Analysis of a shark reveals ancient, Wnt-dependent, habenular asymmetries in vertebrates
Year: 2024
Type: article
Abstract: The mode of evolution of left-right asymmetries in the vertebrate habenulae remains largely unknown. Using a transcriptomic approach, we show that in a cartilaginous fish, the catshark Scyliorhinus canicula, habenulae exhibit marked asymmetries, in both their medial and lateral components. Comparisons across vertebrates suggest that those identified in lateral habenulae reflect an ancestral gnathostome trait, partially conserved in lampreys, and independently lost in tetrapods and neopterygians. Asymmetry formation involves distinct mechanisms in the catshark lateral and medial habenulae. Medial habenulae are submitted to a marked, asymmetric temporal regulation of neurogenesis, undetectable in their lateral counterparts. Conversely, asymmetry formation in lateral habenulae results from asymmetric choices of neuronal identity in post-mitotic progenitors, a regulation dependent on the repression of Wnt signaling by Nodal on the left. Based on comparisons with the mouse and the zebrafish, we propose that habenular asymmetry formation involves a recurrent developmental logic across vertebrates, which relies on conserved, temporally regulated genetic programs sequentially shaping choices of neuronal identity on both sides and asymmetrically modified by Wnt activity.
Source: Nature Communications
Authors: Maxence Lanoizelet, Léo Michel, Ronan Lagadec, Hélène Mayeur, Lucile Guichard, Valentin Logeux, Dany Séverac, Kyle Martin, Christophe Klopp, Sylvain Marcellini, Héctor Castillo, Nicolas Pollet, Eva Candal, Mélanie Debiais-Thibaud, Catherine Boisvert, Bernard Billoud, Michael Schubert, Patrick Blader, Sylvie Mazan
Institutions: Centre National de la Recherche Scientifique, Sorbonne Université, Biologie Intégrative des Organismes Marins, Observatoire Océanologique de Banyuls-sur-Mer, Inserm, Université de Montpellier, Montpellier GenomiX, Biotechnology and Biological Sciences Research Council, UK Research and Innovation, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Genotoul coordination, University of Concepción, Université Paris-Saclay, Évolution, Génomes, Comportement, Écologie, Institut de Recherche pour le Développement, Universidade de Santiago de Compostela, École Pratique des Hautes Études, Institut des Sciences de l'Evolution de Montpellier, Curtin University, Station Biologique de Roscoff, Laboratoire de Biologie Intégrative des Modèles Marins, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche, Université Toulouse III - Paul Sabatier, Université de Toulouse, Centre de Biologie Intégrative de Toulouse
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: gold
Estimated APC paid: $6,790
Funder: Agence Nationale de la Recherche
OpenAlex ID: W4404667649