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Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution

BACKGROUND: Understanding the drivers of morphological diversity is a persistent challenge in evolutionary biology. Here, we investigate functional diversification of secretory cells in the sea anemone Nematostella vectensis to understand the mechanisms promoting cellular specialization across anima...

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Autores principales: Babonis, Leslie S., Ryan, Joseph F., Enjolras, Camille, Martindale, Mark Q.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6767649/
https://www.ncbi.nlm.nih.gov/pubmed/31583070
http://dx.doi.org/10.1186/s13227-019-0138-1
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author Babonis, Leslie S.
Ryan, Joseph F.
Enjolras, Camille
Martindale, Mark Q.
author_facet Babonis, Leslie S.
Ryan, Joseph F.
Enjolras, Camille
Martindale, Mark Q.
author_sort Babonis, Leslie S.
collection PubMed
description BACKGROUND: Understanding the drivers of morphological diversity is a persistent challenge in evolutionary biology. Here, we investigate functional diversification of secretory cells in the sea anemone Nematostella vectensis to understand the mechanisms promoting cellular specialization across animals. RESULTS: We demonstrate regionalized expression of gland cell subtypes in the internal ectoderm of N. vectensis and show that adult gland cell identity is acquired very early in development. A phylogenetic survey of trypsins across animals suggests that this gene family has undergone numerous expansions. We reveal unexpected diversity in trypsin protein structure and show that trypsin diversity arose through independent acquisitions of non-trypsin domains. Finally, we show that trypsin diversification in N. vectensis was effected through a combination of tandem duplication, exon shuffling, and retrotransposition. CONCLUSIONS: Together, these results reveal the numerous evolutionary mechanisms that drove trypsin duplication and divergence during the morphological specialization of cell types and suggest that the secretory cell phenotype is highly adaptable as a vehicle for novel secretory products.
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spelling pubmed-67676492019-10-03 Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution Babonis, Leslie S. Ryan, Joseph F. Enjolras, Camille Martindale, Mark Q. EvoDevo Research BACKGROUND: Understanding the drivers of morphological diversity is a persistent challenge in evolutionary biology. Here, we investigate functional diversification of secretory cells in the sea anemone Nematostella vectensis to understand the mechanisms promoting cellular specialization across animals. RESULTS: We demonstrate regionalized expression of gland cell subtypes in the internal ectoderm of N. vectensis and show that adult gland cell identity is acquired very early in development. A phylogenetic survey of trypsins across animals suggests that this gene family has undergone numerous expansions. We reveal unexpected diversity in trypsin protein structure and show that trypsin diversity arose through independent acquisitions of non-trypsin domains. Finally, we show that trypsin diversification in N. vectensis was effected through a combination of tandem duplication, exon shuffling, and retrotransposition. CONCLUSIONS: Together, these results reveal the numerous evolutionary mechanisms that drove trypsin duplication and divergence during the morphological specialization of cell types and suggest that the secretory cell phenotype is highly adaptable as a vehicle for novel secretory products. BioMed Central 2019-09-30 /pmc/articles/PMC6767649/ /pubmed/31583070 http://dx.doi.org/10.1186/s13227-019-0138-1 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Babonis, Leslie S.
Ryan, Joseph F.
Enjolras, Camille
Martindale, Mark Q.
Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title_full Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title_fullStr Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title_full_unstemmed Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title_short Genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
title_sort genomic analysis of the tryptome reveals molecular mechanisms of gland cell evolution
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6767649/
https://www.ncbi.nlm.nih.gov/pubmed/31583070
http://dx.doi.org/10.1186/s13227-019-0138-1
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