New genomic data and analyses challenge the traditional vision of animal epithelium evolution
Abstract Background The emergence of epithelia was the foundation of metazoan expansion. Epithelial tissues are a hallmark of metazoans deeply rooted in the evolution of their complex developmental morphogenesis processes. However, studies on the epithelial features of non-bilaterians are still spar...
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| Format: | Article |
| Language: | English |
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BMC
2018-05-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4715-9 |
| _version_ | 1819038524052078592 |
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| author | Hassiba Belahbib Emmanuelle Renard Sébastien Santini Cyril Jourda Jean-Michel Claverie Carole Borchiellini André Le Bivic |
| author_facet | Hassiba Belahbib Emmanuelle Renard Sébastien Santini Cyril Jourda Jean-Michel Claverie Carole Borchiellini André Le Bivic |
| author_sort | Hassiba Belahbib |
| collection | DOAJ |
| description | Abstract Background The emergence of epithelia was the foundation of metazoan expansion. Epithelial tissues are a hallmark of metazoans deeply rooted in the evolution of their complex developmental morphogenesis processes. However, studies on the epithelial features of non-bilaterians are still sparse and it remains unclear whether the last common metazoan ancestor possessed a fully functional epithelial toolkit or if it was acquired later during metazoan evolution. Results To investigate the early evolution of animal epithelia, we sequenced the genome and transcriptomes of two new sponge species to characterize epithelial markers such as the E-cadherin complex and the polarity complexes for all classes (Calcarea, Demospongiae, Hexactinellida, Homoscleromorpha) of sponges (phylum Porifera) and compare them with their homologues in Placozoa and in Ctenophora. We found that Placozoa and most sponges possess orthologues of all essential genes encoding proteins characteristic of bilaterian epithelial cells, as well as their conserved interaction domains. In stark contrast, we found that ctenophores lack several major polarity complex components such as the Crumbs complex and Scribble. Furthermore, the E-cadherin ctenophore orthologue exhibits a divergent cytoplasmic domain making it unlikely to interact with its canonical cytoplasmic partners. Conclusions These unexpected findings challenge the current evolutionary paradigm on the emergence of epithelia. Altogether, our results raise doubt on the homology of protein complexes and structures involved in cell polarity and adhesive-type junctions between Ctenophora and Bilateria epithelia. |
| first_indexed | 2024-12-21T08:38:40Z |
| format | Article |
| id | doaj.art-70e1bf3e2c844b5d804313d35b7f8f97 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-21T08:38:40Z |
| publishDate | 2018-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-70e1bf3e2c844b5d804313d35b7f8f972022-12-21T19:10:01ZengBMCBMC Genomics1471-21642018-05-0119111510.1186/s12864-018-4715-9New genomic data and analyses challenge the traditional vision of animal epithelium evolutionHassiba Belahbib0Emmanuelle Renard1Sébastien Santini2Cyril Jourda3Jean-Michel Claverie4Carole Borchiellini5André Le Bivic6Structural and Genomic Information Laboratory, Aix-Marseille Université & CNRS UMR 7256, Mediterranean Institute of Microbiology (IMM FR 3479)Aix Marseille Univ, Univ Avignon, CNRS, IRD, UMR 7263, Mediterranean Institute of Marine and Continental Biodiversity and Ecology (IMBE), Station Marine d’EndoumeStructural and Genomic Information Laboratory, Aix-Marseille Université & CNRS UMR 7256, Mediterranean Institute of Microbiology (IMM FR 3479)Structural and Genomic Information Laboratory, Aix-Marseille Université & CNRS UMR 7256, Mediterranean Institute of Microbiology (IMM FR 3479)Structural and Genomic Information Laboratory, Aix-Marseille Université & CNRS UMR 7256, Mediterranean Institute of Microbiology (IMM FR 3479)Aix Marseille Univ, Univ Avignon, CNRS, IRD, UMR 7263, Mediterranean Institute of Marine and Continental Biodiversity and Ecology (IMBE), Station Marine d’EndoumeAix-Marseille University, CNRS, UMR 7288, Developmental Biology Institute of Marseille Luminy (IBDM)Abstract Background The emergence of epithelia was the foundation of metazoan expansion. Epithelial tissues are a hallmark of metazoans deeply rooted in the evolution of their complex developmental morphogenesis processes. However, studies on the epithelial features of non-bilaterians are still sparse and it remains unclear whether the last common metazoan ancestor possessed a fully functional epithelial toolkit or if it was acquired later during metazoan evolution. Results To investigate the early evolution of animal epithelia, we sequenced the genome and transcriptomes of two new sponge species to characterize epithelial markers such as the E-cadherin complex and the polarity complexes for all classes (Calcarea, Demospongiae, Hexactinellida, Homoscleromorpha) of sponges (phylum Porifera) and compare them with their homologues in Placozoa and in Ctenophora. We found that Placozoa and most sponges possess orthologues of all essential genes encoding proteins characteristic of bilaterian epithelial cells, as well as their conserved interaction domains. In stark contrast, we found that ctenophores lack several major polarity complex components such as the Crumbs complex and Scribble. Furthermore, the E-cadherin ctenophore orthologue exhibits a divergent cytoplasmic domain making it unlikely to interact with its canonical cytoplasmic partners. Conclusions These unexpected findings challenge the current evolutionary paradigm on the emergence of epithelia. Altogether, our results raise doubt on the homology of protein complexes and structures involved in cell polarity and adhesive-type junctions between Ctenophora and Bilateria epithelia.http://link.springer.com/article/10.1186/s12864-018-4715-9Epithelium evolutionNon-bilaterian animalsCell polarityCell-cell junctions |
| spellingShingle | Hassiba Belahbib Emmanuelle Renard Sébastien Santini Cyril Jourda Jean-Michel Claverie Carole Borchiellini André Le Bivic New genomic data and analyses challenge the traditional vision of animal epithelium evolution BMC Genomics Epithelium evolution Non-bilaterian animals Cell polarity Cell-cell junctions |
| title | New genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| title_full | New genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| title_fullStr | New genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| title_full_unstemmed | New genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| title_short | New genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| title_sort | new genomic data and analyses challenge the traditional vision of animal epithelium evolution |
| topic | Epithelium evolution Non-bilaterian animals Cell polarity Cell-cell junctions |
| url | http://link.springer.com/article/10.1186/s12864-018-4715-9 |
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