Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution
Body axis specification is a crucial event in animal embryogenesis and was an essential evolutionary innovation for founding the animal kingdom. This process involves two distinct components that coordinate to establish the spatial organisation of the embryo: initiation of cascades of regionalised g...
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| Format: | Article |
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eLife Sciences Publications Ltd
2025-07-01
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| Online Access: | https://elifesciences.org/articles/104508 |
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| author | Julie Uveira Antoine Donati Marvin Léria Marion Lechable François Lahaye Christine Vesque Evelyn Houliston Tsuyoshi Momose |
| author_facet | Julie Uveira Antoine Donati Marvin Léria Marion Lechable François Lahaye Christine Vesque Evelyn Houliston Tsuyoshi Momose |
| author_sort | Julie Uveira |
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| description | Body axis specification is a crucial event in animal embryogenesis and was an essential evolutionary innovation for founding the animal kingdom. This process involves two distinct components that coordinate to establish the spatial organisation of the embryo: initiation of cascades of regionalised gene expression and orientation of morphogenetic processes such as body elongation. Intense interest in the first component has revealed Wnt/β-catenin signalling as ancestrally responsible for initiating regional gene expression, but the evolutionary origin of oriented morphogenesis has received little attention. Here, by addressing the cell and morphological basis of body axis development in embryos of the cnidarian Clytia hemisphaerica, we have uncovered a simple and likely ancestral coordination mechanism between Wnt/β-catenin signalling and directed morphogenesis. We show that the ligand Wnt3, known to initiate oral gene expression via localised Wnt/β-catenin pathway activation, also has a key β-catenin-independent role in globally orienting planar cell polarity (PCP) to direct morphogenesis along the oral-aboral axis. This PCP orientation occurs in two distinct steps: local orientation by Wnt3 and global propagation by conserved core PCP protein interactions along the body axis. From these findings, we propose novel scenarios for PCP-driven symmetry-breaking underlying the emergence of the animal body plan. |
| format | Article |
| id | doaj-art-ac8e2dcc4c264916a3ca93caab65b6b8 |
| institution | OA Journals |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-07-01 |
| publisher | eLife Sciences Publications Ltd |
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| spelling | doaj-art-ac8e2dcc4c264916a3ca93caab65b6b82025-08-20T02:37:30ZengeLife Sciences Publications LtdeLife2050-084X2025-07-011410.7554/eLife.104508Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolutionJulie Uveira0Antoine Donati1https://orcid.org/0000-0002-3616-3915Marvin Léria2https://orcid.org/0009-0006-5287-4123Marion Lechable3https://orcid.org/0009-0000-5307-7608François Lahaye4Christine Vesque5https://orcid.org/0000-0001-7983-4953Evelyn Houliston6https://orcid.org/0000-0001-9264-2585Tsuyoshi Momose7https://orcid.org/0000-0002-3806-3408Sorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceSorbonne Université, CNRS UMR7622, INSERM U1156, Institut de Biologie ParisSeine (IBPS)-Developmental Biology Unit, Paris, FranceSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceSorbonne Université, CNRS UMR7622, INSERM U1156, Institut de Biologie ParisSeine (IBPS)-Developmental Biology Unit, Paris, FranceSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceSorbonne Université, CNRS, Laboratoire de Biologie du Développement de Villefranche-sur-mer (LBDV- UMR7009), Villefranche-sur-mer, FranceBody axis specification is a crucial event in animal embryogenesis and was an essential evolutionary innovation for founding the animal kingdom. This process involves two distinct components that coordinate to establish the spatial organisation of the embryo: initiation of cascades of regionalised gene expression and orientation of morphogenetic processes such as body elongation. Intense interest in the first component has revealed Wnt/β-catenin signalling as ancestrally responsible for initiating regional gene expression, but the evolutionary origin of oriented morphogenesis has received little attention. Here, by addressing the cell and morphological basis of body axis development in embryos of the cnidarian Clytia hemisphaerica, we have uncovered a simple and likely ancestral coordination mechanism between Wnt/β-catenin signalling and directed morphogenesis. We show that the ligand Wnt3, known to initiate oral gene expression via localised Wnt/β-catenin pathway activation, also has a key β-catenin-independent role in globally orienting planar cell polarity (PCP) to direct morphogenesis along the oral-aboral axis. This PCP orientation occurs in two distinct steps: local orientation by Wnt3 and global propagation by conserved core PCP protein interactions along the body axis. From these findings, we propose novel scenarios for PCP-driven symmetry-breaking underlying the emergence of the animal body plan.https://elifesciences.org/articles/104508planar cell polarityWntbasal bodyevolution |
| spellingShingle | Julie Uveira Antoine Donati Marvin Léria Marion Lechable François Lahaye Christine Vesque Evelyn Houliston Tsuyoshi Momose Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution eLife planar cell polarity Wnt basal body evolution |
| title | Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| title_full | Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| title_fullStr | Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| title_full_unstemmed | Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| title_short | Planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| title_sort | planar cell polarity coordination in a cnidarian embryo provides clues to animal body axis evolution |
| topic | planar cell polarity Wnt basal body evolution |
| url | https://elifesciences.org/articles/104508 |
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