Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.

All vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative...

Full description

Bibliographic Details
Main Authors: Beatriz Albuixech-Crespo, Laura López-Blanch, Demian Burguera, Ignacio Maeso, Luisa Sánchez-Arrones, Juan Antonio Moreno-Bravo, Ildiko Somorjai, Juan Pascual-Anaya, Eduardo Puelles, Paola Bovolenta, Jordi Garcia-Fernàndez, Luis Puelles, Manuel Irimia, José Luis Ferran
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-04-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.2001573
_version_ 1818742505516040192
author Beatriz Albuixech-Crespo
Laura López-Blanch
Demian Burguera
Ignacio Maeso
Luisa Sánchez-Arrones
Juan Antonio Moreno-Bravo
Ildiko Somorjai
Juan Pascual-Anaya
Eduardo Puelles
Paola Bovolenta
Jordi Garcia-Fernàndez
Luis Puelles
Manuel Irimia
José Luis Ferran
author_facet Beatriz Albuixech-Crespo
Laura López-Blanch
Demian Burguera
Ignacio Maeso
Luisa Sánchez-Arrones
Juan Antonio Moreno-Bravo
Ildiko Somorjai
Juan Pascual-Anaya
Eduardo Puelles
Paola Bovolenta
Jordi Garcia-Fernàndez
Luis Puelles
Manuel Irimia
José Luis Ferran
author_sort Beatriz Albuixech-Crespo
collection DOAJ
description All vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative expression of 48 genes with key roles in vertebrate neural patterning in a representative amphioxus embryonic stage. Unlike nonchordates, amphioxus develops its central nervous system (CNS) from a neural plate that is homologous to that of vertebrates, allowing direct topological comparisons. The resulting genoarchitectonic model revealed that the amphioxus incipient neural tube is unexpectedly complex, consisting of several AP and DV molecular partitions. Strikingly, comparison with vertebrates indicates that the vertebrate thalamus, pretectum, and midbrain domains jointly correspond to a single amphioxus region, which we termed Di-Mesencephalic primordium (DiMes). This suggests that these domains have a common developmental and evolutionary origin, as supported by functional experiments manipulating secondary organizers in zebrafish and mice.
first_indexed 2024-12-18T02:13:35Z
format Article
id doaj.art-7c920c7df9a0457f8e9590b239f9c7ec
institution Directory Open Access Journal
issn 1544-9173
1545-7885
language English
last_indexed 2024-12-18T02:13:35Z
publishDate 2017-04-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj.art-7c920c7df9a0457f8e9590b239f9c7ec2022-12-21T21:24:27ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852017-04-01154e200157310.1371/journal.pbio.2001573Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.Beatriz Albuixech-CrespoLaura López-BlanchDemian BurgueraIgnacio MaesoLuisa Sánchez-ArronesJuan Antonio Moreno-BravoIldiko SomorjaiJuan Pascual-AnayaEduardo PuellesPaola BovolentaJordi Garcia-FernàndezLuis PuellesManuel IrimiaJosé Luis FerranAll vertebrate brains develop following a common Bauplan defined by anteroposterior (AP) and dorsoventral (DV) subdivisions, characterized by largely conserved differential expression of gene markers. However, it is still unclear how this Bauplan originated during evolution. We studied the relative expression of 48 genes with key roles in vertebrate neural patterning in a representative amphioxus embryonic stage. Unlike nonchordates, amphioxus develops its central nervous system (CNS) from a neural plate that is homologous to that of vertebrates, allowing direct topological comparisons. The resulting genoarchitectonic model revealed that the amphioxus incipient neural tube is unexpectedly complex, consisting of several AP and DV molecular partitions. Strikingly, comparison with vertebrates indicates that the vertebrate thalamus, pretectum, and midbrain domains jointly correspond to a single amphioxus region, which we termed Di-Mesencephalic primordium (DiMes). This suggests that these domains have a common developmental and evolutionary origin, as supported by functional experiments manipulating secondary organizers in zebrafish and mice.https://doi.org/10.1371/journal.pbio.2001573
spellingShingle Beatriz Albuixech-Crespo
Laura López-Blanch
Demian Burguera
Ignacio Maeso
Luisa Sánchez-Arrones
Juan Antonio Moreno-Bravo
Ildiko Somorjai
Juan Pascual-Anaya
Eduardo Puelles
Paola Bovolenta
Jordi Garcia-Fernàndez
Luis Puelles
Manuel Irimia
José Luis Ferran
Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
PLoS Biology
title Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
title_full Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
title_fullStr Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
title_full_unstemmed Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
title_short Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain.
title_sort molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain
url https://doi.org/10.1371/journal.pbio.2001573
work_keys_str_mv AT beatrizalbuixechcrespo molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT lauralopezblanch molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT demianburguera molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT ignaciomaeso molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT luisasanchezarrones molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT juanantoniomorenobravo molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT ildikosomorjai molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT juanpascualanaya molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT eduardopuelles molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT paolabovolenta molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT jordigarciafernandez molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT luispuelles molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT manuelirimia molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain
AT joseluisferran molecularregionalizationofthedevelopingamphioxusneuraltubechallengesmajorpartitionsofthevertebratebrain