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ORIGINAL RESEARCH article

Front. Cell Dev. Biol.
Sec. Embryonic Development
Volume 13 - 2025 | doi: 10.3389/fcell.2025.1528797
This article is part of the Research Topic Model Organisms in Embryonic Development View all 9 articles

The lamprey habenula provides an extreme example for the temporal regulation of asymmetric development

Provisionally accepted
Lucile Guichard Lucile Guichard 1Ronan Lagadec Ronan Lagadec 1Léo Michel Léo Michel 1,2Hélène Mayeur Hélène Mayeur 1MICHAËL FUENTES MICHAËL FUENTES 1Jordan Pain Jordan Pain 1Noah Heier Noah Heier 1Quentin Rougemont Quentin Rougemont 3Maria Celina Rodicio Maria Celina Rodicio 4Antón Barreiro-Iglesias Antón Barreiro-Iglesias 4,5Patrick Blader Patrick Blader 6Michael Schubert Michael Schubert 7Sylvie Mazan Sylvie Mazan 1*
  • 1 CNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls sur Mer, France
  • 2 The Department of Fundamental Neuroscience, The University of Lausanne, 1005 Lausanne, Switzerland, Lausanne, France
  • 3 Université Paris-Saclay, CNRS, AgroParisTech, Laboratoire Ecologie Systématique et Evolution, UMR 8079, Gif-sur-Yvette, France
  • 4 Departamento de Bioloxía Funcional, Facultade de Bioloxía, Universidade de Santiago de Compostela, 15782, Santiago de Compostela, Galicia, Spain
  • 5 Aquatic One Health Research Center (ARCUS), Universidade de Santiago de Compostela, 15782, Santiago de Compostela, Spain
  • 6 Molecular, Cellular and Developmental Biology (MCD, UMR5077), Centre de Biologie Intégrative (CBI, FR3743), Université de Toulouse, CNRS, UPS, Toulouse, France
  • 7 Laboratoire de Biologie du Développement de Villefranche-sur-Mer, Institut de la Mer de Villefranche, Sorbonne Université, CNRS, Villefranche-sur-Mer, France

The final, formatted version of the article will be published soon.

    By their phylogenetic position and their marked epithalamic asymmetries, lampreys are relevant models for understanding the formation and evolution of this trait across vertebrates. In this study, we use a transcriptomic approach to identify novel signature markers to characterize the highly asymmetric, bipartite organization of habenulae in lampreys. Lamprey habenulae are subdivided into two complementary subdomains related, respectively, to the lateral/ventral and the medial/dorsal habenulae of jawed vertebrates: a dorsal, right-restricted subdomain and a bilateral subdomain that includes the left habenula as well as its ventral right counterpart. Analysis of the formation of the lamprey habenula at prolarval and larval stages using a combination of morphological, immunohistochemical, and in situ hybridization approaches highlights a marked asymmetric temporal regulation. The dorsal right subdomain forms and already expresses all identified signature markers in prolarval stages. In contrast, the left and ventral right subdomain appears significantly later, with the first indication of neuronal identity elaboration in these territories being observed in larval stages. As in gnathostomes, Wnt signaling may be involved in the regulation of this unique, asymmetric mode of development, since b-catenin shows asymmetric and highly dynamic nuclear distributions both in neural progenitors and differentiated neuronal precursors of the two habenular subdomains. These data confirm the importance of lampreys to unravel the developmental logic underlying the recurrence and variation of habenular asymmetries in vertebrates and pave the way for future functional analyses

    Keywords: Habenula, asymmetry, Lamprey, Temporal regulation, Wnt signaling

    Received: 15 Nov 2024; Accepted: 20 Jan 2025.

    Copyright: © 2025 Guichard, Lagadec, Michel, Mayeur, FUENTES, Pain, Heier, Rougemont, Rodicio, Barreiro-Iglesias, Blader, Schubert and Mazan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence: Sylvie Mazan, CNRS, Sorbonne Université, UMR7232-Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique, Banyuls sur Mer, France

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