadly distributed through placode territories, but has become confined to different placodes during the evolution of the vertebrate and tunicate lineages.
spellingShingle Rigon, F
Gasparini, F
Shimeld, S
Candiani, S
Manni, L
Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title_full Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title_fullStr Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title_full_unstemmed Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title_short Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
title_sort developmental signature synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells
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AT shimelds developmentalsignaturesynapticconnectivityandneurotransmissionareconservedbetweenvertebratehaircellsandtunicatecoronalcells
AT candianis developmentalsignaturesynapticconnectivityandneurotransmissionareconservedbetweenvertebratehaircellsandtunicatecoronalcells
AT mannil developmentalsignaturesynapticconnectivityandneurotransmissionareconservedbetweenvertebratehaircellsandtunicatecoronalcells