Gain of gene regulatory network interconnectivity at the origin of vertebrates - Archive ouverte HAL Accéder directement au contenu
Article Dans Une Revue Proceedings of the National Academy of Sciences of the United States of America Année : 2022

Gain of gene regulatory network interconnectivity at the origin of vertebrates

Alejandro Gil-Gálvez
  • Fonction : Auteur
Sandra Jiménez-Gancedo
  • Fonction : Auteur
Alberto Pérez-Posada
  • Fonction : Auteur
Martin Franke
  • Fonction : Auteur
Rafael Acemel
  • Fonction : Auteur
Che-Yi Lin
  • Fonction : Auteur
Cindy Chou
  • Fonction : Auteur
Yi-Hsien Su
  • Fonction : Auteur
Jr-Kai Yu
  • Fonction : Auteur
Juan Tena
  • Fonction : Auteur
José Luis Gómez-Skarmeta
  • Fonction : Auteur

Résumé

Signaling pathways control a large number of gene regulatory networks (GRNs) during animal development, acting as major tools for body plan formation [A. Pires-daSilva, R. J. Sommer, Nat. Rev. Genet. 4, 39–49 (2003)], although only a few of these pathways operate during this period [J. J. Sanz-Ezquerro, A. E. M€unsterberg, S. Stricker, Front. Cell Dev. Biol. 5, 76 (2017)]. Moreover, most of them have been largely conserved during metazoan evolution [L. S. Babonis, M. Q. Martindale, Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20150477 (2017)]. How evolution has generated a vast diversity of animal morphologies with such a limited number of tools is still largely unknown. Here, we show that gain of interconnectivity between signaling pathways and the GRNs they control may have critically contributed to the origin of vertebrates. We perturbed the retinoic acid, Wnt, FGF, and Nodal signaling pathways during gastrulation in the invertebrate chordate amphioxus and zebrafish and compared the effects on gene expression and cis-regulatory elements (CREs). We found that multiple developmental genes gain response to these pathways through vertebrate-specific CREs. Moreover, in contrast to amphioxus, many of these CREs responded to multiple pathways in zebrafish, which reflects their high interconnectivity. Furthermore, we found that vertebrate-specific cell types are more enriched in highly interconnected genes than in tissues with more ancient origin. Thus, the increase of CREs in vertebrates integrating inputs from different signaling pathways probably contributed to gene expression complexity and to the formation of new cell types and morphological novelties in this lineage.
Fichier principal
Vignette du fichier
pnas.202114802 (1).pdf (1.49 Mo) Télécharger le fichier
Origine : Fichiers éditeurs autorisés sur une archive ouverte

Dates et versions

hal-03007547 , version 1 (04-11-2021)
hal-03007547 , version 2 (09-11-2022)

Identifiants

Citer

Alejandro Gil-Gálvez, Sandra Jiménez-Gancedo, Alberto Pérez-Posada, Martin Franke, Rafael Acemel, et al.. Gain of gene regulatory network interconnectivity at the origin of vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 2022, 119 (1), ⟨10.1073/pnas.2114802119⟩. ⟨hal-03007547v2⟩
66 Consultations
122 Téléchargements

Altmetric

Partager

Gmail Facebook X LinkedIn More