A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg


Por: Bourbon H.-M.G., BenetahID, Mikhail H., GuillouID, Emmanuelle, Mojica-Vazquez, Luis Humberto, Baanannou, Aissette, Bernat-Fabre, Sandra, Loubiere, Vincent, Bantignies, Frederic, Cavalli, Giacomo, Boube, Muriel

Publicada: 1 mar 2022
Resumen:
Gene duplications and transcriptional enhancer emergence/modifications are thought having greatly contributed to phenotypic innovations during animal evolution. Nevertheless, little is known about how enhancers evolve after gene duplication and how regulatory information is rewired between duplicated genes. The Drosophila melanogaster bric-a-brac (bab) complex, comprising the tandem paralogous genes bab1 and bab2, provides a paradigm to address these issues. We previously characterized an intergenic enhancer (named LAE) regulating bab2 expression in the developing legs. We show here that bab2 regulators binding directly the LAE also govern bab1 expression in tarsal cells. LAE excision by CRISPR/ Cas9-mediated genome editing reveals that this enhancer appears involved but not strictly required for bab1 and bab2 co-expression in leg tissues. Instead, the LAE enhancer is critical for paralog-specific bab2 expression along the proximo-distal leg axis. Chromatin features and phenotypic rescue experiments indicate that LAE functions partly redundantly with leg-specific regulatory information overlapping the bab1 transcription unit. Phylogenomics analyses indicate that (i) the bab complex originates from duplication of an ancestral singleton gene early on within the Cyclorrhapha dipteran sublineage, and (ii) LAE sequences have been evolutionarily-fixed early on within the Brachycera suborder thus predating the gene duplication event. This work provides new insights on enhancers, particularly about their emergence, maintenance and functional diversification during evolution.

Filiaciones:
Bourbon H.-M.G.:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

BenetahID, Mikhail H.:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

GuillouID, Emmanuelle:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

Mojica-Vazquez, Luis Humberto:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

Baanannou, Aissette:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

Bernat-Fabre, Sandra:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France

Loubiere, Vincent:
 Institute of Human Genetics, University of Montpellier, CNRS Montpellier, France

Bantignies, Frederic:
 Institute of Human Genetics, University of Montpellier, CNRS Montpellier, France

Cavalli, Giacomo:
 Institute of Human Genetics, University of Montpellier, CNRS Montpellier, France

Boube, Muriel:
 Center for Integrative Biology, Molecular Cellular and Developmental (MCD) Biology Unit, Federal University of Toulouse, Toulouse, France
ISSN: 15537390





PLOS GENETICS
Editorial
PUBLIC LIBRARY SCIENCE, 185 BERRY ST, STE 1300, SAN FRANCISCO, CA 94107 USA, Estados Unidos America
Tipo de documento: Article
Volumen: 18 Número: 3
Páginas:
WOS Id: 001044173500001
ID de PubMed: 35294439
imagen gold, Green Published, Gold, Green

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