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

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 duplicate...

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Autores principales: Bourbon, Henri-Marc G., Benetah, Mikhail H., Guillou, Emmanuelle, Mojica-Vazquez, Luis Humberto, Baanannou, Aissette, Bernat-Fabre, Sandra, Loubiere, Vincent, Bantignies, Frédéric, Cavalli, Giacomo, Boube, Muriel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8959175/
https://www.ncbi.nlm.nih.gov/pubmed/35294439
http://dx.doi.org/10.1371/journal.pgen.1010083
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author Bourbon, Henri-Marc G.
Benetah, Mikhail H.
Guillou, Emmanuelle
Mojica-Vazquez, Luis Humberto
Baanannou, Aissette
Bernat-Fabre, Sandra
Loubiere, Vincent
Bantignies, Frédéric
Cavalli, Giacomo
Boube, Muriel
author_facet Bourbon, Henri-Marc G.
Benetah, Mikhail H.
Guillou, Emmanuelle
Mojica-Vazquez, Luis Humberto
Baanannou, Aissette
Bernat-Fabre, Sandra
Loubiere, Vincent
Bantignies, Frédéric
Cavalli, Giacomo
Boube, Muriel
author_sort Bourbon, Henri-Marc G.
collection PubMed
description 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.
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spelling pubmed-89591752022-03-29 A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg Bourbon, Henri-Marc G. Benetah, Mikhail H. Guillou, Emmanuelle Mojica-Vazquez, Luis Humberto Baanannou, Aissette Bernat-Fabre, Sandra Loubiere, Vincent Bantignies, Frédéric Cavalli, Giacomo Boube, Muriel PLoS Genet Research Article 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. Public Library of Science 2022-03-16 /pmc/articles/PMC8959175/ /pubmed/35294439 http://dx.doi.org/10.1371/journal.pgen.1010083 Text en © 2022 Bourbon et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bourbon, Henri-Marc G.
Benetah, Mikhail H.
Guillou, Emmanuelle
Mojica-Vazquez, Luis Humberto
Baanannou, Aissette
Bernat-Fabre, Sandra
Loubiere, Vincent
Bantignies, Frédéric
Cavalli, Giacomo
Boube, Muriel
A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title_full A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title_fullStr A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title_full_unstemmed A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title_short A shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing Drosophila leg
title_sort shared ancient enhancer element differentially regulates the bric-a-brac tandem gene duplicates in the developing drosophila leg
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8959175/
https://www.ncbi.nlm.nih.gov/pubmed/35294439
http://dx.doi.org/10.1371/journal.pgen.1010083
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