The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates

<p>Abstract</p> <p>Background</p> <p>The increasing number of available genomic sequences makes it now possible to study the evolutionary history of specific genes or gene families. Transcription factors (TFs) involved in regulation of gene-specific expression are key p...

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Main Authors: Mazan Sylvie, Plouhinec Jean-Louis, Mella Sébastien, Daburon Virginie, Crozatier Michèle, Vincent Alain
Format: Article
Language:English
Published: BMC 2008-05-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/8/131
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author Mazan Sylvie
Plouhinec Jean-Louis
Mella Sébastien
Daburon Virginie
Crozatier Michèle
Vincent Alain
author_facet Mazan Sylvie
Plouhinec Jean-Louis
Mella Sébastien
Daburon Virginie
Crozatier Michèle
Vincent Alain
author_sort Mazan Sylvie
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The increasing number of available genomic sequences makes it now possible to study the evolutionary history of specific genes or gene families. Transcription factors (TFs) involved in regulation of gene-specific expression are key players in the evolution of metazoan development. The low complexity COE (Collier/Olfactory-1/Early B-Cell Factor) family of transcription factors constitutes a well-suited paradigm for studying evolution of TF structure and function, including the specific question of protein modularity. Here, we compare the structure of <it>coe </it>genes within the metazoan kingdom and report on the mechanism behind a vertebrate-specific exon duplication.</p> <p>Results</p> <p>COE proteins display a modular organisation, with three highly conserved domains : a COE-specific DNA-binding domain (DBD), an Immunoglobulin/Plexin/transcription (IPT) domain and an atypical Helix-Loop-Helix (HLH) motif. Comparison of the splice structure of <it>coe </it>genes between cnidariae and bilateriae shows that the ancestral COE DBD was built from 7 separate exons, with no evidence for exon shuffling with other metazoan gene families. It also confirms the presence of an ancestral H1LH2 motif present in all COE proteins which partly overlaps the repeated H2d-H2a motif first identified in rodent EBF. Electrophoretic Mobility Shift Assays show that formation of COE dimers is mediated by this ancestral motif. The H2d-H2a α-helical repetition appears to be a vertebrate characteristic that originated from a tandem exon duplication having taken place prior to the splitting between gnathostomes and cyclostomes. We put-forward a two-step model for the inclusion of this exon in the vertebrate transcripts.</p> <p>Conclusion</p> <p>Three main features in the history of the <it>coe </it>gene family can be inferred from these analyses: (i) each conserved domain of the ancestral <it>coe </it>gene was built from multiple exons and the same scattered structure has been maintained throughout metazoan evolution. (ii) There exists a single <it>coe </it>gene copy per metazoan genome except in vertebrates. The H2a-H2d duplication that is specific to vertebrate proteins provides an example of a novel vertebrate characteristic, which may have been fixed early in the gnathostome lineage. (iii) This duplication provides an interesting example of counter-selection of alternative splicing.</p>
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spelling doaj.art-96df73f324ff4fd8a39ce18a4eaac1dd2022-12-21T23:12:43ZengBMCBMC Evolutionary Biology1471-21482008-05-018113110.1186/1471-2148-8-131The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebratesMazan SylviePlouhinec Jean-LouisMella SébastienDaburon VirginieCrozatier MichèleVincent Alain<p>Abstract</p> <p>Background</p> <p>The increasing number of available genomic sequences makes it now possible to study the evolutionary history of specific genes or gene families. Transcription factors (TFs) involved in regulation of gene-specific expression are key players in the evolution of metazoan development. The low complexity COE (Collier/Olfactory-1/Early B-Cell Factor) family of transcription factors constitutes a well-suited paradigm for studying evolution of TF structure and function, including the specific question of protein modularity. Here, we compare the structure of <it>coe </it>genes within the metazoan kingdom and report on the mechanism behind a vertebrate-specific exon duplication.</p> <p>Results</p> <p>COE proteins display a modular organisation, with three highly conserved domains : a COE-specific DNA-binding domain (DBD), an Immunoglobulin/Plexin/transcription (IPT) domain and an atypical Helix-Loop-Helix (HLH) motif. Comparison of the splice structure of <it>coe </it>genes between cnidariae and bilateriae shows that the ancestral COE DBD was built from 7 separate exons, with no evidence for exon shuffling with other metazoan gene families. It also confirms the presence of an ancestral H1LH2 motif present in all COE proteins which partly overlaps the repeated H2d-H2a motif first identified in rodent EBF. Electrophoretic Mobility Shift Assays show that formation of COE dimers is mediated by this ancestral motif. The H2d-H2a α-helical repetition appears to be a vertebrate characteristic that originated from a tandem exon duplication having taken place prior to the splitting between gnathostomes and cyclostomes. We put-forward a two-step model for the inclusion of this exon in the vertebrate transcripts.</p> <p>Conclusion</p> <p>Three main features in the history of the <it>coe </it>gene family can be inferred from these analyses: (i) each conserved domain of the ancestral <it>coe </it>gene was built from multiple exons and the same scattered structure has been maintained throughout metazoan evolution. (ii) There exists a single <it>coe </it>gene copy per metazoan genome except in vertebrates. The H2a-H2d duplication that is specific to vertebrate proteins provides an example of a novel vertebrate characteristic, which may have been fixed early in the gnathostome lineage. (iii) This duplication provides an interesting example of counter-selection of alternative splicing.</p>http://www.biomedcentral.com/1471-2148/8/131
spellingShingle Mazan Sylvie
Plouhinec Jean-Louis
Mella Sébastien
Daburon Virginie
Crozatier Michèle
Vincent Alain
The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
BMC Evolutionary Biology
title The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
title_full The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
title_fullStr The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
title_full_unstemmed The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
title_short The metazoan history of the COE transcription factors. Selection of a variant HLH motif by mandatory inclusion of a duplicated exon in vertebrates
title_sort metazoan history of the coe transcription factors selection of a variant hlh motif by mandatory inclusion of a duplicated exon in vertebrates
url http://www.biomedcentral.com/1471-2148/8/131
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